Climate-dependent evolution of Antarctic ectotherms: An integrative

ARTICLE IN PRESS
Deep-Sea Research II 53 (2006) 1071–1104
www.elsevier.com/locate/dsr2
Climate-dependent evolution of Antarctic ectotherms:
An integrative analysis
Hans O. Pörtner
Alfred-Wegener-Institut, für Polar-und Meeresforschung, Ökophysiologie, Postfach 12 01 61, D-27515 Bremerhaven, F.R.G, Germany
Received 8 June 2005; accepted 17 February 2006
Available online 14 July 2006
Abstract
The paper explores the climate-dependent evolution of marine Antarctic fauna and tries to identify key mechanisms
involved as well as the driving forces that have caused the physiological and life history characteristics observed today. In
an integrative approach it uses the recent concept of oxygen and capacity limited thermal tolerance to identify potential
links between molecular, cellular, whole-organism, and ecological characteristics of marine animal life in the Antarctic. As
a generalized pattern, minimization of baseline energy costs, for the sake of maximized growth in the cold, appears as one
over-arching principle shaping the evolution and functioning of Antarctic marine ectotherms. This conclusion is supported
by recent comparisons with (sub-) Arctic ectotherms, where elevated levels of energy turnover result at unstable, including
cold temperatures, and are related to wide windows of thermal tolerance and associated metabolic features.
At biochemical levels, metabolic regulation at low temperatures in general, is supported by the cold compensation of
enzyme kinetic parameters like substrate affinities and turnover numbers, through minute structural modifications of the
enzyme molecule. These involve a shift in protein folding, sometimes supported by the replacement of individual amino
acids. The hypothesis is developed that efficient metabolic regulation at low rates in Antarctic marine stenotherms occurs
through high mitochondrial densities at low capacities and possibly enhanced levels of Arrhenius activation energies or
activation enthalpies. This contrasts the more costly patterns of metabolic regulation at elevated rates in cold-adapted
eurytherms.
Energy savings in Antarctic ectotherms, largely exemplified in fish, typically involve low-cost, diffusive oxygen
distribution due to high density of lipid membranes, loss of haemoglobin, myoglobin and the heat shock response, reduced
anaerobic capacity, large myocytes with low ion exchange activities, and the use of lipid body stores for neutral buoyancy.
Important trade-offs result from obligatory energy savings in the permanent cold: low metabolic rates support coldcompensated growth but imply narrow windows of thermal tolerance and reduced scopes for activity. The degree of
thermal specialization is not uniformly defined by cold temperature but varies with life style characteristics and activity
levels and associated aerobic scope. Trade-offs for the sake of cold compensated growth parallel reduced capacities
for exercise performance, exacerbated by the effect of high haemolymph magnesium levels in crustaceans and, possibly,
other invertebrates. High magnesium levels likely exclude the group of reptant decapod crustaceans from Antarctic waters
below 0 1C.
The hypothesis is developed that energy savings imposed by the permanent cold bear specific life history consequences.
Due to effects of allometry, energy savings are exacerbated at small body size, favouring passive lecithotrophic larvae. At
all stages of life history, reduced energy turnover for the sake of growth causes delays and low rates in other higher
functions, with the result of late maturity, fecundity and offspring release, as well as extended development. As a
Tel.: ++49 471 4831 1307; fax: ++49 471 4831 1149.
E-mail address: [email protected].
0967-0645/$ - see front matter r 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.dsr2.2006.02.015
ARTICLE IN PRESS
1072
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
consequence, extended life spans evolved due to life history requirements. At the same time, polar gigantism is enabled by a
combination of elevated oxygen levels in cold waters, of reduced metabolism and of extended periods of growth at slow
developmental rates.
r 2006 Elsevier Ltd. All rights reserved.
Keywords: Antarctic marine ectotherm; Metabolic cold adaptation; Climate-dependent evolution; Stenothermy versus eurythermy;
Growth; Development
1. Introduction
It has been well documented that decadal-scale
variations in the coupled ocean-atmosphere system
impact animal communities and populations in
marine ecosystems (Cushing, 1982; Beamish, 1995;
Bakun, 1996; Finney et al., 2002). Similarly, current
analyses of the effects of climate change on marine
ecosystems have revealed that present-day effects of
global warming on the biosphere are associated with
shifts in the geographical distribution of ectothermic animals along a latitudinal cline or with poleward or high-altitude extensions of geographic
species ranges (Walther et al., 2002; Parmesan and
Yohe, 2003; Root et al., 2003). However, the level of
significance of such observations is under debate
partly due to the lack of comprehensive cause and
effect understanding (Clarke, 1996; Jensen, 2003).
Nonetheless, temperature means and variability as
associated with the climate regime can be interpreted as major driving forces setting the large scale
biogeography of marine water breathing animals.
On the cold side, temperature variability is
currently lowest in the marine Antarctic with
temperature maintained close to freezing in several
areas (Clarke, 1988; Peck, 2005). At the same time,
Antarctic marine ectotherms live at the low end of
the temperature continuum in marine environments,
and are considered highly stenothermal (Somero
and De Vries, 1967; Peck and Conway, 2000;
Somero et al., 1996, 1998; Pörtner et al., 1999a,
2000; Peck et al., 2002). Temperature means and
variability in relation to the climate regime may thus
exert key influences in shaping survival and functional adaptation to temperature. These patterns are
paralleled by a specialization of animals on limited
thermal windows. The present paper tries to develop
a comprehensive picture of thermal adaptation and
limitation from molecular to ecosystem levels and
thereby, identify the forces and benefits of thermal
specialization from an integrative point of view.
Global climate change late in the Eocene epoch
(about 35 million years ago) started to shape the
characteristics of marine Antarctic ecosystems. This
was the beginning of the transition from a cooltemperate climate in Antarctica to the polar climate
that exists there today (for review see Clarke and
Crame, 1992; Crame, 1993; Clarke, 1996). However,
for a long time, temperatures remained close to 4 or
5 1C and only during the last 4–5 million years
cooling continued and reached the low temperatures
that characterize extant Antarctic waters (Fig. 1).
The cooling trend strongly influenced the structure
of shallow-water, Antarctic marine communities,
and these effects are still evident in modern
Antarctic communities. Current evidence suggests
a long evolutionary history in situ for much of the
Southern ocean fauna, with a large degree of endemism but some exchange via the deep sea (Clarke
and Crame, 1989). Cooling reduced the abundance
and diversity of fish and crabs, gastropods and
bivalves, which in turn reduced skeleton-crushing
predation on invertebrates. Reduced predation
allowed dense populations of ophiuroids and
crinoids to appear in shallow-water settings at the
end of the Eocene and these communities are
persistent today (Aronson et al., 1997). Nonetheless,
temperature oscillations have occurred repeatedly
on timescales of several thousands of years during
recent Antarctic climate history. As an example,
Antarctic surface waters were warm (at 4–5 1C close
to Bouvet island) and ice free between 10,000 and
5000 yr B.P. About 5000 yr B.P., sea surface temperatures cooled by 2–3 1C, sea ice advanced, and
the delivery of ice-rafted detritus to the subAntarctic South Atlantic increased abruptly (Hodell
et al., 2001).
Despite some variability the unique features of
long-term stable cold temperatures throughout the
whole year in the marine Antarctic contrast the
relative thermal instability and young age of the
marine Arctic (Overpeck et al., 2003; Schauer et al.,
2004; Maslowski et al., 2004) as well as the large
temperature fluctuations in temperate climates.
Comparison of fauna from these diverse climates
has served to identify and characterize the special
ARTICLE IN PRESS
Temperature (°C)
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
20
1073
Pachycara
brachycephalum
16
18
14
12
10
8
6
4
2
60
K Paleocene
50
40
30
Million years BP
Eocene
Oligocene
20
10
Miocene
PL P
Fig. 1. Surface-water temperatures for southern high latitudes during the Cenozoic (redrawn from Clarke and Crame, 1992; Crame, 1993).
The figure illustrates the overall cooling process beginning with the mid-Eocene, interrupted by intermittent warming periods and
Milankovitch cyclicity. While some fauna like the notothenioid fish fauna experienced the cooling process in situ, the resulting low
temperature and low temperature variability as well as the depth of Antarctic waters opened the marine Antarctic for immigrants from the
deep sea, like the eelpout, Pachycara brachycephalum, which then became typical elements of the Antarctic fauna (see text, eelpout drawing
by S. Schadwinkel).
physiological characters of Antarctic fauna. For
large-scale studies of marine biogeography and
evolution, animals from marine Antarctic ecosystems, especially those at highest latitudes and with
the largest degree of stenothermy, might thus be
considered as a reference point in the long-term
stable cold.
Studies within the EASIZ (Ecology of the
Antarctic Sea Ice Zone) program have provided
key perspectives for crucial relationships between
physiological characteristics and ecological features
of various Antarctic invertebrates and fish (Clarke,
1998; Pörtner et al., 2000; Peck, 2002). These studies
also have helped to unravel some of the mechanisms
and trade-offs, which define the benefits of thermal
specialization and their potential ecological consequences, for example, the reduced diversity of
crabs and fish. Considering recent progress in the
physiology of thermal tolerance a cause and effect
understanding currently emerges of how fluctuations in body temperature depending on the climate
regime, features of cellular design and the levels of
energy turnover and performance in animals are
interrelated (Pörtner, 2002a).
Key questions are whether, and how, the key
functional properties and limits of Antarctic
ectotherms have been shaped by adaptation to the
permanent cold? The present study assumes that
this process is crucial, while extreme seasonalities in
light conditions or food availability may play a
lesser role. In support of this assumption, eurythermal life forms with contrasting patterns of high
energy turnover are found at similarly high latitudes
under similar patterns of seasonality but more
variable climate and temperature regimes of the
North Atlantic. However, the thermal environments
even of Antarctic oceans are not uniform, with
different temperature means and variability, e.g. in
the Bellingshausen Sea, the Weddell Sea, the
Northern Antarctic peninsula or at various water
depths (Kaplan et al., 1997, 1998; Vaughan et al.,
2001; Vogt, 2004; Fahrbach et al., 2004). The
question then arises; to what extent the stereotype
of a ‘‘good’’ Antarctic ectotherm does exist. It will
be discussed whether Antarctic marine life rather
should be interpreted to be located to variable
degrees at the extreme end of a continuum of life
forms in various climates. This is a general question
beyond more specific ones, e.g., the limited diversity
of the impoverished Antarctic fish fauna due to
requirement and evolution of antifreeze proteins
(Chen et al., 1997) or the special sensitivity of the
crustacean fauna to high magnesium levels in cold
ocean waters, which excluded the reptant decapods
from the marine Antarctic below 0 1C (Frederich et
al., 2001, see below). Another more general question
would be why evolution excluded expensive lifestyles and physiologies from the marine Antarctic
(cf. Clarke, 1998).
The treatment will conclude with a perspective on
how periods with stable versus more unstable
climates in earth history may have supported
evolutionary progress through progressively enhanced diversification of lifestyles between low and
high levels of energy turnover. Thereby, climate
variability may have contributed to speciation and
radiation and, thus, the setting of biodiversity.
Finally, the question arises whether an over-arching
ARTICLE IN PRESS
1074
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
conceptual framework is available that leads to a
comprehensive understanding of the climate-dependent evolution of marine including Antarctic fauna.
Most importantly, such a conceptual framework
should integrate information from molecular, cellular, tissue, blood, organismal, population and
ecosystem levels of biological organisation. Such
integration may include unconventional thinking as
required for unravelling the potential interdependence of phenomena at various levels of biological
organisation. The conceptual framework can be
tested in how it is able to integrate relevant
phenomena at various organisation levels. Such a
framework also should provide guidance in finding
adequate interpretations of individual phenomena.
2. Oxygen and capacity limited thermal tolerance:
evidence from Antarctic species
The concept of oxygen and capacity limited
thermal tolerance might provide such an integrative
framework (based on Pörtner, 2001, 2002a; Pörtner
et al., 2005a). Using the principles of Shelford’s law
this concept suggests that the first level of thermal
intolerance at low and high temperature extremes in
metazoa is a loss in whole organism aerobic scope.
This relative loss occurs at both, the low and the
high borders of the thermal envelope, beyond socalled pejus thresholds (Fig. 2, pejus ¼ getting
worse). This loss occurs in air-saturated water, by
progressively limited capacity of oxygen supply
mechanisms (ventilation, circulation). Beyond pejus
temperatures, a mismatch develops between oxygen
supply and temperature-dependent oxygen demand.
However, warming (cooling) conditions not only
stress animals because of the forced rise (decrease)
in ectotherm metabolic rate and oxygen demand. At
the same time environmental conditions change.
For example, warming reduces water oxygen
solubility and thus contents, thereby providing a
double challenge for oxygen supply capacity.
Thermal constraints on matching oxygen supply
and demand will affect all higher organismal
functions, activity, behaviours, growth, and reproduction, and thereby the long-term fate of populations and species in various climates.
With continued cooling or warming, aerobic
scope finally vanishes towards low or high critical
threshold temperatures (Tc), where transition to
anaerobic mitochondrial metabolism and progressive insufficiency of cellular energy levels occurs as
seen in Antarctic eelpout (Van Dijk et al., 1999).
Between initial aerobic limitation and critical
temperatures progressive hypoxia may already
enhance oxidative stress (Pörtner, 2002a,). At
extreme temperatures survival is time limited and
passive, supported by anaerobic metabolism (Zielinski and Pörtner, 1996; Sommer et al., 1997) and
the protection of protein and membrane functions
by heat shock proteins (Tomanek, 2005) and antioxidative defence (Heise et al., 2006). The concept
of oxygen and capacity limited thermal tolerance
suggests that earliest thermal limits are set at the
highest level of functional complexity, the intact
organism with narrowing windows from molecular
to cellular to systemic levels (Fig. 3). A systemic
to molecular hierarchy of thermal limits results
(Pörtner, 2002a), where whole organism functional
capacity is supported by the optimization of
molecular functions to within the organism’s
thermal range. Available evidence supports this
view by showing that enzyme, mitochondrial and
cellular functions of Antarctic invertebrates and fish
are maintained in a wider window of thermal
tolerance (Pörtner et al., 1999b; Hardewig et al.,
1999a; Mark et al., 2005, Fig. 4) than whole
organism functions that are first affected by limited
oxygen supply and falling aerobic scope (Van Dijk
et al., 1999; Mark et al., 2002; Peck et al., 2002).
Minima of cellular energy demand were found close
to habitat temperature in isolated hepatocytes of
Antarctic and sub-Antarctic fish, notothenioids and
a zoarcid, while the fractions in the cellular energy
budget remained unchanged over a wide range of
temperatures, beyond the window of whole animal
thermal tolerance (cf. Fig. 3). Cost increments as
seen between unicellular and macroorganisms
(Hemmingsen, 1960; Wieser, 1986) and associated
with the addition of central functions and coordination in multicellular organisms (cf. Pörtner, 2002a)
may define or co-define narrower thermal windows
of whole animals versus cells. The lowest rate of
cellular oxygen consumption (Fig. 4A) reflects an
energetic optimum, possibly close to low pejus
temperatures in Fig. 3. Cost increments at temperatures below the optimum would contribute to a cold
induced decrease in aerobic scope. The cost increment above may first be paralleled by a temperature-dependent rise in functional capacity until
oxygen supply becomes limiting at the upper pejus
temperature.
