Physiological basis of temperature-dependent biogeography: trade-offs in muscle design and performance in polar ectotherms
Alfred-Wegener-Institut für Polar- und Meeresforschung, Ökophysiologie, Postfach 12 01 61, D-27515 Bremerhaven, Germany
e-mail: hpoertner{at}awi-bremerhaven.de
Accepted 13 May 2002
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Summary |
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In contrast to the cold-adapted eurytherms of the Arctic, polar (especially Antarctic) stenotherms minimize standard metabolic rate and, as a precondition, the aerobic capacity per milligram of mitochondrial protein, thereby minimizing oxygen demand. Cost reductions are supported by the downregulation of the cost and flexibility of acidbase regulation. At maintained factorial scopes, the reduction in standard metabolic rate will cause net aerobic scope to be lower than in temperate species. Loss of contractile myofilaments and, thereby, force results from space constraints due to excessive mitochondrial proliferation. On a continuum between low and moderately high levels of muscular activity, polar fish have developed characteristics of aerobic metabolism equivalent to those of high-performance swimmers in warmer waters. However, they only reach low performance levels despite taking aerobic design to an extreme.
Key words: polar, ectotherm, thermal tolerance, muscle, performance, oxygen availability, temperature
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Thermal tolerance and muscular performance |
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The present analysis was undertaken to demonstrate that the currently
emerging unifying picture of an oxygen limitation of thermal tolerance in
animals (Pörtner, 2001,
2002a
) helps to develop our
knowledge of muscle function at various temperatures towards a whole-animal
understanding. The comparisons of polar (especially Antarctic) stenotherms
with eurytherms (temperate and Arctic) and even endotherms is appropriate for
testing some of the hypotheses developed. Because of the many gaps in our
understanding of the trade-offs involved in adaptation to various climates and
temperature regimes in a latitudinal cline (see
Pörtner et al., 2000
;
Pörtner, 2001
,
2002a
), this review must
necessarily remain conceptual, and the hypothetical relationships proposed
should contribute to ideas for future experimental work.
Recent work carried out in marine invertebrates and fish has demonstrated
that, in accordance with Shelford's law of tolerance, the onset of a decrease
in whole-animal aerobic scope characterises thermal limitation at low and high
pejus thresholds (Tp, pejus=getting worse) (see
Frederich and Pörtner,
2000; Pörtner,
2001
). Towards temperature extremes, the decrease in aerobic scope
is indicated by falling oxygen levels in the body fluids and by the
progressive limitation of the functional capacity of circulatory and
ventilatory systems to ensure oxygen supply. According to a previous model
(Pörtner et al., 2000
;
Pörtner, 2001
), the
aerobic capacity of muscle mitochondria may become limiting for ventilation
and circulation at low temperatures, whereas at high temperatures, excessive
oxygen demand causes an uncompensated decrease in oxygen levels in the body
fluids. Further cooling or warming beyond pejus limits leads to low or high
critical threshold temperatures (Tc) at which aerobic
scope disappears and the transition to an anaerobic mode of mitochondrial
metabolism and a progressive decline in cellular energy levels occur
(Pörtner et al., 2000
;
Pörtner, 2001
)
(Fig. 1).
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At extreme temperatures, oxygen limitation will contribute to oxidative
stress and, eventually, to the denaturation of molecular functions.
Time-limited passive survival is supported by anaerobic metabolism or by the
protection of molecular functions by heat-shock proteins and antioxidative
defences. In accordance with a hierarchy of thermal tolerance ranging from the
systemic to the cellular and molecular levels, capacity limitations at a high
level of organisational complexity, i.e. the integrated function of the oxygen
delivery system, define the onset of thermal limitation, which then transfers
to lower hierarchical levels and contributes to cellular and molecular
disturbances (for reviews, see Pörtner,
2001,
2002a
).
Thermal limits differ among ectothermic species depending on latitude or
seasonal temperature acclimatisation and are therefore related to geographical
distribution. The tolerance window is narrow, especially in polar areas, most
notably in the Southern Ocean. Nevertheless, despite constant water
temperatures between -1.9 and +1°C, this window is not the same for all
Antarctic species (for a review, see
Pörtner et al., 2000).
The capacities for ventilation and circulation are higher in mobile fish or
octopods than, for example, in sessile bivalves, and this probably relates to
the higher pejus (see above) and critical temperatures found in more mobile
compared with sessile epifauna species.
The finding of an oxygen-limited thermal tolerance is in line with the
concept of symmorphosis (Taylor and
Weibel, 1981), which implies that excess capacity of any component
of the oxygen delivery system is avoided in an evolutionary context. In the
context of thermal adaptation and limitation, this means that oxygen delivery
systems (and, possibly, other systems) are set to a minimum level of
functional capacity in the case of oxygen delivery, just sufficient to
meet maximum oxygen demand between the average highs and lows of environmental
temperatures. Accordingly, the processes and limits of thermal tolerance are
linked to the aerobic scope and aerobic capacity of the whole animal in
addition to parallel adjustments at the molecular or membrane levels. The
crucial mechanism(s) of thermal limitation and adaptation should link low and
high tolerance limits, i.e. changes occurring during acclimation to high
temperatures should reverse the processes involved in acclimation to low
temperature. Since thermal tolerance limits are probably set at the highest
levels of organismic complexity (Pörtner,
2001
,
2002a
), the crucial mechanisms
of temperature adaptation should be visible in all tissues supporting the
functional coordination of the organismic entity.
Following the treatment of thermal tolerance, adaptation to changing
temperatures involves escaping the threat of temperature-induced hypoxia
(Pörtner et al., 1998,
2000
;
Pörtner, 2001
).