Aerobic scope is constrained in the cold by
mitochondrial, cellular and, thus, tissue functional
capacity. The capacity of mitochondria to produce
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
(A)
oxygen
limited
aerobic
scope
Tp
1075
Tp : onset of limitation in aerobic scope
Energy demand /
mitochondrial functions
transition to anaerobic metabolism
Tc
Tc : (loss of aerobic scope)
+ HSP, + antioxidants
(steady
state)
Td : loss of molecular function,
0
.
denaturation
Increasing oxidative stress
(B)
MO2
mitochondrial
oxygen demand
in vivo
max
residual ATP
production capacity
+
proton leakage
0
(C)
rate of
aerobic
performance
0
Temperature
Fig. 2. Central elements of the concept of oxygen and capacity limited thermal tolerance (after Pörtner, 2002a; Pörtner et al., 2004). The
modelled depiction considers progressively enhanced thermal limitation (A), by the consecutive onset of a loss in aerobic scope beyond
pejus thresholds, Tp, of anaerobic metabolism at critical thresholds, Tc, of molecular damage at denaturation thresholds, Td (note that a
lower Td is likely present, but not included in the figure). Downward-pointing linear arrows indicate increased oxidative stress during
progressive oxygen deficiency at cold or warm temperature extremes that contributes to molecular damage (Heise et al., 2006). The parallel
shift of low and high thermal tolerance thresholds (Tp and Tc) during temperature adaptation occurs by adjustments of capacity at various
functional levels. Td likely shifts with molecular modifications (see text) as well as with the adjustment of molecular protection mechanisms
like heat shock proteins or antioxidants. (B) Maximum scope (Dmax) between resting and maximum output in oxygen supply is likely
correlated with the one in mitochondrial ATP generation such that the functional capacity of tissues including ventilatory and circulatory
muscles is co-defined by the capacity of mitochondria to produce ATP. This capacity is limited by oxygen supply in vivo. Part of this
limitation is elicited by the temperature dependent rise in oxygen demand due to the cost of mitochondrial proton leakage or to the cost of
oxygen supply (see text). Maximum scope in ATP generation at the upper Tp not only supports maximum capacity of organismic oxygen
supply by circulatory and ventilatory muscles, but also an asymmetric performance curve of the whole organism (C). Optimal performance
(e.g., growth, exercise) is expected close to upper pejus temperature, Tp, as seen in data sets available for fish (see text).
energy aerobically is one probable mechanism
restricting performance including that of ventilation
and circulation. This may be the major reason why
mitochondrial proliferation is observed in aerobic
muscle in the cold (Guderley, 2004). This reason is
not sufficient, however, to explain the massive
accumulation of mitochondria in tissues of Antarctic
ectotherms (see below). The warm constraints are
associated with excessive mitochondrial oxygen de-
mand (e.g., caused by H+ leakage, which is enhanced
drastically upon warming in mitochondria from
Antarctic bivalves and fish; Hardewig et al., 1999a;
Pörtner et al., 1999b). This rise in baseline oxygen
demand outstrips oxygen supply, thereby also decreasing aerobic scope. As a trade-off between
maximized capacity of aerobic energy production
and associated cost this is one reason why mitochondrial densities are reduced in the warm environment.
ARTICLE IN PRESS
1076
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
Hierarchy of functional limits beyond optimum temperatures
changing ecosystem functioning, biodiversity,
Ecological disturbance: biogeography…
ecosystem
reduced population density…
loss in scope of performance
Organismic disturbance: beyond pejus levels
reduction of growth, reproduction, behaviours,
….recruitment
Cellular disturbance:
al
m
er
Th
organism
loss of functional integration
w
w
do
in
Narrowest
tolerance windows
at highest
functional levels
metabolic depression
beyond critical levels
Molecular disturbance
mortality
Fig. 3. Generalized scheme of a systemic to molecular hierarchy of thermal tolerance limits linking molecular to ecosystem characters and
limits. The integration of different functional levels leads to narrowest tolerance windows at high hierarchical levels which shape ecological
functions and their shift with a changing temperature regime. Note that tolerance thresholds (pejus and critical levels) vary between
Antarctic species and phyla, partly depending on the level of energy turnover (see text). Shifts in species interaction would result. Longterm tolerance limits (pejus levels) that define the onset of performance limitations still await direct quantification in many species.
In two examples, a fish and a bivalve, hyperoxia
was applied to Antarctic species to test whether
excess oxygen is able to widen the range of thermal
tolerance. In fish these tests were not suitable to
show a significant shift of passive thermal tolerance
reflected in critical limits, however, they were able to
reveal a protective effect: by reducing the circulatory workload upon warming (Mark et al., 2002)
hyperoxia supports enhanced aerobic scope in the
warm. A widening of optimum and pejus ranges is
thus likely. Further evidence for a rather modest
shift in pejus and, in this case, critical temperatures
comes from a study in a large infaunal Antarctic
bivalve, Laternula elliptica (Pörtner et al., 2006). In
Laternula, hyperoxia alleviated thermal limitations
by enhancing and stabilizing both inhalant water
and haemolymph oxygenation up to 7 1C. Most
prominent is the upward (by about 2.5 1C) shift of
the rapid decline phases of haemolymph Po2 from
an apparent pejus value of 4.3 1C to beyond 7 1C
and of inhalant water Po2 to beyond 9 1C (DTp in
Fig. 5). In line with a significant improvement of
tissue oxygenation, haemolymph oxygen tensions
remained significantly elevated above those observed in normoxia until beyond 9 1C. A comparison with recent data on thermal limitation of
exercise performance (Urban, 1998; Peck et al.,
2004a) indicates that a limitation of functional
scope may set in even earlier than suggested by the
significant drop of haemolymph oxygen tensions in
Fig. 5. The progressive decrease in arterial haemolymph oxygen tensions observed between 0 and 4 1C
may already reflect some decrement in aerobic
scope, due to mildly limited oxygen uptake. Such
trend is likely more prominent in venous haemolymph similar to observations in fish (Lannig et al.,
2004). Accordingly, temperature-dependent performance capacity in Laternula elliptica may be oxygen
dependent. A first consequence of warming thus
may be a reduction of energy allocation to active
behaviours during warming, for the sake of
sufficient energy provision to maintenance.
The degree to which hyperoxia reduces heat stress
and leads to a widening of the optimum and pejus
range is limited, however. Once the limits defined by
oxygen availability are suspended, further restrictions at cellular or molecular levels are likely to
become effective in reducing functional scope, in
line with a suggested organismal to molecular
hierarchy of thermal tolerance limits (Pörtner,
2001, 2002a). This may be one reason why the
room for shifting thermal tolerance in hyperoxia is
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
0.6
40
Tp
% air saturation
0.5
Tc
0.4
0.3
2
nmol O / min *106 cells
(A)
1077
0.2
20
0.0
0
10
5
15
20
Haemolymph
10
0
0.1
∆Tp
30
0
3
6
9
12
15
50
25
3
state 3
2
Antarctic
20
Inhalant water
Ea = 92.5 kJ mol
Proton
leakage
~Temperate,
eurythermal
-1
Ea = ≈50 kJ mol
3.4
3.5
3.6
0
3
0
3
6
9
12
15
12
15
100
-1
-1
30
0
1
0
40
10
3.7
Temperature (1000 K-1)
Fig. 4. Thermal window and temperature dependence of cellular
(A) and of mitochondrial (B) respiration rates. The pattern of
hepatocyte respiration rates as studied in the Antarctic eelpout,
Pachycara brachycephalum, acclimated to 0 1C (A, data by Mark
et al., 2005), reveals an energetic minimum which matches the
putative thermal window of the species (Tp and Tc values in vivo
according to van Dijk et al., 1999; Mark et al., 2002). Respiration
rates of isolated liver mitochondria of the Antarctic notothenioid,
Lepidonotothen nudifrons, (B) also indicate no functional damage
within the thermal window of the species (Hardewig et al.,
1999a), but a higher thermal response of proton leakage than of
state three respiration rates. The inclusion of temperaturedependent state 4 respiration rates from various temperate,
including terrestrial species (data and references as compiled by
Hardewig et al., 1999a) provides a preliminary basis for
comparison with the high thermal sensitivity of proton leakage
rates seen in Antractic ectotherms (see text).
small, especially with respect to a shift in critical
limits (Mark et al., 2002; Pörtner et al., 2006). In
contrast, the thermal window is narrowed significantly in hypoxia, mirrored in an oxygen dependence of critical temperatures or, conversely, in a
temperature dependence of critical oxygen levels
(Zakhartsev et al., 2003).
% reburying in 24 h
-1
-1
ln respiration rate (nmol O min mg )
(B)
% air saturation
Temperature (°C)
50
0
6
9
Temperature (°C)
Fig. 5. Comparison of maximum oxygen tensions recorded in the
haemolymph and inhalant water of Laternula elliptica with the
progressive limitation of scope for reburying during warming
(% reburying animals within 24 h, data adopted from Peck et al.,
2004a, broken lines depict the 95% confidence interval). The
comparison illustrates that the upper pejus value identified from
haemolymph recordings under normoxia (4.3 1C) is a high
estimate, as the 40% decrement in Po2 observed between 0 and
4 1C may already reflect some reduction in aerobic scope for
exercise. The analysis suggests that the upper pejus temperature
and optimum for muscular performance of the bivalve are found
closer to 0 1C than suggested by the statistical analysis. The shift
in the decline phases of haemolymph and inhalant water Po2
observed under hyperoxia is indicated as a shift in pejus values
(data in Pörtner et al., 2006).
These considerations emphasize the requirement
for a strictly integrative interpretation of experimental findings, similar to conceptual approaches
discussed in the complexity/symmorphosis debate
(Weibel et al., 1991). Functional capacities of
components contributing to complex systems are
not in large excess and are thus interdependent. This
ARTICLE IN PRESS
1078
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
would immediately explain why excess oxygen will
not widen the thermal window to beyond those
limits set at lower levels of organisational complexity but mostly support a widening of a window of
aerobic scope (Fig. 2). Molecular limits in the intact
organism may shift, however, due to the alleviation
of oxidative stress during hyperoxia.
Once the organism leaves its active thermal range
and passively sustains exposure to thermal extremes
beyond critical temperatures, as in the intertidal
zone, the danger of disruptions of molecular
functions or of molecular damage due to thermal
stress would be enhanced (cf. Sokolova and Pörtner,
2003). Antioxidative defence mechanisms and heat
shock proteins were hypothesized to play a key role
in stress protection especially under these conditions
(cf. Pörtner, 2002a). However, due to cooling on
evolutionally time scales these short-term stress
phenomena may not have played a significant role
during evolution in most of the marine Antarctic.
Accordingly, Antarctic notothenioid fish do not
express the heat shock response (Hofmann et al.,
2001), i.e. they have lost the ability to upregulate the
inducible transcript, hsp70, which is constitutively
present (Place et al., 2004). However, hsp70 mRNA
is expressed at high levels in field-acclimatized
fishes. Levels of ubiquitin-conjugated protein were
also elevated, indicating enhanced cellular protein
turnover in Antarctic fish, possibly due to trade-offs
between enhanced protein flexibility required for
function at cold temperature and the associated loss
in stability (Fields, 2001). This may emphasize the
need to minimize other cellular costs and thereby
enhance energy efficiency in the cold for a maximization of growth (see below). The heat shock
response still needs testing in marine Antarctic
invertebrates tolerating air exposure and more
extreme temperatures in the intertidal zone, as
found in the limpet, Nacella concinna (Pörtner
et al., 1999a).
2.1. Phylogenetic aspects
General applicability of the concept of oxygen
and capacity limited thermal tolerance is supported
by evidence available across various aquatic phyla,
namely annelids, sipunculids, molluscs (bivalves,
cephalopods), crustaceans, and fish, including the
Antarctic species (for review see Pörtner, 2001,
2002a; Pörtner et al., 2004). However, it needs to be
considered to what extent special functional design
and mechanisms (phylogenetic constraints) are
involved in various phyla? This has not been widely
investigated. In sipunculids the functional loss of
ventilation is clearly crucial, a circulatory system
does not exist (Zielinski and Pörtner, 1996). Among
molluscs, the situation is not clear in bivalves but
reduced oxygenation of both haemolymph and
inhalant water of the Antarctic bivalve, Laternula
elliptica, suggests thermally limited capacity of both
ventilation and circulation. It is unclear, however,
whether one is limited earlier than the other
(Pörtner et al., 2006). The highly active cephalopods
display thermal limitation in circulatory capacity
earlier than in ventilation, as seen in Sepia officinalis
(F. Melzner, C. Bock, H.O. Pörtner, unpublished).
Among crustaceans, data reveal a coordinated
limitation of both circulatory and ventilatory
capacity (Frederich and Pörtner, 2000), which elicits
the onset of hypoxia beyond pejus temperatures.
Finally, collapse of both systems occurs at temperature extremes where anaerobic metabolism sets in.
This latter point of failure may match the loss of
circulatory functioning seen in various species of
porcelain crabs in response to heat exposure (Stillman and Somero, 2000). This point of failure was
found to correlate with the thermal window of the
species, but values came close to high ambient
temperature extremes only in the warmest acclimated species. The progressive mismatch between
oxygen supply and demand develops earlier, however, as indicated by oxygen recordings in the
haemolymph (Frederich and Pörtner, 2000), emphasizing that loss of aerobic functional flexibility is
the first process that experiences thermal limitation
(Fig. 2).
Aerobic functional flexibility of crustaceans
appears to be heavily influenced by magnesium
levels in the haemolymph, especially in the cold. On
average, these levels are found much higher in
reptant anomurans and brachyurans than in
shrimp, amphipods and isopods. Magnesium elicits
muscle relaxation and anaesthesia; moreover, these
effects are exacerbated by cold temperatures. The
associated inactivation of ventilation and circulation leads to a reduction in functional capacity
especially in the cold such that low pejus levels are
found at higher temperatures than expected at
reduced haemolymph magnesium levels. In support
of this hypothesis, experimental reduction of
haemolymph magnesium levels reduced the thermal
dependence of metabolic functioning altogether
and alleviated the degree of cold-induced inactivation in various species of reptant decapods (Fig. 6).
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
Change of heart rate (%)
(A)
0
20
40
60
80
100
-2
-1
0
1
2
3
4
5
6
7
1
2
3
4
Temperature (°C)
5
6
7
(B)
35
*
Reaction time (sec)
30
*
25
20
15
10
5
0
-2
-1
0
Performance level
(C)
2+
low [Mg ]HL
2+
high [Mg ]HL
-
Temperature
+
Fig. 6. Effect of experimental reduction of mean haemolymph
Mg2+ levels ([Mg2+]HL) on heart rate (A, reduction from 50,
open symbols, to 15 mmol l1, filled symbols) and reactivity (B,
reduction from 39 to 9.5 mmol l1, filled symbols) of Hyas
araneus (after Frederich et al., 2000a). The conceptual model (C)
considers data obtained in Carcinus maenas, H. araneus, Maja
squinado and Eurypodius latreillei and indicates that ([Mg2+]HL
reduction is always effective in the cold but may also become
effective over a wider temperature range (redrawn from Frederich
et al., 2001). The reason for the different patterns remains
unexplained.
It caused a small, 1–2 1C downward shift of pejus
temperatures in Maja squinado (Frederich et al.,
2000b). Capacity for the regulation of haemolymph
magnesium levels thus appears as a phylogenetic
constraint, at least in anomuran and brachyuran
crabs.