Accordingly, thermal adaptation will also affect performance levels, which
depend on the maintenance of aerobic and, also, anaerobic scope. Performance
increases with temperature to a maximum and then decreases at higher
temperatures, yielding a species-specific bell-shaped curve that shifts
depending on thermal adaptation (Beamish,
1978
). The temperature of optimum performance is expected to
correspond to the preferred temperature of the fish, maximum performance
occurring when acclimation and exposure temperature are identical
(Beamish, 1978
;
Schurmann and Steffensen,
1997
). However, this can only be true within the thermal tolerance
window when full aerobic scope becomes available to the locomotory muscles
(see above). Accordingly, temperature-dependent performance limitations set in
at an organismic level, i.e. the capacity of circulatory and ventilatory
muscle tissues to support the take-up and provision of substrates and oxygen
to the tissues.
Taking this integrative view of thermal tolerance, low temperatures in
particular appear to be a major constraint limiting the scope of cellular
functional capacity, including muscular activity levels, with ultimate
consequences for lifestyle and population dynamics. As the narrowest tolerance
windows are found at low standard metabolic rates (SMRs) in Antarctic
stenotherms and correlate with a reduced aerobic scope for exercise, the
question arises of whether the elevated SMRs observed in cold-adapted
populations of eurythermic animals
(Pörtner et al., 2000)
will extend to cold-compensated metabolic scopes and activity levels. In this
context, the treatment of cold adjustments needs to consider not only the
physiology of stenotherms and eurytherms but also the various short-term to
evolutionary time scales involved; i.e. between seasonal cold acclimatisation
via cold adaptation in eurytherms at high latitudes (especially in
the Northern hemisphere) (see
Pörtner, 2001
) to
permanent cold adaptation in polar areas. Compared with Antarctic seas, the
much younger thermal history of Arctic fauna and the lesser degree of
isolation of the Arctic from adjacent seas require consideration. Accordingly,
species or species subpopulations (as in the case of the Atlantic cod
Gadus morhua) in the Arctic may still be found in transition to life
in the permanent cold, while those in the Antarctic have developed features of
permanent cold adaptation over millions of years.
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Temperature adaptation, aerobic scope and whole-animal performance |
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Although the rises in mitochondrial density and capacity in the cold are
probably cost-determined (Pörtner et
al., 2000; Pörtner,
2001
), the mechanistic stimulus for cold-induced mitochondrial
proliferation remains unclear because energy deficiency and hypoxia occur at
both ends of the thermal tolerance window and mitochondrial density decreases
during warm acclimation, thereby reducing the excessive oxygen demand
associated with excess mitochondrial capacity (see below). The key role of
mitochondria does not neglect that integrated modifications in lipid
saturation, kinetic properties of metabolic enzymes, contractile proteins and
transmembrane transporters are required to contribute to the optimization of
higher functions within the window of thermal tolerance (see
Johnston, 1990
;
Hazel, 1995
;
Storelli et al., 1998
;
Pörtner et al., 1998
).
These functions include the integration of muscular and nervous systems
operative in ventilation and circulation which maintain contractility and
contractile frequency such that aerobic scope is retained to support metabolic
flexibility and locomotor activity in the cold.
In addition to the cost of mitochondrial biosynthesis and degradation,
proton leakage accounts for the cost of mitochondrial maintenance
(Pörtner et al., 1998).
Mitochondrial proton leakage rates in the resting cell make up a consistently
large fraction of SMR in ecto- and endotherms, 25% of baseline metabolic rate
in rat hepatocytes, 50% in skeletal muscle and 20-30% in the whole animal
(Brand, 1990
;
Brand et al., 1994
;
Rolfe and Brand, 1996
;
Brookes et al., 1998
). Higher
mitochondrial densities as a consequence of cold adaptation should therefore
indicate elevated oxygen demand under resting conditions or cold-compensated
SMR and aerobic scope. This may not, however, be observed in polar stenotherms
(see below). Nonetheless, while enhancing mitochondrial capacity in the cold
eliminates the capacity limitations of ventilation and circulation, a
reduction in mitochondrial capacity in the warm reduces the oxygen demand of
mitochondrial maintenance, thereby allowing the upper Tc
to shift to higher values (see Pörtner,
2001
,
2002a
,
b
) and, as a trade-off,
leaving enough aerobic energy for ventilation and circulation to maintain
aerobic scope. These observations immediately suggest that mitochondria are
more efficient in the warm. They will then leave more cellular space for
enhancing contractile apparatus and, thus, capacity and performance levels
than is possible in the cold.
Metabolic scopes and performance in cold-acclimated versus
cold-adapted eurytherms
The questions frequently asked in this context are to what extent the
capacity of locomotory muscular activity is fully compensated in the cold and
whether it reaches as high as at warmer temperatures (for a general treatment
of the effects of temperature on muscular function in teleost fish, see
Sidell and Moerland, 1989). In
temperate-zone eurythermal fish, cold acclimation in goldfish and striped bass
(Fry and Hart, 1948
;
Rome et al., 1984
;
Sisson and Sidell, 1987
) does
not lead to complete compensation of performance levels since warm-acclimated
fish are able to maintain higher swimming speeds than cold-acclimated animals
at their respective acclimation temperature. The same conclusion is true for
Atlantic cod (Gadus morhua) from the North Sea: fish acclimated to 15
°C reached higher swimming speeds than at 5 °C
(Schurmann and Steffensen,
1997
). One reason may be reduced force generation per muscle
cross-sectional area (see Rome,
1995
) at cold temperature, which requires the recruitment of a
larger number of fibres for a similar power output to that in warm-acclimated
fish (for comparison, 1.5-2 times more fibres would be recruited in carp
Cyprinus carpio or scup Stenotomus chrysops to compensate
for a 10 °C fall in temperature) (see
Rome, 1995
). Recruitment of a
larger number of muscle fibres for the same performance level will contribute
to the enhanced expression of slow oxidative fibres in the cold (see
Sidell and Moerland, 1989
).
Nonetheless, using more fibres for the same power output indicates that
maximum limits are reached earlier than in warm waters causing, on average,
lower performance levels in cold- compared with warm-acclimated fish (see
above) (see Johnston and Altringham,
1985
; Johnston,
1989
; Sidell and Moerland,
1989
; Johnson and Johnston,
1991
; Johnson et al.,
1996
; Johnston and Ball,
1997
; Guderley,
1998
). For compensatory molecular changes involved, see Gauvry et
al. (2000
).
In the muscle of cold-acclimated eurytherms
(Guderley and Johnston, 1996;
Guderley, 1998
) or in
cold-adapted populations of eurytherms analysed during the summer at high
latitudes (Tschischka et al.,
2000
; Sommer and Pörtner,
2002
), both a rise in mitochondrial density and a significant,
approximately twofold, rise in mitochondrial capacity (per milligram of
mitochondrial protein) have been observed. According to the scenario developed
above, these processes increase the costs of mitochondrial maintenance and
cause a rise in SMR. Such metabolic cold compensation at the whole-animal
level is actually seen in temperate ectotherms during winter cold (with
activity maintained, no dormancy involved) or in eurythermal, especially
Northern hemisphere, populations along a latitudinal cline (for further
climate-related and evolutionary background, see Pörtner,
2001
,
2002a
).
In a variety of physiologically distinct populations of Atlantic cod
(Gadus morhua) between the North Sea and the Barents Sea, the
northernmost subpopulations studied (northeastern Arctic cod from the Barents
Sea or cod from the White Sea) display higher, i.e. cold-compensated, SMRs (if
acclimated and analysed at identical temperatures) than their temperate
conspecifics (Pörtner et al.,
2001; T. Fischer, R. Knust and H. O. Pörtner, unpublished
results). The increment between populations appears to be larger than the
temperature-specific metabolic increment observed, for example, in
cold-acclimated North Sea specimens between 12 and 4 °C. A similar pattern
is found in invertebrate eurytherms such as Arenicola marina
(Pörtner et al., 2000
;
Sommer and Pörtner,
2002
). However, very few data indicate whether cold compensation
also extends to the levels of maximum metabolic rate and factorial and net
metabolic scope. Because of their very similar modes of life, swimming
behaviour and morphology, cod populations and species from various latitudes
provide a unique basis for such analyses.
At acclimation temperatures between 15 and 4 °C, cod maintain factorial
scopes of between 2 and 5 (Bushnell et
al., 1994; Claireaux et al.,
1995
; Schurmann and
Steffensen, 1997
). Scope increased from 2.6 to 3.5-4.1 with some
decrease in acclimated SMR from 15 to 10 or 5 °C in the North Sea cod
population (Schurmann and Steffensen,
1997
) (Fig. 2). Net
metabolic scope during exercise fell only slightly
(Schurmann and Steffensen,
1997
). In conclusion, net metabolic scope appears to be partially
compensated in exercising cold-acclimated North Sea cod on the basis of
cold-compensated SMR (see above) between 15 and 5 °C.
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As a consequence of enhanced red fibre densities, striped bass (Morone
saxatilis) acclimated to 9 °C reached higher critical swimming
velocities during acute exposure to 15 °C (2.5 compared with 1.9
BL s-1 at 9 °C, where BL is body length) than
fish acclimated to 25 °C and brought to 15 °C (1.8 compared with 2.8
BL s-1 at 25 °C)
(Sisson and Sidell, 1987). The
data of Claireaux et al.
(1995
) indicate, however, that
cod acutely exposed to higher temperatures reach a metabolic ceiling during
exercise that is not very different from the maximum rate seen at the lower,
acclimated temperature. According to the modelled depiction in
Fig. 2B, this implies a drop in
maximum sustainable activity (critical velocity) at acutely elevated
temperature in cod. However, this does not appear to be a general pattern
(Sisson and Sidell, 1987
;
Taylor et al., 1997
). In cod
of the same population, longer-term acclimation to the warmer temperature may
be required for improved performance to Ucrit levels
beyond those reached in cold-acclimated specimens (see
Beamish, 1978
;
Schurmann and Steffensen,
1997
) (Fig.
2B).
For comparison, cold-adapted Atlantic cod collected from a population close
to Greenland as well as Greenland cod (Gadus ogac), both acclimated
and studied at 4°C, displayed temperature-specific SMRs even higher than
North Sea cod acclimated to and analysed at 5°C. With a value of 2.1,
factorial scope in the polar cod was below that of North Sea cod acclimated to
low temperature (Fig. 2)
(Bushnell et al., 1994).
Nonetheless, the northern cod reached somewhat higher critical swimming
velocities with a lower metabolic increment and similar or slightly lower
maximum metabolic rates than their southern conspecifics or confamilials (in
the case of G. ogac) at 5°C.
First, these findings would indicate metabolic cold compensation of SMR to
a higher degree in northern cod than in North Sea cod, a finding in line with
recent comparisons of SMR in Barents Sea (northeastern Arctic) cod and
Norwegian coastal or North Sea cod acclimated to the same temperature (T.
Fischer, R. Knust and H. O. Pörtner, unpublished results; see above).
Second, maximum metabolic rates may also be cold-compensated in northern cod.