1079
The reasons for a special sensitivity of crustaceans
to high magnesium levels compared to that of other
invertebrates are not clear. The special role of
ventilation in the thermal sensitivity of crustaceans
may be revealing in this context, whereas in other
groups the circulatory system may be more relevant
(see above). Ventilation of the gill chamber depends
on high frequency contraction of musculature
driving the small scaphognathite, which displays a
similar or somewhat higher frequency than the heart
(Frederich and Pörtner, 2000; Stegen and Grieshaber, 2001). Such high frequency ventilation and
circulation systems are not operative in other
invertebrates except for cephalopods (where the
effect of Mg is compensated for by elevated K
levels, F.J. Sartoris, pers. comm). These systems
may be especially prone to muscular relaxation
under magnesium and thus, represent an evolutionary constraint of this group. In the light of high
embryonic and larval heart beat frequencies (Spicer
and Morritt, 1996; Harper and Reiber, 2004) such
effects may set in early during development.
In contrast to crustaceans, oxygen limitation in
fish is set by circulatory capacity. Recordings of
oxygen partial pressures in arterial and venous
blood of Atlantic cod (Gadus morhua) showed
arterial oxygen tensions unaffected by temperature
as long as the animal did not collapse from thermal
stress (Sartoris et al., 2003). An earlier thermal
limitation of circulation than of ventilation is
indicated by falling venous oxygen tensions beyond
a narrow optimum range (Lannig et al., 2004). These
conclusions are in line with earlier observations by
Heath and Hughes (1973), who observed that
ventilation in trout remained virtually unchanged
during warming when heart rate already decreased.
The limits of aerobic scope in the heart may lead to
insufficient blood circulation at warm temperatures
(Farrell, 1997). In the integrated oxygen supply
system, the bottleneck is the high pressure closed
circulation system likely because it operates at a
higher cost than an open circulatory system. The
ventilatory system is set to provide maximum
amounts of oxygen such that the thermal window
of the circulatory system can be as wide as possible.
The limiting role of circulation may be even more
expressed in fish than in cephalopods, owing to the
fact that the systemic heart is supplied exclusively by
venous blood in many fish, but is supplied by
arterial blood (haemolymph) in cephalopods.
As a general concern, work with Antarctic fish
is frequently carried out with notothenioids or
ARTICLE IN PRESS
1080
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
comparisons of polar and non-polar fish are based
on comparisons of Antarctic and non-Antarctic
notothenioids. This approach is constrained by the
fact that wide-ranging comparisons of Southern
hemisphere stenotherms and Northern hemisphere
eurytherms are not possible, and that it is difficult to
disentangle patterns characteristic for the Southern
hemisphere notothenioids from general patterns of
cold adaptation. Future studies thus should not
only investigate the notothenioids but also include
investigations of cosmopolitan fish families like the
zoarcids (Hardewig et al., 1999b; Lucassen et al.,
2003) or study of congeneric species or of species
populations in a latitudinal cline in both hemispheres (see above).
2.2. Ecological relevance
Previous efforts in understanding thermal adaptation were largely focused on mechanisms providing passive tolerance. However, active behaviours
and life functions depend on temperature-dependent
performance capacity of the organism. According to
Fig. 2 functional capacity of the organism may
display its thermal optimum at high pejus values.
While critical temperatures indicate the long-term
physiological limits for passive survival, pejus values
reflect the onset of performance limits and thus, the
long term environmental limits of a species (Frederich and Pörtner, 2000). In general, direct assays of
upper and even more so, lower pejus temperatures
as well as of thermal optima of aerobic scope and of
functional capacity of the whole organism are scarce
and even more so comparisons of pejus temperatures with environmental impacts on species distribution and performance in situ are hardly
available. Direct measures of aerobic capacity
would be processes like aerobic exercise or growth
(Pörtner et al., 2005a). Growth curves similarly
shaped to the performance curve in Fig. 2C and,
thus, likely set by aerobic scope were found in
invertebrates (Mitchell and Lampert, 2000; Giebelhausen and Lampert, 2001) and in fish (Jobling,
1997). Aerobic scope and growth rate were found
related in a population of cod (Claireaux et al.,
2000). In line with these conclusions, recent findings
indicate that low blood oxygen tensions limit
proteins synthesis rates as seen in feeding crabs
(Mente et al., 2003). Indirect indicators of aerobic
scope are thus blood oxygen tension (Frederich and
Pörtner, 2000; Lannig et al., 2004) or patterns of
circulatory or ventilatory response to temperature
(Frederich and Pörtner, 2000; Mark et al., 2002;
Lannig et al., 2004; Melzner et al., 2006). With
respect to ecological validity and applicability of
these indicators, the most convincing data set
currently available is based on a comparison of
pejus values, critical temperatures and of field
data of temperature-dependent population density
for temperate eelpout (Zoarces viviparus) in the
German Wadden Sea (Pörtner and Knust, unpublished). These data suggest that enhanced mortality and reduction of population density are elicited
once ambient temperature exceeds upper pejus
values, where limited aerobic scope likely reduces
performance capacity and thus fitness of the
individual. Upper pejus values also coincide with
the thermal optimum of growth performance of the
common eelpout. Further analyses in closely related
species and their populations are required to
confirm this emerging picture. In Antarctic invertebrates (a scallop, Adamussium colbecki, a limpet, N.
concinna, a bivalve, Laternula elliptica) the early loss
of muscular performance upon warming (Peck et al.,
2004a) also relates to maximum ambient temperatures and would confirm this line of thinking.
However, the issue may be more complicated as
shifts in energy budget may occur during warming,
at the expense of exercise capacity. That aerobic
scope may be exploited differently depending on
temperature is indicated by the observation of a
drastic rise in growth performance of Antarctic
scallops during small degress of warming (see below).
In some cases pejus values were determined
indirectly, based on the onset of decreasing blood
oxygen tensions or on the changing temperature
dependence of circulatory performance or blood
flow. In Antarctic eelpout (Pachycara brachycephalum) pejus values estimated from blood flow were
found slightly higher than mean environmental
extremes (Mark et al., 2002); they are, however, in
line with the relatively high degree of eurythermy of
this species (Mark et al., 2005; Lannig et al., 2005).
Cod (G. morhua) acclimated to 10 1C grow optimally close to 10 1C (Pörtner et al., 2001). However,
upper pejus values in these fish as estimated from
highest venous oxygen tensions were found at about
6 1C. Venous oxygen tensions resulted lower at
acclimation temperature (Lannig et al., 2004). In
conclusion, the matching and integration of direct
and indirect measures of aerobic optima and limits
need further comparative investigation.
The picture emerges that not all species narrow
their thermal window down to match ambient
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
temperature fluctuations and extremes. Especially
under stable temperature conditions as in the
Antarctic, some species appear to be more eurythermal than they need to be (cf. Pörtner et al.,
2000; Lannig et al., 2005; Seebacher et al., 2005).
From an integrative point of view, thermal tolerance, in fact, may not only relate to ambient
temperature variability. Some evidence indicates
that the width of the thermal window and level of
aerobic capacity are interrelated (Pörtner, 2002b,
2004) such that animals with a higher aerobic scope
display wider windows of thermal tolerance and vice
versa. Nonetheless, the most temperature sensitive
species to date, the Weddell Sea bivalve Limopsis
marionensis displays an upper critical temperature
around 2 1C (Pörtner et al., 1999a). Laternula
elliptica loses capacity for exercise performance at
a pejus temperature of about 0 1C but reaches a
critical temperature only at 6 1C (Peck et al., 2002;
Pörtner et al., 2006). Oxygen- and capacity-limited
thermal tolerance windows are thus narrow in some
(more passive) Antarctic invertebrate species and
reflect their high sensitivity to current and, possibly,
future warming scenarios in Antarctic waters (Gille,
2002).
From an integrative point of view, an oxygen and
capacity limitation of metazoan life in the oceans is
also confirmed by the finding that rising oxygen
concentrations in cold waters support larger body
sizes in some species (polar gigantism, Chapelle and
Peck, 1999). Temperature stability and metabolic
rate likely play an important role in this context.
Large body sizes as seen among Antarctic marine
ectotherms are supported by low rates of metabolism at stable cold temperatures. As a simple reason,
low metabolic rates require lower oxygen gradients
for diffusion and tolerate larger distances for
diffusion. Thereby, it becomes possible to extract
sufficient oxygen from oxygen-rich water despite
large body sizes (Pörtner, 2002c). Conversely, recent
evidence indicates that eurythermy in the cold
would cause elevated metabolic rates. Eurythermy
is also supported by small body sizes due to shorter
oxygen transport pathways and diffusion distances
and high body surface to volume ratios (cf. Pörtner,
2004). These points suggest an integrated adjustment of the functional capacity of oxygen supply
systems and body size in relation to energy turnover
and a limited thermal window as co-determined by
ambient temperature variability (see below).
Oxygen-limited thermal tolerance of decapod
crustaceans has received special interest as it may
1081
be influenced by ion, and especially magnesium,
regulation (see above). These relationships may play
a key role in the shaping of extant Antarctic
ecosystems. Reptant decapods are present in both
the Arctic and Antarctic only at temperatures
permanently at and above 0 1C. The loss of the
reptant decapod crustacean fauna from high Antarctic ecosystems was hypothesized to be associated
with the high magnesium levels in the haemolymph
of this group, as a phylogenetic constraint (see
above, Frederich et al., 2000a, 2001). However, the
relevance of high haemolymph magnesium levels for
biogeographical patterns of anomurans and brachyurans is unlikely to be restricted to their
exclusion from the coldest parts of the Antarctic.
Available physiological data suggest a magnesium
effect that does not set in below a threshold
temperature, but is progressively enhanced during
cooling (Frederich et al., 2000a, 2001; Fig. 6).
Accordingly, this effect may develop gradually with
falling temperatures in a latitudinal cline and may
limit the variety of decapod life forms more and
more to those with a sluggish lifestyle. These
constraints may be involved in the decline of
anomuran and brachyuran diversity towards high
Southern latitudes (Astorga et al., 2003). At the cold
end of a progressive diversity decline only the
lithodids are left behind in (warmer waters of) the
Antarctic. The observation of 54 Brachyuran
species in the English Channel versus only 2 species
in Spitsbergen (Hiscock et al., 2004) would indicate
similar relationships for the Northern hemisphere,
where similar analyses are not yet available. It will
be investigated below to what extent this loss in
diversity may be elicited through the special
sensitivities of larval stages and not only by the
slowing of physiological rates due to high magnesium levels but also by cold temperatures per se.
With the current warming trends the limitation of
crustaceans to areas outside the Antarctic may be
alleviated, crabs may reconquer the Antarctic in due
course (Thatje et al., 2005).
High haemolymph magnesium levels characterize
other marine invertebrates as well and may thus
play a wider role in shaping Antarctic ecosystems.
Peck et al. (2004b) found that the level of routine
activity in Antarctic marine invertebrates is always
lower than in comparable temperate species (Fig. 7).
Only Antarctic fish display similar levels of routine
activity as their temperate counterparts. The single
most obvious difference between the groups is that
body fluids in invertebrates are iso-osmotic to sea
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
1082
1.4
Fish
Sustained
swimming
1.2
Limpet
locomotion
Relative rate
1.0
Clap
frequency
0.6
0.4
Drilling in
Trophon
snails
Scallop
0.8
Closing
velocity
Fish
burst
swimming
Anemone
burrowing
0.2
Burrowing
in Laternula
Burrowing
in Yoldia
0.0
Fig. 7. Levels of routine activity in Antarctic marine invertebrates and fish compared to related or ecologically similar temperate species
(redrawn from Peck et al., 2004b). The hatched line represents a representative rate for the respective temperate species, set to 1. Boxes
show the range and mean of values. Note that the comparison does not consider the existence of more active lifeforms in temperate waters.
water and possess much higher magnesium levels
than in fish. Lower activity levels in Antarctic
invertebrates may thus relate to enhanced Mg2+induced muscular relaxation at cold temperatures.
As a general constraint, high magnesium levels may
contribute to limit routine physiological rates of
polar to below those of temperate marine invertebrates. However, it needs to be emphasized that
performance levels in the Antarctic cold are limited
not only in invertebrates and not only due to high
magnesium levels but also due to permanently low
temperatures. High performance levels as among
fish are excluded from the Antarctic (Clarke, 1998).
These generalizations reflect the need to look more
closely at the patterns and trade-offs of thermal
adaptation characterizing Antarctic fauna (see for
example patterns in Fig. 8).
3. Trade-offs in the processes and limits of thermal
adaptation
Mechanisms setting aerobic and functional scope
especially the adjustment of O2 supply capacity and
of the functional capacity of tissues appear crucial in
climate-dependent evolution in general (Pörtner,
2001, 2002a, 2004) and also in Antarctic evolution.
The underlying systemic to molecular mechanisms of
adaptation and the associated tradeoffs (cf. Pörtner
et al., 2005c) are thus key to understand the
specialization of polar fauna on limited thermal
windows. Adjustments in oxygen supply occur
through the setting of ventilatory and circulatory
capacities, of blood oxygen transport, of tissue
capillarization and of mechanisms of cellular oxygen
flux to mitochondria. On the demand side, functional adjustments to temperature occur in all tissues
including circulatory and ventilatory muscles and O2
demand usually rises with functional capacity.
In Antarctic species, function but not necessarily
functional capacity is maintained in the permanent
cold. This includes cold compensation to various
degrees of nervous conduction, of muscular force,
of excitation/contraction coupling, of oxygen transport pathways with a special role for lipids, of ion
and pH regulation, of mitochondrial density and
costs, of mitochondrial capacity and kinetics, of
aerobic enzyme concentrations as well as their
capacity and kinetics. Adjustments in function and
capacity need to be addressed at various, molecular,
membrane, cellular, tissue, whole organism and
ecosystem levels and the findings interpreted from
an integrative point of view (cf. Figs. 2 and 3).
3.1. Energy turnover in stenotherms and eurytherms
An integrative point of view implies that understanding the special functional features of Antarctic
marine ectotherms is associated with the key
question of why thermal tolerance windows display
different widths in ectotherms and why windows are
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
-1
-1
ATP turnover (µmol h g )
40
Antarctic
eelpout
(0 °C)
30
Rainbow
trout
(15°C)
Excess Post-exercise
Oxygen Consumption
(calculated)
20
gluconeogenesis
10
ATP resynthesis
Rest
rephosphorylation
of creatine
0
8
Rest
EPOC
-1 -1
Oxygen consumption (µmol h g )
Rest
trout
(calculated)
6
trout
4
eelpout
2
eelpout
1083
over in colder climates at high (Southern) latitudes
(e.g., in perciform fishes). While early papers
postulated full cold compensation of metabolic
energy turnover (Scholander et al., 1953; Wohlschlag, 1964), more recent work, starting with the
landmark paper by George Holeton (1974), provided no evidence for metabolic cold adaptation
(sensu Krogh) in Antarctic and (high) Arctic fish
(Clarke and Johnston, 1999; Steffensen, 2002;
Fig. 9) and in Antarctic invertebrates (Peck and
Conway, 2000). Comparisons across latitudes of the
metabolism of species at their normal habitat
temperatures show a monotonic decrease from
tropical to polar species.