However, measured values remain close to levels seen in cold-acclimated North
Sea cod despite higher SMRs (Fig.
2A). The slope of the metabolic increment seen during exercise is
reduced in northern cod, reflecting an increased energy efficiency that may be
a result of the long-term cold adaptation process in these populations. The
increased slopes observed for cold-acclimated North Sea cod in
Fig. 2B suggest that, possibly
as a consequence of cold-compensated SMR, North Sea cod at 5°C would reach
the same extrapolated activity levels (point of intersection) at higher net
costs of swimming than those acclimated to 15°C. A larger metabolic
increment with increasing swimming speed in cold-acclimated cod from the same
population is also visible in the data of Webber et al.
(1998). Over the range of
temperatures studied, changing water properties would not explain such a
significant increase in the cost of swimming (e.g.
Rome et al., 1990
). The
elimination of this cost increment in Arctic cod instead indicates that, at
low to medium activity levels, complete cold compensation of performance may
be possible during long-term cold adaptation, as has also been concluded for
Antarctic fish (see below).
As a result of elevated SMRs, factorial scopes appear to be reduced in
cold-adapted northern cod populations to levels lower than in cold-acclimated
temperate cod and even more so than in Antarctic fish (see below). Similarly,
among benthic zoarcids, a comparison of a cold-acclimated eurythermal
temperate (Zoarces viviparus) and an Antarctic species (Pachycara
brachycephalum) revealed a somewhat lower factorial scope (2.9
versus 6.6, estimated from the oxygen demand of the recovery
processes) in the North Sea than in the Antarctic eelpout
(Hardewig et al., 1998). These
comparisons clearly show that factorial scope is influenced by metabolic
cold-acclimation versus adaptation.
As a corollary, the few data available for northern populations indicate
that cold-adapted eurytherms, at the expense of elevated SMR, keep performance
levels similarly high in the cold as their southern conspecifics at warmer
temperatures, possibly even higher the more eurythermal they are. This
contrasts with the situation in Antarctic stenotherms (see below). Many more
species need to be investigated to determine whether this pattern reflects a
unifying principle of long-term eurythermal cold adaptation to Arctic and
sub-Arctic environments. Also, very little is known about the specific
cellular biochemistry of cold adaptation (compared with acclimation) in
eurytherms in a latitudinal cline in contrast to the large body of knowledge
existing for polar stenotherms, especially from the Antarctic. From a wider
perspective, the earlier use of maximum aerobic capacity at lower performance
levels in the cold would explain why high-performance species observed in
temperate to tropical areas among salmonids or scombrids do not exist in polar
areas. As adequately stated by Clarke
(1998), there are no polar
tuna.
Metabolic scopes and performance in polar stenotherms
Antarctic fish display continuous exercise at moderate levels of 1.4-2.6
BLs-1, which have been interpreted as adequately
cold-compensated compared with fish of similar lifestyle and body size in
temperate and tropical waters (van Dijk
et al., 1998; Peck,
2002
; cf. Wardle,
1980
). With respect to performance levels in Antarctic fish, some
uncertainty arises during interpretation of the data because of the
predominance of one fish family in the Antarctic, the Notothenioidea, which
makes it difficult to distinguish true patterns of cold adaptation from the
special features of this group. In this case, low performance levels might
arise from a benthic ancestor of all notothenioids, characterised by labriform
locomotion. Such an origin would also explain the absence of a swim bladder;
pelagic descendants use reduced ossification and extensive lipid deposits as a
secondary means of adjusting buoyancy
(Kock, 1992
;
Eastman, 1993
). However, Peck
(2002
) reviewed the
invertebrate literature and concluded that the levels of activity (walking and
digging in limpets, anemones and bivalves) in pelagic and benthic invertebrate
taxa are reduced compared with those in temperate taxa with little evidence
for temperature compensation. As in fish, performance at the high end appears
to be cold-restricted in invertebrates, although data on the invertebrates
with the highest performance rates, muscular squid, are not yet available (see
Pörtner, 2002b
, and
below).
Factorial metabolic scopes during exercise of between 3.9 and 5.7 have been
measured in Pagothenia borchgrevinki and Notothenia
coriiceps, values similar to those of temperate or tropical species with
a similar lifestyle (Forster et al.,
1987; Johnston et al.,
1991
; for spontaneous scopes, see
Zimmermann and Hubold, 1998
).
Higher factorial scopes in Antarctic stenotherms than in cold eurythermal
species (see above) clearly appear to be a consequence of low SMRs, which are
4-9 times lower in polar fish than in other species at 20°C
(Clarke and Johnston, 1999
).
Nonetheless, the metabolic rates reached during exercise are well within the
range seen in cod from temperate to Arctic latitudes
(Fig. 2A). Accordingly, overall
comparisons suggest that significant cold compensation of standard metabolic
rate, in contrast to findings in cold eurythermal fish and invertebrates (see
above), does not occur in fish and invertebrates from the permanent cold of
polar areas and the deep sea (e.g. Clarke
and Johnston, 1999
; Peck and
Conway, 2000
) and may, thus, be small. It must be emphasized that
these global statements are based on among-species comparisons and fail to
pick up more subtle differences among closely related species or among species
subpopulations in a latitudinal cline.
Nonetheless, the global trend observed matches a model presented previously
by Pörtner et al. (2000)
(cf. Pörtner, 2002b
) that
predicts that metabolic cold compensation should be greater in
winter-acclimated (with activity maintained) or cold-adapted eurytherms than
in stenotherms (Fig. 3).
Antarctic species in particular were able to minimize the metabolic costs of
cold adaptation, but at the expense of being obligatory stenotherms.