These analyses, however, may not explain all
variability observed. Especially viewing the data
compiled by Clarke and Johnston leads us to ask
whether Antarctic variability as well as peculiarities
are fully explained by the statement that there is no
metabolic cold compensation? Levels of energy
turnover are variable, some functions are cold
compensated (see Fig. 8) and this variability
may relate to some variability in the widths of
thermal tolerance windows (see above). A more
Fig. 8. A role for cold-compensated aerobic capacity in causing
high EPOC in Antarctic fish during recovery from muscular
exercise. High EPOC results in Antarctic eelpout (0 1C, Pachycara brachycephalum, Antarctic peninsula) compared to coldacclimated eelpout from the North Sea (0 1C, Z. viviparus,
bottom). Despite much lower rates of ATP turnover during rest,
EPOC results almost as high as in rainbow trout (15 1C) (top,
data adopted from Scarabello et al., 1992; Hardewig et al., 1998;
van Dijk et al., 1998) and contributes to faster removal of lactate
and gluconeogenesis, earlier repletion of phosphocreatine, ATP
resynthesis and faster recovery from intracellular acidosis in
white muscle.
narrow especially in cold-adapted (Antarctic) stenotherms. Uncovering the selective advantage of
this specialization will be relevant in understanding
molecular to whole animal functional properties
and their lifestyle consequences.
Over the last decades analyses have focussed on
the question whether cold adaptation is linked to
changes in energy turnover. Comparisons of
ectotherms from various latitudes and climates have
revealed a universal trend to decrease energy turn-
Ln (Resting O2 consumption, mmol h-1 )
15 °C
Antarctic 0 °C
North Sea 0 °C
15 °C
Antarctic 0 °C
North Sea 0 °C
0
1
0
-1
Higher
aerobic
scopes
-2
-3
Increasing
widths of
thermal
windows?
-4
3.2
3.3
3.4
3.5
3.6
3.7
Inverse temperature (K-1 x 103 )
Fig. 9. Resting oxygen consumption rates (SMRs) in perciform
fishes from various latitudes (after Clarke and Johnston, 1999),
depicted in an Arrhenius plot. Note that the variability between
species remains more or less unchanged across temperatures,
indicating variability between lifestyles which appears to be as
large in the Antarctic notothenioids (filled symbols) as in other
perciform fish species at lower latitudes (open symbols). This
would suggest the existence of variable thermal windows in
relation to variable aerobic scopes according to lifestyle requirements. On average, the data show no evidence for metabolic cold
adaptation (sensu Krogh) but they show a lower Q10 of the
between species relationships than usually found in within species
acclimation studies (for further discussion see text).
ARTICLE IN PRESS
1084
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
comprehensive picture may arise from comparisons
of species in various climates, taking into account
that climates and temperatures are more variable in
the Northern than in the Southern hemisphere
(Gaston and Chown, 1999), likely eliciting different
patterns of thermal adaptation. More specifically,
what is the difference between temperate to (sub)polar eurytherms (esp. sub-Arctic) and Antarctic
stenotherms?
Starting with the early work by Vernberg (1959),
Vernberg and Vernberg (1964), Vernberg and
Costlow (1966) on fiddler crabs, Uca sp., from
different latitudes, comparisons of congeneric species and species populations have shown significant
metabolic cold-adaptation in invertebrate and fish
populations in a Northern hemisphere latitudinal
cline. Recent evidence confirms such patterns in
Eastern populations of Atlantic cod (G. morhua), in
populations of intertidal lugworms, Arenicola marina (Sommer and Pörtner, 2002), in intermediate,
reproductive age classes of mussels, Mytilus edulis
(Sukhotin et al., 2006), but not in intertidal
(semiterrestrial) Littorina saxatilis populations
(Sokolova and Pörtner, 2003). Elevated metabolic
rates have been associated with observations of a
downward shift of critical temperatures in coldadapted populations of a species (Sommer and
Pörtner, 2002; T. Fischer, R. Knust, H.O. Pörtner,
unpublished). The width of summer thermal windows was maintained, likely due to high temperature variability at high Northern latitudes.
However, such patterns were not observed in
populations of Atlantic silverside in the Western
Atlantic (Billerbeck et al., 2000), possibly due to less
temperature variability in this area, in the absence
of thermal effects of the Gulf stream. Windows also
were found narrower and at a lower metabolic rate
in A. marina during winter (Wittmann, 2005). As a
corollary, metabolic cold adaptation requirements
may rise with local temperature variability and with
active lifestyles (e.g. in amphibious fiddler crabs or
A. marina and cod during summer). The cost of cold
adjustments may be minimized by the use of
metabolic depression strategies as during passive
tolerance of air exposure or during hibernation at
more stable winter temperatures (Sommer and
Pörtner, 2004).
The physiological differences observed between
Southern and Northern populations are permanent,
associated with significant genetic differences. Differences also extend not only to differences in
metabolic capacities associated with different en-
zyme capacities but also to temperature-related
differences in the allele frequencies and functional
properties of enzymes like NADP-dependent isocitrate dehydrogenase or phosphoglucomutase
(Hummel et al., 1997).
3.2. Kinetic background of stenothermy versus
eurythermy
In general, specialization on temperature is
related to the specialization of membranes as well
as of proteins on temperature (Hochachka and
Somero, 2002). Associated trade-offs in molecular
adjustment are seen in the kinetic properties of
enzymes in metabolic pathways, in the leakiness and
homeoviscous adaptation of membrane structures,
in the stability of functional proteins and thereby
the cost and capacity for protein turnover (for
further detail see Pörtner et al., 2005a). Metabolic
regulation at low temperatures in general, is
supported by the cold compensation of enzyme
kinetic parameters like substrate affinities and
turnover numbers, through minute structural modifications of the enzyme molecule. These involve a
shift in protein folding, sometimes supported by the
replacement of individual amino acids. Protein
specialization is reflected in an increased catalytic
rate constant (K) as seen in A4–lactate dehydrogenases, or in a conservation for Km regardless of
temperature, a classical example being the Km for
pyruvate of pyruvate kinase (Somero, 2003). In the
cold, protein flexibility may have to be enhanced for
these adjustments, at the expense of reduced
stability (Fields, 2001). These solutions may be
found combined or in isolation depending on the
protein investigated such that a uniform trend for
Kcat or Km (Vetter and Buchholz, 1998) or even for
protein stability is not visible (Zakhartsev et al.,
2004). One former paradigm, namely that cold
adaptation should typically involve a drop in
activation enthalpy to facilitate enzyme turnover
in the cold, does also not hold as a unifying
principle. A shift between the uses of metabolic
pathways may occur with changing temperature and
be supported by decreased or increased activation
enthalpy. Increased activation enthalpies were observed in some regulatory enzymes (cf. Pörtner et
al., 2000) and also in equilibrium enzymes like
lactate dehydrogenase (Zakhartsev et al., 2004) and
have been interpreted as a mechanism for the downregulation of metabolic pathways, in this case the
glycolytic pathway in the cold (see below).
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
An integrative approach would lead to the
questions what the consequences of these molecular
patterns are at higher functional levels and whether
these patterns explain the metabolic background of
elevated energy demand in cold-adapted eurytherms
on the one hand, or of the down-regulated energy
demand in Antarctic stenotherms on the other
hand? Studies of mitochondrial capacities in Antarctic notothenioids revealed extremely high mitochondrial densities at uncompensated capacities
(Johnston, 1989; Johnston et al., 1998). Mitochondria isolated from Antarctic fish liver and also from
marine invertebrates were highly coupled at low
capacities and low levels of proton leakage rates,
thereby indicating low costs of mitochondrial
maintenance (Hardewig et al., 1999a; Pörtner
et al., 1999b; cf. Fig. 4). These features are likely
relevant in setting metabolic rates of Antarctic
stenotherms low. In contrast to Antarctic stenotherms, moderate mitochondrial densities with
high capacities and costs owing to high proton
leakage rates appear to characterize cold-adapted
eurytherms from high northern latitudes (Pörtner et
al., 2000; Tschischka et al., 2000; Sommer and
Pörtner, 2002; Fischer, 2003) and their level of
metabolic cold adaptation. These enhanced mitochondrial ATP synthesis capacities reflect the level
of cold compensated aerobic scope. Accordingly,
wide thermal tolerance windows and associated
high levels of standard metabolic rate (SMR) in
northern hemisphere eurytherms have been hypothesized to support active lifestyles and high
exercise capacities (Pörtner, 2002b, 2004).
However, Fig. 9 already shows that not all
Antarctic fish species are created equal: we find
variable SMRs in fish as much as they are variable
in other areas according to lifestyle requirements.
Accordingly, functional capacities may differ according to mode of life and, thus, may influence the
width of the thermal tolerance window. This
hypothesis needs to be re-examined as direct
estimates of pejus temperatures and of temperature-dependent performance are not commonly
available.
The question arises whether there are metabolic
design features that elicit different widths of oxygen
and capacity-limited thermal windows in eurytherms or stenotherms and, at the same time,
define the baseline level of energy turnover? More
specifically, are narrow thermal windows a result of
low SMR in cold stenotherms due to specific
mechanisms of metabolic down-regulation? As
1085
thermal limits are set by a mismatch of oxygen
supply capacity vs. demand, steeper increases in
costs or oxygen demand with warming or low
capacities for oxygen uptake and distribution as
associated with low SMRs would, in fact, contribute
to narrow windows. So the mirror-image question
for an explanation of eurythermy in the cold is:
Why is SMR elevated and does this involve specific
mechanisms of thermal independence in active cold
eurytherms? As thermal limits are first set by a
mismatch of oxygen supply capacity vs. demand,
wide thermal windows should involve moderate
increases in costs or oxygen demand with warming.
In line with the insight derived from Figs. 2–4 the
dichotomy of eurytherms and stenotherms makes it
very clear that narrow windows of thermal tolerance
as in stenotherms are not enforced by trade-offs in
thermal adaptation of molecules alone, as eurytherms can adapt to live at the same temperatures
as Antarctic stenotherms. This leads us to ask for
specific mechanisms that cause a narrowing of the
windows of oxygen limited thermal tolerance.
There is very little information on the kinetic
background of stenothermy versus eurythermy and
associated trade-offs in energy turnover. The
temperature dependence of mitochondrial proton
leakage rates in the Antarctic notothenioid fish
(Fig. 4B) or bivalves suggests a high thermal
sensitivity of proton leakage in Antarctic stenotherms (Hardewig et al., 1999a; Pörtner et al.,
1999b), higher than found in many studies of
temperate eurythermal mitochondria. This provides
evidence for a high Arrhenius activation energy
(EA), which mirrors the free enthalpy of activation
DHz and thus the kinetic barrier of this process.
Setting the enthalpy term of a process high, despite
cold temperature, already has been mentioned as a
mechanism of metabolic down regulation (Pörtner
et al., 2000; Fig. 10). In the case of mitochondrial
proton leakage this mechanism may contribute to
explain the link between a low SMR and functional
capacity and a high thermal sensitivity in oxygen
demand as a basis for narrow tolerance windows in
Antarctic stenotherms. By use of this mechanism
the organism would save energy despite high
mitochondrial densities. The hypothetical nature
of this statement is underscored by the fact that the
molecular nature of the mitochondrial proton leak
remains unidentified as are the molecular mechanisms eliciting such high thermal sensitivity.
Such differences in the thermal dependence of
mitochondrial oxygen demand lead to the expectation
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
1086
(A)
Enzyme density
cold compensated
‡
H
cold compensated
‡
H
essed
depr
eurytherm
Metabolic
flux
stenotherm
Temperature
SMR or SMR component
(B)
Thermal window
Eurytherm: High SMR,
high capacity for
oxygen supply,
‡
low H
Stenotherm: Low SMR,
low capacity for
oxygen supply,
high H‡
Temperature
Fig. 10. A role for activation enthalpy DHz in balancing the cost
of metabolic cold adaptation (A, after Pörtner et al., 2000) and in
setting thermal tolerance (B). Arrhenius activation energy (EA)
mirrors the free enthalpy of activation DHz and thus the kinetic
barrier of a process. Setting the enthalpy term of a process high,
despite cold temperature, may be used as a mechanism of
metabolic down regulation under conditions when enzyme
density is cold compensated. Conversely, setting DHz low is
associated with cold compensation, as in eurytherms. High levels
of Arrhenius activation energies (activation enthalpies) at
various, molecular to organ to whole organism levels of
biological organisation may thus contribute to stenothermy (B).
They would explain an earlier drop in aerobic scope of the whole
organism in the warm and, thereby, a narrowing of the thermal
tolerance window. A cold-adapted stenotherm may display low
SMR due to high DHz, and also a low capacity for oxygen
supply, leading to a high EA for circulatory cost upon warming.
that they may shape whole-animal oxygen consumption. Contrasting changes in whole-animal oxygen
demand have been observed during eurythermal vs.
stenothermal adjustment to cold in various eelpout
species (Zoarcidae). Upon cold acclimation and
latitudinal cold adaptation in temperate zone Z.
viviparus, SMR clearly showed a lowering of EA and
thus a smaller thermal response of energy turnover
(van Dijk et al., 1999; Zakhartsev et al., 2003), in line
with eurythermal adjustment to cold. In field
collected, cold-adapted Antarctic eelpout (Pachycara
brachycephalum) analysed after short-term aquarium
maintenance, whole-animal SMR proved to be more
temperature dependent and thus EA higher than in
the temperate zone species acclimated to cold (van
Dijk et al., 1999), in line with (more) stenothermal
cold adaptation. However, an explanation based on
mitochondrial characteristics may be too simple.
Lannig et al. (2005) showed that Arrhenius activation
energies of proton leakage in liver mitochondria did
not differ between groups of Antarctic eelpout
acclimated to 0 and 5 1C or between groups of North
Sea eelpout acclimated to 5 and 10 1C. Similar Q10
and EA values of mitochondrial respiration rates
but higher Q10 and EA values of in vivo SMRs of
P. brachycephalum compared to cold-acclimated
Z. viviparus suggest that mitochondrial functional
properties do not fully explain the pattern of whole
animal respiration at various temperatures. In the
Antarctic bivalve Laternula elliptica oxygen consumption rates mirrored the high thermal increment
in mitochondrial proton leakage (Q10 about 4.2,
Pörtner et al., 1999b) during initial warming (Q10
between 4 and 5, Peck et al., 2002), but no longer in
the acclimated rates of oxygen consumption. Considering the early onset of oxygen and muscular
performance limitation in this species during acute
warming (Fig. 5) suggests that oxygen supply falls
short of resting metabolic rate and mitochondrial
oxygen demand early on provoking an early fall in
residual aerobic scope (Fig. 2B).
Moreover, high activation enthalpy values of
baseline oxygen demand may not necessarily or not
only result at the level of molecular, organellar or
cellular functioning, but also may be set at higher
levels of biological organisation. In line with this
conclusion, Mark et al. (2002) showed in the
Antarctic eelpout that the EA of whole animal
SMR was reduced when specimens were exposed to
rising temperatures under hyperoxia rather than
normoxia. Their study provided evidence that
excess oxygen availability reduces the workload of
the circulatory system and, thereby, lowers the
increment in SMR during warming. The temperature dependence of the costs of oxygen supply
through circulation is thus influenced by oxygen
availability and modulates the change in SMR with
temperature. In the Crustacean example, the experimental reduction of [Mg2+]e in some reptant
decapods also reduced the thermal sensitivity (EA)
of whole animal oxygen consumption, in this case
by raising SMR in the cold, associated with elevated
heart rates and elevated haemolymph supply to
tissues (Fig. 6, Frederich et al., 2000a). Enhanced
motor activity of the animals in the cold indicates
that the reduction of [Mg2+]e enhances functional
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
capacity, at the expense of elevated metabolic costs
in the cold.