Significant metabolic cold adaptation, although not to the full extent
originally postulated by Wohlschlag
(1964
), may still be found if
more closely related species are compared. For example, cold-adapted Antarctic
eelpout (Pachycara brachycephalum) displayed the same metabolic rate
as cold-acclimated North Sea or Baltic eelpout (Zoarces viviparus),
both values being greater than that of warm-acclimated Zoarces
viviparus at low temperatures (van
Dijk et al., 1999
).
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Despite a secondary reduction in SMR during the transition from eurythermal
to stenothermal cold (Pörtner et al.,
1998), Antarctic species display features of metabolic cold
adaptation in their musculature: high mitochondrial densities compared with
temperate species at warm acclimation temperatures are still found in cold
stenothermal ectotherms, e.g. in slow fibres of notothenioid fish muscle
(Johnston, 1987
;
Dunn et al., 1989
). In white
muscle of the Antarctic notothenioid Gobionotothen gibberifrons,
cytochrome c oxidase (COX) activities were five times higher than in
a temperate-zone fish with a similar lifestyle
(Crockett and Sidell, 1990
),
whereas citrate synthase activities were increased by only 1.4- to 2.8-fold in
Trematomus newnesi and G. gibberifrons above the levels
found in temperate species. Mitochondrial proliferation involves enhanced
expression of aerobic enzymes such as cytochrome oxidase, measured by the
accumulated message (RNA) for this process. However, more message was found in
eurythermal fish (eelpout Zoarces viviparus) after cold-acclimation
than in cold-adapted stenothermal Antarctic eelpout Pachycara
brachycephalum (Hardewig et al.,
1999
), a finding in line with the suggested secondary
downregulation of cold compensation.
In contrast to eurythermal cold-acclimation or adaptation (see above), the
aerobic capacity per milligram of mitochondrial protein in Antarctic fish and
invertebrates is not evidently cold-compensated
(Johnston et al., 1998;
Pörtner et al., 2000
),
and the surface area of mitochondrial cristae in Antarctic red-blooded fish
(36-37 m2 m-3), a measure of membrane folding, is not
significantly different from those of temperate and tropical perciform fish
with similar lifestyles (Archer and
Johnston, 1991
; Johnston et
al., 1998
), but is significantly lower than the highest values
reported, which are for tuna red muscle (63-70 m2 cm-3)
and hummingbird flight muscle (58 m2 cm-3)
(Moyes et al., 1992
;
Suarez et al., 1991
). This
surface area is traditionally interpreted to correlate with aerobic capacity,
but recent evidence suggests that this correlation is less tight in icefish
(O'Brien and Sidell, 2000
).
For comparison, a theoretical limit of 83 m2 cm-3 was
suggested by Srere (1985
),
with limited space left for Krebs cycle enzymes. The respective values for
invertebrates are not known.
In Antarctic fish, skeletal muscle mitochondrial volume density is at least
29-33%, whereas in Mediterranean fish with similar activity the value is 8-13%
(Johnston et al., 1998). The
highest mitochondrial densities found in the cold were 56% for the pelagic
notothenioid Pleuragramma antarcticum and above 50% for icefish
(Johnston, 1987
;
Dunn et al., 1989
;
Johnston et al., 1998
).
Species lacking haemoglobin tend to have higher densities than red-blooded
species in association with a lower density of lipid droplets
(Johnston, 1987
;
Dunn et al., 1989
) (see
below). In warm waters, even very active fish do not have values above 40%,
with some influence of body size; 46% was reported for small anchovies and 29%
for tuna (Johnston, 1982
;
Moyes et al., 1992
). The value
for hummingbird flight muscle is 35%
(Suarez et al., 1991
).
As a corollary, despite extreme cold-induced mitochondrial proliferation in
pelagic Antarctic fish, full performance compensation is only possible for low
to moderate activity levels. Mitochondrial volumes in the red muscles of
Antarctic fish (Johnston et al.,
1988,
1998
;
Archer and Johnston, 1991
) are
elevated even beyond those seen in temperate or warm-blooded species. In
contrast to cold eurytherms, SMR is only cold-compensated to a non-significant
degree in Antarctic ectotherms, such that factorial scope is higher than, for
example, in northern cod. It appears that, in a trade-off between the space
adopted by myofilaments, oxidative metabolism and SMR, the requirement for
more mitochondrial volume for the same functional capacity in the cold is a
major constraint on the maximum scope for activity, linked to lower levels of
muscular force per muscle cross-sectional area. This affects all the
musculature, including the circulatory muscles, such that the space
constraints within cardiomyocytes and the limits on the size of the heart in
relation to body mass in icefish (Tota et
al., 1991
; Axelsson et al.,
1998
; O'Brien and Sidell,
2000
) will also reflect the limitation of aerobic scope for the
whole organism to within the borders of the narrow thermal tolerance
window.
According to Pörtner et al.
(2000), the reduction in SMR
during stenothermal, in contrast to eurythermal, cold may be a secondary
situation linked to the reduced mitochondrial capacities and increased
Arrhenius activation energies (Ea) of mitochondrial oxygen
demand, particularly proton leakage, and of flux-regulating enzymes in
metabolism such as isocitrate dehydrogenase. A high kinetic barrier may
support a low metabolic flux in cold stenotherms despite mitochondrial
proliferation. High Ea values in Antarctic species reflect
a high temperature-dependence of metabolism and, in consequence, reduced heat
tolerance, i.e. cold stenothermy of the whole organism. In contrast, the
Ea value of overall metabolism appears to be reduced in
active cold-acclimated eurytherms, with the consequence that SMR is elevated
(see Pörtner, 2001
,
2002a
).
The finding of excess aerobic design for low-activity lifestyles would also
explain why anaerobic capacity is, on average, reduced in polar fish. In
general, oxidative enzymes and creatine kinase, adenylate kinase and AMP
deaminase show relatively high degrees of cold compensation in notothenioids,
while glycolytic enzymes do not (Dunn and
Johnston, 1986; Johnston,
1987
; Crockett and Sidell,
1990
), with some variability in enzyme levels depending on mode of
life (Dunn et al., 1989
).
Cold-compensated anaerobic capacity was, however, found in some, but not all,
temperate freshwater fish (see van Dijk
et al., 1998
). In contrast to findings of low lactate levels in
fatigued notothenioids, a recent comparison of cold-acclimated temperate
(North Sea) with Antarctic zoarcids (Zoarces viviparus versus Pachycara
brachycephalum) led to the conclusion that a similar anaerobic capacity
is expressed in both species in the cold
(Hardewig et al., 1998
). These
benthic sluggish fish formed similar amounts of lactate (11.5 µmol
g-1 muscle tissue) as flounder acclimated to 11 °C
(Milligan and Wood, 1987
). On
the basis of these data, a low glycolytic capacity does not appear to be a
general phenomenon in Antarctic fish. The conclusion arises that cold
compensation of anaerobic pathways is, in principle, possible, but this
possibility is not expressed in the notothenioid fish family
(Egginton and Davison, 1998
)
which, in contrast to strictly benthic zoarcids, tend to have a more active
mode of life and, therefore, tend to express a more aerobic mode of
metabolism.
Low SMRs and similar factorial scopes as in moderately active temperate
species should cause the absolute metabolic increment to be lower in Antarctic
fish compared with temperate or eurythermal species. Peck
(1998,
2002
) emphasized that the
four- to ninefold lower absolute metabolic scopes in Antarctic fish and
invertebrates compared with temperate species at 20 °C also contribute to
extended periods of post-prandial metabolic increments (specific dynamic
action, SDA) when polar and temperate species have the same meal size. Again,
factorial increments of SDA above SMR are similar in polar, temperate and
tropical environments (Johnston and
Battram, 1993
; Peck,
1998
), corroborating the observation that, despite similar
factorial scopes, absolute metabolic scopes are reduced in the permanent cold
because of low SMRs. The general validity of this statement still needs to be
established because SMRs and metabolic scopes in the few Antarctic fish
species analysed during exercise in swim tunnels are well within, and even
beyond, the range found for moderately active, temperate and cold-adapted
Arctic eurytherms such as cod (Fig.
2A). Nonetheless, the patterns seen within the closely related
gadids suggest different modes of cold-acclimation and adaptation in
eurythermal compared with stenothermal fish species (see above).
![]() |
Similarities of cold- and high-performance adaptations |
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In similar ways, cold-adaptation seems to favour rapid recovery. Starting
from similar levels of anaerobic disturbance, enhanced recovery rates were
observed in cold-adapted Antarctic compared with cold-acclimated eurythermal
eelpout (Hardewig et al.,
1998). Moreover, starting from elevated SMRs, a lower increment in
metabolic rate, i.e. enhanced aerobic efficiency at high swimming speed,
characterizes cold-adapted Northern compared with cold-acclimated temperate
cod populations (see above). This resembles the effects of long-term exercise
training. Less circulatory work results, thereby contributing to cost
reductions during exercise. Despite elevated factorial scopes and low SMRs
compared with eurythermal fish, features of high-performance metabolism are
still present in Antarctic fish (Fig.
4), as in both seasonal and permanent cold, more mitochondrial
volume or mitochondrial functional components are needed for the same level of
functional performance than in the warm.
|
The role of lipids and lipid metabolism
Another important aspect of cold-acclimation and cold-adaptation is that
the development of an enhanced mitochondrial density goes hand in hand with a
shift from carbohydrate to lipid catabolism, the preferred use of lipids by
mitochondria and, as a precondition, enhanced whole-body and intracellular
storage of lipids (Fig. 4). The
trend to accumulate lipids seen in rainbow trout slow muscle fibres during
seasonal cold (Egginton et al.,
2000) goes hand in hand with a trend to increase the capacity of
ß-oxidation, especially in red muscle
(Guderley and Gawlicka, 1992
).
Such a shift from the glycogenolytic pathway, which is structurally associated
with muscular fibrils, to the ß-oxidation pathway located in the
mitochondrial matrix appears to be a logical consequence of increased
mitochondrial and decreased myofibrillar cell volume fractions in the cold.
Preferred use of lipids by cold mitochondria is seen in striped bass, for
example, with twofold higher rates observed at cold (5°C) compared with
warm (25°C) acclimation and measurement temperatures. As a consequence of
high mitochondrial densities, Antarctic fish also display elevated capacities
of mitochondrial ß-oxidation, indicated by activities of
3-hydroxy-acyl-CoA dehydrogenase and carnitine palmitoyltransferase (CPT) (for
a review, see Sidell and Moerland,
1989
). Rate-limiting control of lipid catabolism may be exerted by
transfer of acyl derivatives across the mitochondrial membrane supported by
CPT rather than by ß-oxidation
(Driedzic and Hochachka, 1978
;
Weber and Hamann, 1996). In the lipid stored by notothenioids (whole animal),
monoenoic fatty acids such as 18:1 predominate
(Hagen et al., 2000
), a
finding in line with the preferred use of this fatty acid by the mitochondria
of notothenioid fish (Sidell et al.,
1995
). Overall, the high volume density of mitochondria combined
with cold-compensated and preferred lipid metabolism in cold-acclimated
temperate and permanently cold-adapted polar fish
(Johnston and Harrison, 1985
;
Sidell, 1991
,
1998
;
Sidell et al., 1995
) again
resemble metabolic features seen in high-performance scombrid fish such as
mackerel or tuna and also in mammals.