The question arises how the temperature-dependent costs of circulation are modified by adaptation
and thereby co-define the width of the thermal
window. The cost of oxygen transport to tissues
depends on demand, on tissue capillarisation and on
the concentration of oxygen in the body fluids, i.e.
the combined oxygen quantities dissolved and
bound to pigment. Antarctic ectotherms benefit
from high oxygen solubilities in the cold and
notothenioid fish have thus reduced the contents
of blood pigment, mirrored by low haematocrit. In
a principle trade-off between the levels of cardiocirculatory workload and of blood pigment concentration (haematocrit) and capillarity, the latter
two should be set to levels allowing for efficient
oxygen supply at a workload as low as possible. In
largely resting animals with low aerobic scopes as in
cold-adapted stenotherms the emphasis is on low
baseline circulatory costs during rest. In this case
circulatory systems are low capacity (low capillarisation and low haematocrit) systems, which operate
at a lower cost at rest than high performance
systems. In fact, Antarctic notothenioids display a
two- to three-fold lower capillary to fibre ratio than
sub-Antarctic notothenioids and Mediterranean
perciform fishes indicating reduced capillary supply
in the permanent cold (Egginton et al., 2002). Low
or even absent blood pigment levels also characterize Antarctic notothenioid fish, especially channichthyids, and are, on average, combined with a
low-pressure, low-resistance cardiovascular system
operated by larger hearts at low heart rates and
high-volume output (Wells et al., 1980; Egginton,
1997a, b; Axelsson, 2005). Upon rising oxygen
demand during warming and exercise, a higher
circulatory workload would have to compensate for
then deficient blood pigment levels and function and
would thereby cause a rapid rise in circulatory costs
upon warming. The limits of cardiovascular scope
would soon be reached, and this would cause an
early loss in aerobic scope in the warm and
contribute to narrow thermal windows.
A simple analysis of circulatory performance in
relation to tissue capillarisation and blood flow may
provide further insight. Blood flow to tissues
depends on capillary density, i.e. the number of
capillaries, i, and, according to the law of Hagen
Poiseuille, on capillary diameter. Flow rises with i
times the radius to the power 4 for each capillary
under the simplifying assumption, that the pressure
1087
difference driving flow, and blood viscosity are
maintained. Flow thus depends linearly on the
number of capillaries and, to the power 4, on
changes in radius of each of i capillaries in the
capillary bed. While the capillary to fibre ratio is
two to three-fold lower in Antarctic notothenioids
than in warmer water perciform fish, vessels in redblooded nototheniids are somewhat larger than in
the average vertebrate. Channichthyids even display
1.5 times larger capillary diameters than their redblooded congeners (Egginton et al., 2002). Egginton
et al. (2002) elaborated that wide-bore capillaries
support maintenance of tissue oxygenation in the
absence of respiratory pigments due to enhanced
capillary surface. Enhanced capillary diameters also
suggest that resistance to flow is reduced in both the
red blooded nototheniids and even more so in the
channichthyids. In the light of reduced capillary
density, this feature should support energy savings
in blood circulation in the permanent cold. Upon
warming, however, large diffusion distances due to
fibre hypertrophy and low capillary-to-fibre ratios
would again cause an early mismatch between
supply and demand. Overall, energy savings have
been realized in Antarctic fish through circulatory
design but at the expense of limited capacity to
match rising oxygen demand upon warming.
In contrast, high capacity circulatory systems
would operate at elevated resting costs, but would
provide enhanced efficiency upon additional work
loads. These expectations are supported by comparisons of high performance fish, where heterothermic, i.e. eurythermal scombrid fish display high
resting rates of metabolism, but low metabolic
increments upon increased swimming velocity. Due
to the involvement of high performance circulatory
systems, they also reach higher steady speeds than
ectothermal scombrids or salmonids (Korsmeyer et
al., 1996; Katz, 2002). Cold-adapted eurytherms
were discussed to follow similar patterns and to be
pre-adapted to enhanced exercise levels (Pörtner,
2002b). The comparative cardio-circulatory mechanics and performance of cold-adapted eurytherms and stenotherms remains largely
unexplored, interest has focussed on polar versus
temperate species (Axelsson, 2005). A comprehensive comparative picture of tissue design including
capillarity changes in various populations of eurythermal ectotherms from a temperate to polar
latitudinal cline is also not available; work has
focused on seasonal cold acclimatization patterns
(cf. Guderley, 2004, for review). These may involve
ARTICLE IN PRESS
1088
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
winter phenomena of metabolic adjustments to
limited food availability or to reduced activity levels
(see above). Accordingly, the role of variable
climates in setting the contribution of cardiovascular performance to thermal tolerance still needs to
be developed.
As a generalized conclusion, high Arrhenius
activation energies are conceivable at various,
molecular to organ to whole organism levels of
biological organisation in stenotherms and, together
with reduced functional capacity, would explain an
early drop in aerobic scope of the whole organism in
the warm and, thereby, a narrowing of the thermal
tolerance window in Antarctic stenotherms. A coldadapted stenotherm may display low SMR due to
high DHz, and a low capacity for oxygen supply.
High activation enthalpy DHz may thus balance the
costs of metabolic cold adaptation (Fig. 10). In
contrast, metabolic increments elicited by rising
temperature must be kept small in eurytherms in
order to maintain aerobic scope in the warm.
Eurytherms are exposed to the full cost of metabolic
cold adaptation because they need to make use of
their mitochondria and because they need to have
aerobic scope available within the widest possible
range of short-term ambient temperature fluctuations. As a precondition, and in contrast to the
situation in stenotherms, this minimizes the degree
to which temperature-dependent kinetic barriers
like high activation enthalpies can be established
for various processes like proton leakage or
circulatory costs. A cold-adapted active eurytherm
thus displays high SMR due to low DHz, associated
with a high capacity for oxygen supply. Elevated
SMRs then translate into higher capacities for
aerobic muscular performance. At the same time,
they require enhanced cost efficiency with work load
increments as imposed by higher temperatures. This
is likely paralleled by an enhanced cost-efficiency of
circulation such that a lower Arrhenius activation
energy of circulation may result. As much of this
picture is hypothetical, unravelling the role of
circulatory capacity and efficiency in setting thermal
windows and temperature-dependent energy budgets would thus need extensive comparative investigation.
3.3. Setting aerobic scope: gene expression in
stenotherms versus eurytherms
The level of aerobic energy turnover crucially
depends on the rate of energy provision by aerobic
metabolic pathways. Cold compensation of aerobic
enzyme capacities has been observed in Antarctic
and (sub-) Arctic as well as in cold-acclimated
temperate species (Pörtner et al., 2005a). However,
studies of the regulation of this process including
gene expression of aerobic enzymes are in their
infancy. Study of the expression of cytochrome c
oxidase in the white musculature of eelpout from
North Sea and Antarctica demonstrated higher gene
expression levels in cold-acclimated eurythermal
North Sea than in cold-adapted Antarctic eelpout
(Hardewig et al., 1999b; Fig. 11). Among populations of eurythermal cod (G. morhua) in a latitudinal
cline gene expression capacity of white muscle
aerobic enzymes was found higher in a comparison
of cold eurythermal cod from the Barents Sea than
in a temperate cod population from the North Sea
(Lucassen et al., 2006). These findings indicate that,
on the one hand, stenothermal cold adaptation of
Antarctic species may be associated with lower gene
expression levels of aerobic enzymes than eurythermal cold acclimation and, on the other hand, that
gene expression capacity may correlate with the
degree of eurythermal cold adaptation. This conclusion needs further substantiation by analyses in
other species; however, the patterns observed mirror
the changes observed in the content of mitochondria
and in their functional capacity (see above). Such
analyses have become even more relevant in the
light of recent findings that thermal acclimation
capacity still exists in Antarctic fish, including
zoarcids (Lannig et al., 2005) and notothenioids
(Seebacher et al., 2005).
In the Antarctic eelpout, modulation of gene
expression in response to temperature has been
demonstrated to affect not only the levels and
capacity of citric acid cycle and respiratory chain
enzymes but also of uncoupling proteins (UCP) (F.
Mark, M. Lucassen, H.O. Pörtner, unpublished).
UCP may play a role in the temperature-dependent
setting of organismal energy turnover. Therefore,
the genes and expression of fish UCP were
investigated in the Antarctic eelpout Pachycara
brachycephalum and a temperate confamilial species, the common eelpout Z. viviparus. Protein
sequences of zoarcid UCP were found closely
related to other fish and to mammalian UCP2.
Expression of UCP2 was enhanced during cooling
from 10 to 2 1C in the common eelpouts, in line with
cold induced mitochondrial proliferation. However,
UCP mRNA and protein levels were also found
increased in Antarctic eelpout which had been
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
COX activity
0.5
*
0.4
U g-1 wet wt.
1089
0.3
0.2
0.1
3
*
3
2
1
normalized COX activity
COXI mRNA levels
4
2
North Sea 0°C
Antartic 0°C
North Sea 0°C
Antarctic 0°C
North Sea 18°C
1
0
0
North Sea 18°C
COX I (rel. amount g-1 wet wt.)
0.0
0
1
2
normalized COXI mRNA
3
Fig. 11. Cytochrome c oxidase (COX) activity and expression of sub-unit I in the white musculature of eelpout from the North Sea (Z.
viviparus, acclimated to cold or warm) and from Antarctica (P. brachycephalum). Left: COX activity levels parallel the level of
mitochondrial transcripts, however, values normalized to tissue wet mass (on the right), indicate an overproportional accumulation of
mRNA in cold-acclimated Z. viviparus (after Hardewig et al., 1999a).
warm-acclimated from 0 to 5 1C. Despite a concomitant decrease in mitochondrial protein content
in Antarctic eelpout (Lannig et al., 2005) UCP levels
rose upon warm acclimation by a factor up to 2.0
(mRNA) and 1.6 (protein). Changes in UCP
expression indicate that this protein may play a
role during exposure and acclimation to cold as well
as warm extremes, but levels do not necessarily
parallel the level of energy turnover. According to a
recent hypothesis UCPs may respond to enhanced
mitochondrial formation of reactive oxygen species
(ROS) by causing mild uncoupling of mitochondria
through enhanced proton leakage (Echtay et al.,
2002). They may thus control the mitochondrial
membrane potential to balance ROS formation
during thermal stress. This function would be in line
with the oxygen-limitation hypothesis and the
postulated increase of ROS formation during
temperature induced hypoxia (Pörtner, 2002a; Heise
et al., 2006). However, it needs to be emphasized
that this is likely a safety mechanism and the
mechanism causing the baseline rate of mitochon-
drial proton leakage still remains unidentified and
unexplained. The data rather provide evidence that
mitochondrial composition and functional properties change upon thermal acclimation not only in
temperate but also in Antarctic fish.
In the context of the oxygen limitation concept,
not only enhanced gene expression patterns of
aerobic enzymes or of UCP are relevant but specific
features of oxygen supply to tissues are also
reflected in the loss of myoglobin (Mb) or haemoglobin expression in icefish (Channichtyidae) and
the mechanisms behind (di Prisco et al., 2002; Small
et al., 2003; Grove et al., 2004). Loss of haemoglobin expression arose from a single, large-scale
deletion of all icefish globin genes with the exception
of a truncated, transcriptionally inactive a1-globin
gene. Loss of cardiac Mb, not known in coldadapted eurytherms, occurred independently more
than four times in six of the 16 species of Antarctic
icefish. The different mechanisms found all prohibit
transcription, despite the presence of the respective
DNA message. In the notothenioid hearts which
ARTICLE IN PRESS
1090
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
express Mb, loss of Mb means a loss of functional
capacity (Acierno et al., 1997). However, changes in
cardiac and cellular structure of icefish compensated
for this loss (see below). The exclusive nature of
these phenomena suggests that only under the cold,
highly oxygenated conditions of the Southern
Ocean were such rearrangements of oxygen supply
pathways possible and are sustaining survival.
These modifications may even provide selective
advantages (for a discussion of selective advantages
see below). Survival without haemoglobin or Mb
was secured not only due to cold temperatures but
also due to elimination of high-performance ectothermal lifeforms as competitors or predators. In
the future, such gene expression studies will be
highly relevant to understand the mechanisms and
pathways of evolutionary temperature adaptation
(cf. Pörtner, 2004).
3.4. Setting aerobic scope: trade-offs in cell structure
and functional capacity
Activity levels in Antarctic ectotherms are low to
moderate only, despite extreme mitochondrial contents. In cold-adapted slow aerobic muscle fibres of
Antarctic notothenioids mitochondrial densities
450% are among the largest if not the largest seen
in vertebrate skeletal muscle (Johnston, 1989).
These high densities go hand in hand, with an
emphasis on aerobic energy production and reduced
anaerobic capacity, at least in pelagic lifeforms;
however, muscular force per muscle cross sectional
area is reduced due to reduced myofibrillar density.
More fibres need to be recruited for the same
workload. The question arises whether and why
such a large mitochondrial volume and network is
needed at moderate activity levels in fish? In the
light of the concept of oxygen and capacity limited
thermal tolerance four explanations appear possible: large mitochondrial networks are related to
(1) the overcoming of enhanced diffusion limitations
for oxygen as part of a general response to
restricted diffusion in the cold (Sidell, 1998)?
(2) the energy saving distribution of oxygen by
enhancing oxygen diffusion and by alleviating
the workload on ventilatory and, especially
circulatory systems?
(3) the provision of high aerobic capacity despite low
SMR? Large mitochondrial networks also may
have a kinetic background and support cost
efficient energy turnover. It is clear that more
low than high-capacity mitochondria would be
needed for the same cellular tasks and their
maintained rates. Low-capacity mitochondria as
in Antactic ectotherms may be more tightly
coupled (Hardewig et al., 1999a; Pörtner et al.,
1999b) and, thus, provide the same service at a
lower baseline cost. Therefore,
(4) if a reduction in SMR and associated energy
production by mitochondria is supported by
elevated levels of activation enthalpy, largely
elevated mitochondrial densities may balance
this process, as a principle trade-off in cold
adaptation?
Evidence for hypothesis (1) or (2) might arise from
comparative studies of muscle morphology in
various species of Antarctic fish. The comparison
of fish with and without the presence of oxygen
binding proteins is particularly promising in this
context. Recent work by O’Brien et al. (2003) showed
lower mitochondrial densities (25%), larger cristae
surface densities (37.7 m1), smaller cells (2103 mm2),
and larger capillary density in the red-blooded
nototheniid G. gibberifrons than in the ‘‘white’’blooded channychtiid C. rastrospinosus, which displayed a higher mitochondrial density (53%), lower
cristae surface density (25.5 m1), larger cells
(9352 mm2), and lower capillary density. When taking
these different characteristics into account, cristae
surface area per unit muscle mass is conserved in
both species at approximately 9 m2 g–1. Adopting
mass specific cristae surface density as a correlate of
aerobic capacity these findings clearly support
Sidell’s hypothesis and hypothesis (1) in that larger
mitochondrial densities replace lost myglobin and
haemoglobin and support oxygen flux into the cell.
At first sight, this compensates for diffusion limitations that are also emphasized by larger cells and
lower capillary density. Icefish muscle design may
then be the result of oxygen limitations in the cold.
However, this hypothesis (1) does not explain why
oxygen-binding pigments were lost in the first place,
why cells are large and capillarity is less.
This apparent contradiction may be solved if an
alternative explanation (2) is considered namely, that
a loss of Mb and Hb, associated with large cell sizes,
with a high density of mitochondrial membrane
networks and with a low mitochondrial capacity, as
well as with low SMR are indicative of excessive O2
supply at low cellular costs (Pörtner, 2002b; Pörtner
et al., 2005a). In more detail, the pressure on
maintaining Mb function is reduced at high oxygen
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
availability, as the role of Mb is replaced by high
oxygen solubility in the cold cytosol and in membrane
and other lipids. The reduction in oxygen diffusibility
in the cold is in fact overcompensated due to excessive
lipid accumulation. A cold-induced rise in lipid
synthesis, especially at high mitochondrial densities
as in pelagic organisms (Pörtner, 2002b) might trigger
the over-proportional increase of oxygen supply in
the cold. However, Mb would not only be made
redundant by lipids and their high capacity for
oxygen solution and diffusion. This trend is enforced
by the over-arching trend in Antarctic species to
reduce energy turnover and thus oxygen demand,
linked to a low-capacity circulatory system (see
above). Larger cell sizes go hand in hand with this
trend. Due to reduced cellular membrane surface
areas in relation to cellular volume, the amount of
maintenance work through ion exchange across
membranes is reduced, but at the same time the
capacities of the cells to be responsive to external
stimuli are reduced. All of these findings indicate
reduced energy demand despite enhanced O2 availability, at the expense of reduced functional capacity.
This then will also reduce the workload of convective
O2 supply and contribute to the loss of haemoglobin
function in the icefish, which is thus not only
supported by enhanced oxygen solubility in the cold.
In conclusion, shifting to reduced convective and
to enhanced passive diffusive O2 supply supports
enhanced energy savings at progressively increasing
ambient O2 availability. This conclusion is in line
with hypothesis (2) rather than hypothesis (1): high
mitochondrial networks relate to excessive lipid
biosynthesis and the energy saving distribution of
excess oxygen (by enhanced diffusion), rather than
to compensation of reduced oxygen availability.
This shift thereby supports the evolution of low
energy turnover modes of lifestyle. The contrasting
trends of compensatory adjustments seen in Mb
deficient mice also corroborate these conclusions
(Gödecke et al., 1999). These mice respond to Mb
loss by increased cardiac capillarisation at unchanged mitochondrial density and aerobic capacity. These patterns clearly counterbalance the
threat of hypoxia and, thereby, contrast the situation in Antarctic fish.
3.5. Exploiting aerobic scope: trade-offs in energy
allocation to slow versus fast functions
Addressing hypotheses (3) and (4) requires a
consideration of the various whole organism phy-
1091
siological processes that are fuelled by aerobic
metabolism. A general trend to reduce baseline
aerobic energy turnover and scope and the level of
muscular performance already has been elaborated.
Aerobic capacity is also needed to digest and
process a meal. Specific dynamic action (SDA),
the post-prandial increase in oxygen consumption,
has been studied in Antarctic organisms. At small
meal sizes the rate of oxygen consumption rose with
increasing meal size but reached saturation at some
point. Maximum SDA was found to be characterized by moderate factorial scopes and significant
extension over time, the total size of the SDA
response remaining unchanged (Peck, 1998). It
needs to be considered that factorial increments of
metabolism start, on average, from lower levels of
SMR in Antarctic ectotherms. Furthermore, the
trade-offs observed between oxygen allocations to
digestion or other processes, including exercise in
fish (Boutilier, 1998), suggest a limitation to SDA
scopes. Accordingly, the level of net aerobic scope
available for SDA does not appear to be coldcompensated in Antarctic ectotherms, similar to the
level of aerobic scope available for exercise.
In line with a reduction in aerobic scope these
considerations would lead to the expectation that
growth is also slower in Antarctic ectotherms than
in temperate species. This is true for both mean
annual growth rates (Brey, 1999) and for peak
summer growth rates which are found below or in
the low range of those seen in temperate species
(Brey and Clarke, 1993; Arntz et al., 1994; Kock
and Everson, 1998; Peck, 2002). In a number of
Antarctic nototheniids and channichthyids growth
performance is similar to comparable species from
boreal and temperate waters (Kock and Everson,
1998), with growth rates 3–5 times faster in summer
than in winter (North, 1998). Among invertebrates
some high-latitude Arctic and Antarctic species also
show low annual growth rates, but levels of summer
growth performance as high as seen in comparable
species from lower latitudes (Dahm, 1999; Bluhm,
2001). Others, like juvenile Adamussium colbecki
remain below the summer growth rate of temperate
species (Heilmayer et al., 2005). In some cases, body
mass grown during summer in Antarctic invertebrates is lost during winter starvation despite
variable degrees of metabolic depression (Peck
et al., 2000; Fraser et al., 2002a).
In support of elevated summer growth rates the
capacity for protein synthesis (Storch et al., 2005)
and the rates of cell cycling (Brodeur et al., 2003)
ARTICLE IN PRESS
1092
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
were found cold-compensated in Antarctic fish.
Cold compensated protein synthesis capacity also
was elaborated in Antarctic scallops (Storch et al.,
2003), with unchanged stoichiometric costs of
protein synthesis (Storch and Pörtner, 2003). On
top of a beneficial effect of elevated RNA levels on
translational efficiency (Whiteley et al., 1996;
Robertson et al., 2001; Marsh et al., 2001; Fraser
et al., 2002b), the RNA translation apparatus is
cold-compensated with enhanced catalytic efficiencies (Storch et al., 2003, 2005), thereby supporting
high cost efficiency as well as high capacity. This
may support not only growth but also elevated rates
of protein turnover due to reduced stability in the
cold as discussed above.
Among pectenid species the overall decrease in
annual growth across latitudes and temperatures is
much less than the decrease in SMR (Heilmayer
et al., 2004), indicating cold-compensation of
growth in relation to metabolic rate. Available
evidence thus indicates that hypothesis (3), which
postulates that high mitochondrial densities elicit
cold-compensated aerobic capacity, cannot be
rejected (Figs. 13 and 14). Moreover, cold compensated growth at low SMR in the cold only can be
achieved if growth exploits a larger fraction of
aerobic metabolism at low temperature (cf. Heilmayer et al., 2004; Pörtner et al., 2005b). There may
even be an aerobic reserve available to slow
functions in Antarctic ectotherms. Juvenile Antarctic scallops displayed slow summer growth at 0 1C,
but an extreme rise in growth rate at 3 1C with a Q10
of 71 (Heilmayer et al., 2005). Similarly, developmental rate also displays higher than usual Q10
values in the cold (10–15, Bosch et al., 1987;
Stanwell-Smith and Peck, 1998), indicating (a) that
higher functions are under tight kinetic control in
the cold, and (b) that small degrees of seasonal
warming may support rapid exploitation of higher
rates, especially of growth. These observations are
in line with hypothesis (3) and (4). They indicate
cold-compensated growth at the expense of other
functions and illustrate the selective pressure in
favour of enhanced energy efficiency in the cold.
Elevated tissue aerobic capacity in the cold may
also have some influence on metabolism during and
after exercise despite limited whole organism aerobic scope. A recent study of exercise performance
and recovery in cold-adapted Antarctic versus coldacclimated temperate eelpout investigated the levels
of anaerobic metabolism and post-anaerobic recovery (Hardewig et al., 1998). In contrast to the
pattern seen among demersal and pelagic Antarctic
fish, the benthic Antarctic zoarcid Pachycara
brachycephalum used anaerobic glycolysis during
exercise to a similar extent as cold-acclimated North
Sea eelpout. During recovery, however, Excess
Post-exercise Oxygen Consumption (EPOC) in
Antarctic eelpout reached far beyond the levels
seen in cold acclimated eelpout from the North Sea,
reflecting enhanced aerobic capacity in the Antarctic species (cf. Fig. 8). As a consequence, lactate
removal resulted faster after anaerobic exercise.
Fast repayment of an oxygen debt within 50–60 min
was observed in the cryopelagic Pagothenia borchgrevinki with more extended periods of lactate
removal (Forster et al., 1987). Despite some cold
compensation of burst performance capacity during
fast start in pelagic or demersal notothenioid fishes
(Franklin et al., 2003), the capacity of anaerobic
metabolism to support longer-term burst activity
appears reduced. This loss is likely not found to the
same extent in benthic Antarctic species (Pörtner
et al., 2005a; Fig. 13).
Overall, enhanced tissue aerobic capacity in the
cold may not be available to support high net
aerobic scopes during exercise or SDA. This is likely
due to overall reduced capacities of muscular
performance and of oxygen supply, for example
related to fibre hypertrophy and reduced capillarity
and circulatory capacity, and also due to an
emphasis on diffusive oxygen pathways. However,
not all physiological rates are reduced to the same
extent in the Antarctic cold. Cold compensated
aerobic capacity at the tissue level still exists
resembling features of high-performance metabolism (Pörtner, 2002b), and may thus become
relevant for slower functions like growth or postexercise recovery. These considerations are in line
with the suggestion of significant cold compensation
of aerobic metabolic capacity in tissues of Antarctic
notothenioids based on enzyme studies (Kawall
et al., 2002; Pörtner et al., 2005a).
4. Driving forces of Antarctic evolution
4.1. Trade-offs and savings in energy turnover: life
history aspects
There are slow functions not found cold-compensated in Antarctic ectotherms, namely life history
functions like reproduction, hatching and larval
development (Arntz et al., 1994; cf. Clarke, 1987).
In the case of echinoids the slowing of development
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
.
.Q
MO2
Antarctic
anae
Temperate
0
rate of aerobic performance
with falling temperature across latitudes was not
linear but rose exponentially (Stanwell-Smith and
Peck, 1998) such that the temperature effect was
drastic at high polar latitudes (see above). These
overarching commonalities elaborated for Antarctic
marine ectotherms strongly point to one key
question: Why have low SMRs been commonly
found in most, if not all investigated ectothermic
animal groups in the permanent Antarctic cold
when compared to their counterparts from warmer
waters? Why have SMRs evolved low despite the
principal cost of cold adaptation? Why pay potential penalties for trade-offs associated with low
energy turnover, like stenothermy, low performance
or, in general, life in the slow lane? The more or less
universal patterns observed suggest that a universal
driving force is operative in the permanent cold.
One major selective advantage becomes evident
from the insight that for the sake of faster growth
rates despite cold temperature, rates of standard
metabolism and thus basal costs of living have to be
low (Heilmayer et al., 2004), indicating cold
compensation of growth at the expense of other
functions. Low metabolic rates in the (stenothermal) cold reflect increased energy efficiency and low
baseline costs, which in turn allows allocation of
elevated energy and substrate quantities to growth
and thus elevated growth performance in stenotherms (Fig. 12). Similar relationships prevail in
fish, where selection for partially cold compensated
growth also enforces excessive energy savings at
cellular and whole organism levels (reduced ion
exchange activities, large myocytes in cardiac and
skeletal muscle, reduction of bones, reduced calcification of the skeleton, gill raker, fin and body
sizes, the use of lipid body stores for neutral
buoyancy, low activity lifestyles; after Eastman
and De Vries, 1982; Ekau, 1988; Dorrien, 1993;
Pörtner et al., 1998; Zimmermann and Hubold,
1998). Although these energy saving strategies are
implemented in pelagic as well as benthic fish,
pelagic lifestyles still seem more costly than benthic
lifestyles as indicated by a lower SMR and faster
growth in the latter (Pörtner et al., 2005a, b). These
patterns clearly indicate that the cold-compensated
growth machinery as outlined above can only be
exploited once reduced energy allocation to other
higher functions supports energy allocation to
growth. The enhancement of growth provides clear
selective advantages at young age, like enhanced
winter survival at larger body size or reduced
pressure from smaller predators. This selective
1093
Tp
Tc
growth
rate
exercise
0
Temperature
Fig. 12. Schematic comparison of thermal windows in a
stenotherm and a temperate eurytherm during summer (cf. Figs.
2, 4 and 10). Metabolic cold adjustments in the Antarctic
stenotherm reduce energy availability due to energy savings and
lead to trade-offs in energy budget. These lead to enhanced
growth efficiency in relation to metabolic expenditure at the
expense of reduced scope for aerobic exercise. A downward shift
in thermal windows and functional optima of the whole organism
occurs as a principal consequence of cold adaptation. During
Antarctic evolution, a maximization of mitochondrial densities
and a minimization of their capacities occurred in parallel with a
narrowing of thermal windows and a loss in exercise performance.
benefit appears to rank so high that even reproductive or developmental rates remain uncompensated
for cold in Antarctic ectotherms.
The trade-off between growth rate and SMR at
low temperature is operative at all life stages, but
especially in larvae. Larvae operate at aerobic
design limits due to small body size such that
synergistic constraints of both cold temperatures
and allometry become operative. High standard and
active metabolic rates of 2 mg larvae of temperate
roach, Rutilus rutilus, are supported by 3- to 4-fold
higher muscle mitochondrial densities than in
juvenile fish (10 g) (Wieser, 1995). In muscle of
smaller fish, in general, citrate synthase capacity
increases and mirrors the progressive increase of
mitochondrial densities (Somero and Childress,
1990). In adult (large) notothenioid fish, some cold
compensation of activity capacity is supported by
mitochondrial densities already close to cellular
space limitations. In larvae, mitochondrial densities
would have to be maximized not only due to cold
but also due to small body size. As a consequence
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
1094
Antarctic:
Eelpout
Notothenioid Fish
Demersal / coastal
fish and squid
Benthic sit and
wait predator
Temperate:
T-specific
organismic aerobic
vs.
anaerobic
capacity
High activity fish
and squid
Cold
adaptation
lar
vae
aerobic
anaerobic
0
Locomotor performance
Fig. 13. Schematic comparison of whole organism aerobic and anaerobic capacities in response to cold versus warm adaptation. Owing to
tradeoffs associated with thermal adaptation groups display different levels of locomotor performance and lifestyle. Use of anaerobic
metabolism is maximized in sluggish benthic or demersal species, minimized in moderately active aerobic cruisers (like the pelagic
Antarctic notothenioids) and enhanced again in high performance fish (and squid) found in warmer waters. Cold adaptation (broken
arrows) elicits reduced performance levels at maximized aerobic design in stenotherms (blue vs. green lines), especially for cold-adapted
larvae as seen in notothenioid fish (see text). Due to cellular space constraints cold adaptation of anaerobic capacity (magenta vs. red lines)
in Antarctic fish only occurs in sit and wait predators whereas in moderately active Antarctic fish anaerobic capacity appears reduced, as a
trade-off in the maximization of aerobic design. (cf. Pörtner, 2002b; adapted from Pörtner et al., 2005a). Note that temperate eurytherms
escape some of the cold adaptation constraints by exploiting warmer summer temperatures.
and for the sake of faster growth, the pressure to
minimize energy expenditure is even more expressed
than in adults (Fig. 13). This would explain
uncompensated low rates of muscular activity seen
in Antarctic fish larvae (Archer and Johnston, 1989;
Johnston et al., 1991) and again an overproportional reduction in developmental rates. In consequence, a mismatch develops at high latitudes
between extended larval development and short
intense periods of primary production, i.e. food
availability (Clarke, 1982, 1987). Larvae thus
appear more uncoupled from food supply rhythms
at high latitudes than in temperate zones (Arntz and
Gili, 2001). This strengthens the primary trade-offs
in energy budget outlined above and, as a consequence, lecithotrophy and inactive, non-feeding
larvae are used as common strategies not only to
bridge the long period of inactivity associated with
extended larval development but also the seasonal
oscillations in food supply. The general trend
towards energy saving modes of larval development
and survival (cf. Poulin and Feral, 1996) thus
would not be due primarily to the slowing
effects of permanently cold temperatures but to
the tradeoffs involved in the maximization of
growth rates. Due to higher rates of energy turnover
among (non-gelatinous) plankton compared to
benthic organisms (e.g. Clarke and Peck, 1991) this
primary trade-off would affect pelagic more than
benthic organisms and would explain why active
pelagic larvae are less frequently found at high
latitudes. Among decapod crustaceans, predominant lifestyle strategies at high latitudes include
passive, non-feeding, or lecithotrophic larvae and
thus, a loss of active planctotrophic larvae (Arntz
et al., 1994; Poulin and Feral, 1996). These relationships may in fact contribute to the loss in
Brachyuran and Anomuran diversity towards high
latitudes (Astorga et al., 2003).