In notothenioids, intracellular lipid content in oxidative muscle ranges
between approximately 9 % of dry mass in the demersal species
Gobionotothen nudifrons, 37 % in the cryopelagic Pagothenia
borchgrevinki (Sidell et al.,
1995) and 45.6 % in Pleuragramma antarcticum
(Hubold, 1985
). Much of this
lipid is accumulated, especially in the pelagic food chain, by feeding on
lipid-rich pelagic zooplankton (see Clarke
and Peck, 1991
). Although the largest lipid contents have been
found in pelagic fish, selective pressure towards lipid storage and aerobic
lipid metabolism in the cold appears to prevail even at low activity levels.
This is emphasized by a comparison of benthic North Sea and Antarctic zoarcids
fed on the same shrimp (Crangon crangon). North Sea eelpout
(Zoarces viviparus) accumulated only 10 % lipids per body dry mass,
whereas Antarctic eelpout (Pachycara brachycephalum) accumulated 33 %
(Brodte, 2001
), suggesting that
this process is triggered by cold temperatures. These findings also
corroborate the conclusion that, in the Antarctic ecosystem, lipid
accumulation in fish cannot be explained simply by the uptake of lipid-rich
zooplankton. Cold-adapted metabolism in predators and their prey instead
follows the same rules, leading to an overall accumulation of lipid in the
food chain.
Lipid storage in fish is in the form of triglycerides. In a comparison of
31P nuclear magnetic resonance (NMR) spectra of the muscle tissue
of the two species (Bock et al.,
2001), the levels of high-energy phosphates and inorganic
phosphate did not appear very different, but high levels of
glycerophosphatidylethanolamine (GPE), glycerophosphatidylcholine (GPC),
phosphatidylethanolamine (PE) and phosphatidylcholine (PC), in addition to an
unknown phosphate compound (X) in the phosphodiester region, were
visible in Antarctic eelpout Pachycara brachycephalum but not in
North Sea eelpout Zoarces viviparus
(Fig. 5). This indicates a
higher free phospholipid content, possibly associated with higher membrane
contents and metabolic rate used to preserve membrane fluidity
(Storelli et al., 1998
). The
high phosphodiester content will also reflect the higher density of
mitochondria and their membranes in Antarctic fish. Mitochondria predominantly
possess phosphatidylcholine, phosphatidylethanolamine and, to a lesser extent,
cardiolipin, with decreasing concentrations of phosphatidylcholine, a general
phenomenon in cold-adapted membranes
(Wodtke, 1978
;
van den Thillart and de Bruin,
1981
; Storelli et al.,
1998
).
|
A rise in cellular/organellar lipid contents and a reduction in
inter-mitochondrial distances cause a parallel rise in cellular oxygen
solubility and diffusibility (Tyler and
Sidell, 1984; Egginton and
Sidell, 1989
; Londraville and
Sidell, 1990
), which appears beneficial during both cold and
performance adaptations by supporting oxygen supply. Otherwise, a drop in the
Krogh diffusion constant (KO2) of 1.6 %
°C-1 would occur during cooling, which comprises a drop in
diffusion coefficient DO2 of 3 %
°C-1 as well as an increase in oxygen solubility of
approximately 1.4 % °C-1. A 42 % lower Krogh constant would
result for the cytosol of an Antarctic fish (at -1.8°C) compared with that
of a temperate fish at 25°C (Sidell,
1998
). Work carried out on striped bass unequivocally demonstrates
that this drop in KO2 is not only compensated
for during lipid accumulation but that, instead of being reduced,
KO2 virtually doubles between 25 and 5°C as
a result of a more than 10-fold increase in the fractional cell volume filled
with lipid and the associated doubling of cellular oxygen solubility. The
diffusion coefficient DO2 is more-or-less
maintained because of structural changes in the cell. With membranes being the
preferred pathways of oxygen diffusion, Sidell
(1998
) convincingly argued
that the enhanced mitochondrial density, together with the increasing level of
lipid unsaturation, would support oxygen flux into the centre of the cell.
The question arises of whether lipid accumulation is adaptive and driven by
limitations in aerobic scope (as concluded for mitochondrial proliferation;
see above) or whether it is a beneficial by-product of an increased
mitochondrial proliferation and the associated shift to lipid metabolism. The
latter appears to be the case. The scenario of a secondary drop in SMR during
the evolution of Antarctic fauna probably occurred at elevated mitochondrial
densities and enhanced lipid contents in aerobic muscles, as seen in
cold-acclimated eurytherms. At low metabolic rates and high oxygen solubility
in body fluids and cellular lipid depots, excess rather than too little oxygen
becomes available, supporting energy savings by a reduction in the
PO2 gradients needed for oxygen flux and, thus,
in ventilatory and circulatory effort. Loss of haemoglobin and myoglobin
function in icefish corroborate this view by indicating excess oxygen
availability not only linked to excess oxygen availability from cold ambient
water and via cold body and cell fluids but also via the
accumulation of lipids in the cold. Excess oxygen availability in the cold and
diffusion/solubility limitations lower than in warm-acclimated fish are also
indicated by a trend for the development of red muscle fibre hypertrophy, as
seen in cold-acclimated striped bass
(Egginton and Sidell, 1989).