Among reptant decapod crustaceans at high
latitudes these tradeoffs may be emphasized by high
haemolymph magnesium levels (see above) and
explain why endotrophic, food-independent, demersal modes of development are observed in lithodid
crabs in the sub-Antarctic Magellan region. This
may characterize Antarctic lithodids as well (Thatje
et al., 2005). In shrimp with their reduced haemolymph magnesium levels, planktotrophic or only
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
partially food-independent development may be
rather the dominating mode of reproduction,
combined with high starvation resistance. A
strongly abbreviated mode of larval development
(cf. Thatje et al., 2004) may compensate to some
extent for the slowing of developmental rates.
The question arises; if stenotherms have to
enforce energy savings so much in the permanent
cold, why are eurytherms able to be more inefficient
in the cold? How do sub-Arctic eurytherms survive
despite higher metabolic costs, at the same light
conditions as in the Antarctic? The principal
difference certainly is that Northern hemisphere
eurytherms experience high temperatures in summer. Warm acclimation and the associated reduction in mitochondrial densities and costs then
enhances energy availability for maximized growth,
for reproductive activity and output, for faster
development and for locomotion. Maintaining all of
these patterns of energy use in winter would imply
an excessive energy penalty associated with the
inefficiency of eurythermal cold adaptation. The
energy penalty is likely reduced at least by
suspending reproductive activity in winter. Nonetheless, some of this penalty appears obligatory,
likely due to the maintenance of a widened thermal
window and the associated kinetic consequences
(see above). In active eurytherms the energy penalty
is paid by maintained feeding and associated
locomotory activity. Alternatively, winter exposure
may be tolerated passively by use of hibernation
strategies, thereby minimizing or even escaping
from cold acclimation costs. Overall, these considerations support the contrasting picture developed for Antarctic stenotherms. Trade-offs in
energy budget for the sake of cold-compensated
growth then appear as an over-arching principle
driving Antarctic evolution and causing many of the
extant physiological and lifestyle characteristics seen
there today.
4.2. Longevity and gigantism
This generalized statement also relates to two
other characteristics, longevity and gigantism. Due
to obligatory reduction of higher functional rates
(reproductive output, development) for the sake of
growth in Antarctic marine ectotherms lifetime
functions need to be fulfilled over longer time
scales. A principal feature in Antarctic marine fauna
is its extended longevity where bivalves, brachiopods, echinoids, and fish were found to live about
1095
2–10 times longer than temperate species (DeVries
and Eastman, 1981; Peck and Bullough, 1993; Brey
and Clarke, 1993; Brey et al., 1995; Cailliet et al.,
2001; La Mesa and Vacchi, 2001). For example,
bivalve molluscs from high latitudes grow more
slowly, attain a larger maximum size, and have a
longer lifespan than do con-familial species from
higher latitudes (Roy et al., 2000; Heilmayer et al.,
2003). The question arises whether this is a passive
consequence of cold temperatures due to reduced
metabolic rates or whether the extension of higher
functions like reproduction or development over
time has caused selection for longevity. In accordance with major theories of aging (Johnson et al.,
1999; Troen, 2003), three principal processes may
modulate the maximum lifespan of a species: rate of
metabolism, associated rate of formation of ROS in
aerobic mitochondrial metabolism and the balance
of associated oxidative damage by antioxidative
defence mechanisms. This includes the respective
links of these processes to the gene level (Epel et al.,
2004; Sapolsky, 2004). Elevated levels of antioxidative defence mechanisms, especially higher levels of
non-enzymatic compounds, are commonly observed
in Antarctic invertebrates (for review, Abele and
Puntarulo, 2004) and also in polar fishes (SpeersRoesch and Ballantyne, 2005). In contrast, activities
of antioxidant enzymes have not been found
enhanced in Arctic and Antarctic fishes.
A series of recent papers by Philipp et al.
(2005a, b, 2006) illustrates how the balance between
the three factors, metabolic rate, mitochondrial
ROS formation, and antioxidative defence, shapes
the aging process. Philipp and colleagues studied
these mechanisms in Antarctic compared to temperate bivalves, in two mud clams, the temperate Mya
arenaria and the Antarctic Laternula elliptica, and in
two scallops, the temperate Aequipecten opercularis
and the Antarctic Adamussium colbecki. The series
shows that the balance between the three factors
strongly depends upon lifestyle requirements. In
general, lifetime aerobic energy turnover of the
long-lived species far exceeds the balance expected
from a simple correlation between rate of living and
life expectancy. Metabolic rate reduction was found
more influential in the more passive mud clams and
modulation of the other two factors, ROS formation and antioxidative defence, was more strongly
involved in the active scallops. Reduced rates of
ROS formation and higher glutathione levels more
than other antioxidative defence mechanisms appear to be prime requisites for the maintenance of
ARTICLE IN PRESS
1096
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
mitochondrial functions over extended time periods.
Within both the mud clams and the scallops, the
longer-lived species of each group (Laternula
elliptica, A. opercularis) showed higher glutathione
concentrations compared to their shorter-lived
counterparts (M. arenaria, A. opercularis) (Philipp,
2005). A similar picture has been found in liver
samples of two zoarcid fish species (Heise, 2005).
Moreover, elevated levels of lipophilic vitamin E
have been found in blood and tissues of Antarctic
fishes (Gieseg et al., 2000; Dunlap et al., 2002). This
was suggested to reflect enhanced protection from
radical attack due to higher levels of lipid unsaturation in membranes. However, in some fauna the
level of unsaturation is not evidently elevated.
Similar levels of unsaturated fatty acids were found
in the soft tissue of Laternula elliptica and in several
marine bivalves from warmer waters (Ahn et al.,
2000). Furthermore baseline oxidative stress is likely
low in polar marine environments due to low SMR,
low rates of formation of radical oxygen species
(ROS), and low rates of ROS-mediated cellular
damage. In addition to compensating for the
slowing of defence reactions in the cold, enhanced
concentrations of non-enzymatic antioxidants may
then not compensate for enhanced oxidative stress
but may rather support extended lifespans. In a
sequence of antioxidative mechanisms, glutathione
and vitamin E may represent the first line of
defence, with later steps complementing the quenching of ROS levels and activities.
In line with earlier findings in temperate cephalopods (Zielinski and Pörtner, 2000), the adjustment
of antioxidative defence to various levels according
to lifespan strongly suggests that lifespan does not
simply follow metabolic rates or antioxidative
defence levels. Extended lifespans of Antarctic
fauna rather appear as a consequence of selection
for longevity, with a secondary setting of aging
patterns and protective mechanisms according to
lifetime requirements. These are defined by, e.g.
maintained lifetime reproductive output under
conditions when annual reproductive output decreases (Clarke, 1987; Brey, 1995; Fig. 14). The
‘‘enforced energy savings’’ hypothesis and the
implied trade-offs in higher functions, namely their
delay and reduced rates for the sake of higher
growth would thus appear as causal driving forces
in the selection process for extended life spans in the
Antarctic.
Long lifespans at cold-compensated growth
capacities and reduced rates of development likely
also contribute to explain one other phenomenon
that typifies polar marine fauna, namely polar
gigantism. Species selected for long age have the
time to grow larger. This does not imply that all
Antarctic fauna is larger, but only that some groups
experience an expansion of body size ranges in the
cold (Chapelle and Peck, 1999, 2004; McClain and
Rex, 2001). These papers have convincingly shown
that larger body sizes are supported by elevated
ambient oxygen levels. However, the positive effect
of high ambient oxygen levels on body size in the
cold is increased or may depend on the obligatory
reduction of organismic oxygen demand at cold
temperatures. From a physiological point of view
both the reduced level of energy turnover in
stenotherms and enhanced ambient oxygen levels
define the additional scope available for extended
body sizes in the cold (Pörtner, 2002c).
5. Summary and perspectives: pathways of Antarctic
evolution
The examples discussed in this paper, drawn from
various molecular, physiological and ecological
studies, have been interpreted in the light of the
integrative concept of oxygen and capacity limitation of thermal tolerance. This analysis has been
able to integrate information from various, molecular to ecosystem levels of biological organization
that have traditionally been addressed separately.
The analysis also has identified crucial links between
these levels. A clearer understanding of priorities
and consequences results with respect to selective
pressures, trade-offs and constraints in Antarctic
evolution. The author is not aware of an alternative
concept that is capable of developing a similar
power of integration.
The time course and pattern of Metazoan
evolution in Antarctic oceans becomes comprehensible based on the principal insight that Antarctic
cooling at low temperature variability was paralleled by the down-regulation of energy turnover in
Antarctic marine ectotherms (Fig. 14). Integrative
re-interpretation of functional properties and design
features elaborated at molecular, cellular, organ or
tissue and whole organism levels suggests that they
have largely evolved for the sake of contributing to
such energy savings. Energy savings thus appears as
a unifying explanation for molecular to organismic
features. The down-regulation of energy turnover
was enforced for the sake of growth at all life stages
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
1097
Climate oscillations
Eurythermal cold adaptation: more and higher capacity mitochondria, leakier membranes
Antarctica: Long term
progressive cooling
Reduction of seasonal T,
permanently high [O 2 ]
(water and body fluids)
Daily and seasonal temperature
oscillations maintained
Behavioral hyperthermia and vertical migrations
Summer
Reduced cost, SMR and mitochondrial capacities
Hibernation
Loss of force, ion exchange capacity, (Hb, Mb)
High aerobic capacity,
Elevated kinetic barriers limiting metabolic flux
metabolic rate and scope
Stenothermal cold adaptation:
Enhanced diffusive oxygen supply
Low metabolic scopes
Enhanced antioxidative defence
Maximized growth
Delayed reproduction and development
Longevity, Gigantism
High ventilatory and circulatory capacity
Maximized growth and timely
reproduction,
short to medium lifespans
(e.g. temperate cephalopods)
Fig. 14. Conceptual scheme of the pathway of Antarctic evolution: Animals are suggested to follow two principal, contrasting pathways
of energy turnover. Energy savings are imposed by stable low temperatures and supported by high oxygen concentrations of Antarctic
waters and body fluids. In contrast, high energy turnover modes of life result from eurythermal tissue design (Pörtner, 2004). Low
metabolic rates at high levels of antioxidative defence support Antarctic longevity and gigantism and are selected for in response to,
especially, late and extended reproduction and the need to maximize growth.
and was made possible by taking advantage of the
permanent excess of ambient oxygen supply.
Initially, mitochondrial density rose to maintain
performance levels but also provided the membrane
network for inward oxygen diffusion. Consecutively, the selection for reduced SMRs and performance levels led to a reduction of mitochondrial
capacity and their baseline idling and oxygen
demand. High levels of cellular membrane density
associated with large mitochondrial networks could
be selected for due to reduced requirements for
force development and, thus, low densities of
myofibrils. These membranes served the evolution
of maximized diffusive oxygen supply pathways,
which alleviated the workload on convective oxygen
transport through ventilation and circulation. Energy savings also were supported by the evolution of
large cell sizes and their lower ion exchange
requirements as well as of low tissue capillary
density but enhanced capillary diameters. The
reduction in oxygen demand finally allowed for
the loss of Mb and haemoglobin. This loss may once
again have contributed to energy savings by
eliminating the need for associated protein turnover
and repair. Energy savings thus may include specific
mechanisms of metabolic down regulation which
compensate for the cost of metabolic cold adapta-
tion and, at the same time, enhance thermal
sensitivity. Low-capacity convective and elevated
diffusive oxygen supply has a small functional
reserve and thereby also enhances thermal sensitivity. As a trade-off associated with space constraints
due to enhanced mitochondrial networks and the
parallel reduction of force at moderate activity
levels, anaerobic capacity was reduced as well,
especially in pelagic species. Nonetheless, aerobic
recovery from fatigue occurs rapidly as a side effect
of enhanced expression of the aerobic machinery.
Enhanced aerobic capacity seen at the tissue level
also should fuel the cold-compensated rates of
growth or other ‘‘slow’’ functions which do not
demand large increments in convective oxygen
supply.
In the light of the principal cost of cold
adaptation, which is evident in temperate to subArctic species, the reduction of metabolic rates as
seen in the permanent cold in Antarctic stenotherms
appears as a secondary process which could only
evolve in the stable marine environment of the
Antarctic. At each level of organisation excessive
energy savings occur for the sake of higher
organismic growth despite permanently low temperatures. Enhanced growth capacity is supported
by cold-compensated protein synthesis capacity. As
ARTICLE IN PRESS
1098
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
a trade-off, high growth rates despite low metabolic
rates would exploit the cold compensated metabolic
capacity but at the expense of low capacities for
motor activity. Furthermore, they also imply delays
and low functional rates at all stages of life history
with the result of late maturity, late fecundity and
offspring release, extended development, and passive larvae supported by lecithotrophy. This also
may support the emphasis on direct development
rather than planctotrophic larvae in the cold.
Extended life spans were required to cover lifetime
functions and were accordingly selected for and not
just a consequence of polar life in the slow lane. The
commonality of cold exposure consequences for all
ecosystem players likely explains why the consequences of cold adaptation do not result harmful at
the level of between species interactions like
predator prey relationships. Only one exception is
conceivable to this apparent rule. The restriction of
marine ectothermic animal life in the Antarctic to
the slow lane may be one key reason why the marine
Antarctic is such a rewarding feeding ground for
warm-blooded mammals and birds.
As a perspective, the level of specialization of
Antarctic marine fauna to the stable cold environment poses important questions for its future: In
fact, Antarctic species are possibly the most
thermally limited animals on Earth, as they survive
only in a 5–10 1C window. This poses a new degree
of significance and urgency on studies of the
climate-dependent evolution of marine Antarctic
ectotherms as this is important to fully understand
the degree of thermal sensitivity. Further in depth
understanding of cause and effect in Antarctic
evolutionary patterns should become possible by
testing hypotheses within the concept of oxygen and
capacity limited thermal tolerance, e.g. by quantifying the interdependence of thermal windows, metabolic design, energy turnover, thermal tolerance,
gene expression and functional protein levels; tradeoffs and priorities in energy budgets and finally, the
potential consequences of organismic functioning
for biodiversity. This understanding also should be
supported by the view that Antarctic marine life is
located to variable degrees at the extreme end of a
continuum of life forms in various climates. Knowledge summarized here matches and supports the
framework and applicability of the oxygen and
capacity limitation concept and emphasizes that the
origin of functions in Antarctic marine fauna was
dependent on climate development and climate
stability. The making of a ‘‘good’’ Antarctic
ectotherm was climate dependent indeed and likely
involves at least those functional specializations
discussed as typical in the present study. In the light
of future global change, however, this stereotype
will likely be less successful and warming trends
have already started to test its acclimation capacity.
Acknowledgements
Supported by the Mar Co Pol I program of the
AWI. The author thanks A. Clarke and C. Smith
for an excellent symposium.