In Antarctic fish, both slow oxidative and fast glycolytic muscle fibres are
larger, with reduced capillary density for a maintained intracellular
PO2 profile, compared with those of temperate
and tropical species with a similar mode of life (Johnston,
1987
,
1989
;
Johnston et al., 1988
;
Dunn et al., 1989
;
Egginton, 1999
).
An increased mitochondrial capacity for lipid oxidation in itself does not
explain why and how lipids are accumulated in tissues and organisms in the
cold. It has been hypothesized that tissues with elevated mitochondrial
contents maintain a higher adenylate energy charge with low levels of free
ADP, AMP and inorganic phosphate, thus minimizing stimulation of glycolysis
and favouring the use of non-carbohydrate substrates
(Holloszy and Coyle, 1984). In
Antarctic species, such trends would be supported by a low-energy-turnover
lifestyle with infrequent activity bouts and rare use of anaerobic
metabolism.
Again, the reasons and mechanisms for enhanced cellular lipid accumulation
may be similar in high-performance skeletal and heart muscle to those in
animals acclimating to cold temperatures and are emphasized at high SMRs.
Lipogenesis in male gulf killifish, Fundulus grandis, was stimulated
by cold temperature and led to lipid accumulation during cold exposure in
autumn (Weld and Meier,
1985). Hepatocytes from cold-acclimated rainbow trout exhibited
significantly higher rates of fatty acid and sterol synthesis (measured as
tritium incorporation) (Hazel and Sellner,
1979
) at assay temperatures of 15 and 20 °C than did
hepatocytes from warm-acclimated trout. Enhanced mitochondrial densities, seen
particularly in pelagic species, probably support the shift towards enhanced
fatty acid synthesis in liver and muscle. Put simply, enhanced mean cellular
levels of mitochondrial intermediates such as citrate are a logical
consequence of high mitochondrial volume fractions. Excess citrate is exported
from the mitochondria into the cytosol to initiate lipogenesis. This occurs
particularly at resting metabolic rates, when other cellular costs are reduced
(Goodridge, 1985
). This
scenario matches the situation in Antarctic fish and invertebrates, in which
long periods of resting metabolic rate prevail. Low levels of muscular
exercise at high mitochondrial densities will further increase the fraction of
time available for net lipogenesis. All these factors probably contribute to
the extraordinary levels of lipid seen in pelagic Antarctic ectotherms.
Last but not least, a trend to use fatty acids as substrates transported to
and synthesized within muscle cells may be enforced by greatly reduced rates
of energy-dependent transport across cellular membranes in polar cold mirrored
by low Na+/K+-ATPase activity (see
Pörtner et al., 1998) as
well as reduced capacities for temperature-dependent acidbase
regulation (Pörtner and Sartoris,
1999
; van Dijk et al.,
1997
). Fatty acids are bound to an albumin-like protein to be
transferred through the interstitial fluid. Diffusive transfer through the
membrane does not appear to be energy-dependent, but driven by a concentration
gradient. As in endurance-adapted species, a larger fraction of cellular
energy demand in cold-adapted muscle will be obtained from intramuscular
substrate stores and a smaller fraction from blood-borne substrates (Johnston
and Moon,
1980a
,b
;
Weber and Haman, 1996
).
Protein stores will be reduced as a result of enhanced mitochondrial
densities, so cellular lipid stores, with their high energy density, would
appear most suitable to replace protein as a substrate. However, lipid
transport in fish is largely unexplored, especially with respect to its
thermal sensitivity.
![]() |
Conclusions and perspectives |
---|
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---|
Reduced motor activity combined with enhanced levels of aerobic machinery, particularly in pelagic Antarctic fishes, and a cold-induced shift to aerobic metabolism probably explain the reduced glycolytic capacity compared with the high end of the activity spectrum in warm-water fish such as scombrids or salmonids. In parallel with the maximization of aerobic design, lipid accumulation occurs in the cold; this is not driven by oxygen limitations but rather appears as a secondary benefit from enhanced mitochondrial densities supported by low-activity lifestyles and low metabolic rates in the cold.
The patterns observed support the overall conclusion that warm-bodied animals achieve a higher power output with lower mitochondrial density. For this reason, cold-adapted animals develop characteristics of cellular design and biochemistry typical of high-performance species in the warm. These are maximized in Antarctic pelagic fish, with extreme mitochondrial densities and huge lipid depots but a lack of cold-compensated mitochondrial capacities compared with Arctic eurytherms. The attainment of a lower muscular performance with maximized aerobic design characterizes the trade-offs and constraints involved in adaptation to the permanent cold. As a by-product of these considerations, extrapolations to the warm end of the activity spectrum immediately suggest that aerobic muscle with maximized aerobic power output is best designed close to mammalian and bird body temperatures (Fig. 6).
|
While previous work has focused on the degree of cold compensation of SMR,
with the general conclusion that minimisation of the degree of metabolic
cold-adaptation and cold stenothermy go hand in hand
(Pörtner et al., 2000),
future work must consider how far metabolic cold-compensation extends to
maximum metabolic rates and absolute metabolic scopes. Closely related species
need to be preferentially investigated to minimize the risk of otherwise
misleading conclusions from global comparisons.
Fig. 2 demonstrates that
maximum metabolic rates in notothenioid fish match or even, in the case of
Notothenia neglecta, exceed those in cold-acclimated Atlantic cod.
This suggests cold-compensation of metabolic scope at relatively low SMRs in
more active Antarctic fish; however, such a generalized conclusion is not
(yet) possible. Future work must also focus on the close interactions between
cellular biochemistry, whole-animal performance and developments of the
natural temperature regime and its oscillations over time to provide a more
comprehensive picture of eurythermal versus stenothermal adaptation
to cold.
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Acknowledgments |
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