References
Abele, D., Puntarulo, S., 2004. Formation of reactive species and
induction of antioxidant defence systems in polar and
temperate marine invertebrates and fish. Comparative Biochemistry and Physiology A 138, 405–415.
Acierno, R., Agnisola, C., Tota, B., Sidell, B.D., 1997.
Myoglobin enhances cardiac performance in Antarctic fish
species that express the protein. American Journal of
Physiology 273, R100–R106.
Ahn, I.Y., Cho, K.W., Choi, K.S., Seo, Y., Shin, J., 2000. Lipid
content and composition of the Antarctic lamellibranch,
Laternula elliptica (King & Broderip) (Anomalodesmata:
Laternulidea), in King George Island during an austral
summer. Polar Biology 23, 24–33.
Archer, S.D., Johnston, I.A., 1989. Kinematics of labriform and
subcrangiform swimming in the Antarctic fish Notothenia
neglecta. Journal of Experimental Biology 143, 195–210.
Arntz, W., Gili, J.S., 2001. A case for tolerance in marine
ecology: let us not put out the baby with the bathwater.
Scientia Marina 65, 283–299.
Arntz, W.E., Brey, T., Gallardo, V.A., 1994. Oceanography and
marine biology, annual reviews. Antarctic Zoobenthos 32,
241–304.
Aronson, R.B., Blake, D.B., Oji, T., 1997. Retrograde community structure in the late Eocene of Antarctica. Geology 15,
903–906.
Astorga, A., Fernández, M., Boschi, E.E., Lagos, N., 2003. Two
oceans, two taxa and one mode of development: latitudinal
diversity patterns of South American crabs and test for
possible causal processes. Ecology Letters 6, 420–427.
Axelsson, M., 2005. The circulatory system and its control. In:
Farrell, A.P., Steffensen, J.F. (Eds.), The Physiology of Polar
Fishes. Fish Physiology (Randall, D.R., Farrell, A.P., Eds.),
vol. 22, pp. 239–280.
Bakun, A., 1996. Patterns in the Ocean-Ocean Processes and
Marine Population Dynamics. California Sea Grant College
System, La Jolla.
Beamish, R.J., 1995. Climate Change and Northern Fish
Populations. Canadian Special Publication of Fisheries and
Aquatic Science, 121, 739pp.
Billerbeck, J.M., Schultz, E.T., Conover, D.O., 2000. Adaptive
variation in energy acquisition and allocation among latitudinal populations of the Atlantic silverside. Oecologia 122,
210–219.
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
Bluhm, B., 2001. Age determination in polar crustacea using the
autofluorescent pigment lipofuscin. Berichte zur Polarforschung/Reports on Polar Research 382, 1–127.
Bosch, I., Beauchamp, K.A., Steele, E., Pearse, J.S., 1987.
Development, metamorphosis and seasona abundance of
embryos and larvae of the Antarctic sea urchin, Sterechinus
neumayeri. Biological Bulletin 173, 126–135.
Boutilier, R.G., 1998. Physiological ecology in cold ocean
fisheries: a case study in Atlantic cod. In: Pörtner, H.O.,
Playle, R.C. (Eds.), Cold Ocean Physiology. Cambridge
University Press, Cambridge, pp. 465–489.
Brey, T., 1995. Temperature and reproductive metabolism in
macrobenthic populations. Marine Ecology Progress Series
125, 87–93.
Brey, T., 1999. Growth performance and mortality in aquatic
macrobenthic invertebrates. Advances in Marine Biology 35,
153–223.
Brey, T., Clarke, A., 1993. Population dynamics of marine
benthic invertebrates in Antarctic and Subantarctic environments: are there unique adaptations? Antarctic Science 5,
253–266.
Brey, T., Pearse, J., Basch, L., MClintock, J., Slattery, M., 1995.
Growth and production of Sterechinus neumayeri (Echinoidae: Echinodermata) in McMurdo Sound, Antarctica. Marine
Biology 124, 279–292.
Brodeur, J.C., Calvo, J., Clarke, A., Johnston, I.A., 2003.
Myogenic cell cycle duration in Harpagifer species with subAntarctic and Antarctic distributions: evidence for cold
compensation. Journal of Experimental Biology 206,
1011–1016.
Cailliet, G.M., Andrews, A.H., Burton, E.J., Watters, D.L.,
Kline, D.E., Ferry-Graham, L.A., 2001. Age determination
and validation studies of marine fishes: do deep-dwellers live
longer? Experimental Gerontology 36, 739–764.
Chapelle, G., Peck, L.S., 1999. Polar gigantism dictated by
oxygen availability? Nature 399, 114–115.
Chapelle, G., Peck, L.S., 2004. Amphipod crustacean size
spectra: new insights in the relationship between size and
oxygen. Oikos 106, 167–175.
Chen, L., DeVries, A.L., Cheng, C.H.C., 1997. Convergent
evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proceedings of the National
Academy of Sciences, USA 94, 3817–3822.
Claireaux, G., Webber, D.M., Legardere, J.-P., Kerr, S.R., 2000.
Influence of water temperature and oxygenation on the
aerobic metabolic scope of Atlantic cod (Gadus morhua).
Journal of Sea Research 44, 257–265.
Clarke, A., 1982. Temperature and embryonic development in
polar marine invertebrates. International Journal of Invertebrate Reproduction 5, 71–82.
Clarke, A., 1987. Temperature, latitude and reproductive output.
Marine Ecology Progress Series 38, 89–99.
Clarke, A., 1996. The influence of climate change on the
distribution and evolution of organisms. In: Johnston, I.A.,
Bennett, A.F. (Eds.), Animals and Temperature: Phenotypic
and Evolutionary Adaptation. Cambridge University Press,
Cambridge, pp. 377–407.
Clarke, A., 1988. Seasonality in the Antarctic marine environment. Comparative Biochemistry and Physiology 90B,
461–473.
Clarke, A., 1998. Temperature and energetics: an introduction to
cold ocean physiology. In: Pörtner, H.O., Playle, R.C. (Eds.),
1099
Cold Ocean Physiology. Cambridge University Press, Cambridge, pp. 3–30.
Clarke, A., Crame, J.A., 1989. The origin of the southern ocean
marine fauna. In: Crame, J.A. (Ed.), Origins and evolution of
the Antarctic Biota. Geological Society Special Publications,
vol. 47, pp. 253–268.
Clarke, A., Crame, J.A., 1992. The Southern ocean benthic fauna
and climate change: a historical perspective. Philosophical
Transactions of the Royal Society of London B 338, 299–309.
Clarke, A., Peck, L.S., 1991. The physiology of polar marine
zooplankton. In: Proceedings of the Pro Mare Symposium on
Polar Ecology, Trondheim. Sakshaug, E., Hopkins, C.,
Oritsland, N. (Eds.) Polar Research 10, 355–369.
Clarke, A., Johnston, N.M., 1999. Scaling of metabolic rate and
temperature in teleost fish. Journal of Animal Ecology 68,
893–905.
Crame, J.A., 1993. Latitudinal range fluctuations in the marine
realm through geological time. Trends in Ecology and
Evolution 8, 162–166.
Cushing, D.H., 1982. Climate and Fisheries. Academic Press,
London.
Dahm, C., 1999. Ophiuroids (Echinodermata) of southern
Chile and the Antarctic: Taxonomy, biomass, diet and growth
of dominant species. Scientia Marina (Barcelona) 63,
427–432.
DeVries, A.L., Eastman, J.T., 1981. Physiology and ecology of
notothenioid fishes of the Ross Sea. Journal of the Royal
Society of New Zealand 11, 329–340.
Di Prisco, G., Cocca, E., Parker, S., Detrich, H.W., 2002.
Tracking the evolutionary loss of hemoglobin expression by
the white blooded Antarctic fishes. Gene 295, 185–191.
Dorrien, C.v., 1993. Ecology and respiration of selected Arctic
benthic fish species. Berichte zur Polarforschung/Reports on
Polar Research 125, 1–104.
Dunlap, W.C., Fujisawa, A., Yamamoto, Y., Moylan, T.J.,
Sidell, B.D., 2002. Notothenioid fish, krill and phytoplankton
from Antarctica contain a vitamin E constituent (alphatocomonoenol) functionally associated with cold-water adaptation. Comparative Biochemistry and Physiology B 133,
299–305.
Eastman, J.T., De Vries, A.L., 1982. Buoyancy studies of
notothenioid fishes in McMurdo Sound, Antarctica. Copeia
2, 385–393.
Echtay, K.S., Roussel, D., St-Pierre, J., Jekabsons, M.B.,
Cadenas, S., Stuart, J.A., Harper, J.A., Roebuck, S.J.,
Morrison, A., Pickering, S., Clapham, J.C., Brand, M.D.,
2002. Superoxide activates mitochondrial uncoupling proteins. Nature 415, 96–99.
Egginton, S., 1997a. Control of tissue blood flow at very low
temperatures. Journal of thermal Biology 22, 403–407.
Egginton, S., 1997b. A comparison of the response to induced
exercise in red- and white-blooded Antarctic fishes. Journal of
Comparative Physiology B 167, 129–134.
Egginton, S., Skilbeck, C., Hoofd, L., Calvo, J., Johnston, I.A.,
2002. Peripheral oxygen transport in skeletal muscle of
Antarctic and sub-Antarctic notothenioid fish. Journal of
Experimental Biology 205, 769–779.
Ekau, W., 1988. Ecomorphology of nototheniid fish from the
Weddell Sea, Antarctica. Berichte zur Polarforschung/Reports on Polar Research 51, 1–140.
Epel, E.S., Blackburn, E.H., Lin, J., Dhabhar, F.S., Adler, N.E.,
Morrow, J.D., Cawthon, R.M., 2004. Accelerated telomere
ARTICLE IN PRESS
1100
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
shortening in response to life stress. Proceedings of the
National Academy of Sciences USA 101, 17312–17315.
Fahrbach, E., Hoppema, M., Rohardt, G., Schröder, M.,
Wisotzki, A., 2004. Decadal-scale variations of water mass
properties in the deep Weddell Sea. Ocean Dynamics 54,
77–91.
Farrell, A.P., 1997. Effects of temperature on cardiovascular
performance. In: Wood, C.M., McDonald, D.G. (Eds.),
Global Warming: Implications for Freshwater and Marine
Fish. Cambridge University Press, pp. 135–158.
Fields, P., 2001. Protein function at thermal extremes: balancing
stability and flexibility. Comparative Biochemistry and
Physiology A 129, 417–431.
Finney, B.P., Gregory-Eaves, I., Douglas, M.S.V., Smol, J.P.,
2002. Fisheries productivity in the northeastern Pacific Ocean
over the past 2200 years. Nature 416, 729–733.
Fischer, T., 2003. The effects of climate induced temperature
change on cod (Gadus morhua): linking ecological and
physiological investigations. Dissertation, University of Bremen.
Forster, M.E., Franklin, C.E., Taylor, H.H., Davison, W., 1987.
The aerobic scope of an Antarctic fish, Pagothenia borchgrevinki and its significance for metabolic cold adaptation.
Polar Biology 8, 155–159.
Franklin, C.E., Wilson, R.S., Davison, W., 2003. Locomotion at
1.0 1C: burst swimming performance of five species of
Antarctic fish. Journal of Thermal Biology 28, 59–65.
Fraser, K.P.P., Clarke, A., Peck, L.S., 2002a. Feast and famine in
Antarctica: seasonal physiology in the limpet Nacella
concinna. Marine Ecology Progress Series 242, 169–177.
Fraser, K.P.P., Clarke, A., Peck, L.S., 2002b. Low-temperature
protein metabolism: seasonal changes in protein synthesis and
RNA dynamics in the Antarctic limpet Nacella concinna
Strebel 1908. Journal of Experimental Biology 205,
3077–3086.
Frederich, M., Pörtner, H.O., 2000. Oxygen limitation of thermal
tolerance defined by cardiac and ventilatory performance in
the spider crab Maja squinado. American Journal of
Physiology 279, R1531–R1538.
Frederich, M., Sartoris, F.J., Arntz, W., Pörtner, H.O., 2000a.
Haemolymph magnesium regulation in decapod crustaceans:
physiological correlates and ecological consequences in polar
areas. Journal of Experimental Biology 203, 1383–1393.
Frederich, M., De Wachter, B., Sartoris, F.J., Pörtner, H.O.,
2000b. Cold tolerance and the regulation of cardiac performance and haemolymph distribution in Maja squinado
(Crustacea, Decapoda). Physiological and Biochemical Zoology 73, 406–415.
Frederich, M., Sartoris, F.J., Pörtner, H.O., 2001. Distribution
patterns of decapod crustaceans in polar areas: a result of
magnesium regulation? Polar Biology 24, 719–723.
Gaston, K.J., Chown, S.L., 1999. Why Rapoport’s rule does not
generalise. Oikos 84, 309–312.
Giebelhausen, B., Lampert, W., 2001. Temperature reaction
norms of Daphnia magna: the effect of food concentration.
Freshwater Biology 46, 281–289.
Gieseg, S.P., Cuddihy, S., Hill, J.V., Davison, W., 2000. A
comparison of plasma vitamin C and E levels in two Antarctic
and two temperate water fish species. Comparative Biochemistry and Physiology B 125, 371–378.
Gille, S.T., 2002. Warming of the Southern Ocean since the
1950s. Science 295, 1275–1277.
Gödecke, A., Flögel, U., Zanger, K., Ding, Z., Hirchenhain, J.,
Decking, UKM., Schrader, J., 1999. Disruption of myoglobin
in mice induces multiple compensatory mechanisms. Proceedings of the National Academy of Sciences USA 96,
10495–10500.
Grove, T.J., Hendrickson, J.W., Sidell, B.D., 2004. Two species
of antarctic icefishes (genus Champsocephalus) share a
common genetic lesion leading to the loss of myoglobin
expression. Polar Biology 27, 579–585.
Guderley, H., 2004. Metabolic responses to low temperature in
fish muscle. Biological Reviews 79, 409–427.
Hardewig, I., van Dijk, P.L.M., Pörtner, H.O., 1998. High energy
turnover at low temperatures: recovery from exercise in
Antarctic and common eelpout (Zoarcidae). American
Journal of Physiology 274, R1789–R1796.
Hardewig, I., Peck, L.S., Pörtner, H.O., 1999a. Thermal
sensitivity of mitochondrial function in the Antarctic Notothenioid, Lepidonotothen nudifrons. Journal of Comparative
Physiology B 169, 597–604.
Hardewig, I., van Dijk, P.L.M., Moyes, C.D., Pörtner, H.O.,
1999b. Temperature-dependent expression of cytochrome c
oxidase in fish: a comparison between temperate and
Antarctic and eelpout. American Journal of Physiology 277,
R508–R516.
Harper, S.L., Reiber, C.L., 2004. Physiological development of
the embryonic and larval crayfish heart. Biological Bulletin
206, 78–86.
Heath, A.G., Hughes, G.M., 1973. Cardiovascular and respiratory changes during heat stress in rainbow trout (Salmo
gairdneri). Journal of Experimental Biology 59, 323–338.
Heilmayer, O., Brey, T., Chiantore, M., Cattaneo-Vietti, R.,
Arntz, W.E., 2003. Age and productivity of the Antarctic
scallop, Adamussium colbecki, in Terra Nova Bay (Ross Sea,
Antarctica). Journal of Experimental Marine Biology and
Ecology 288, 239–256.
Heilmayer, O., Brey, T., Pörtner, H.O., 2004. Growth efficiency
and temperature in scallops: a comparative analysis of species
adapted to different temperatures. Functional Ecology 18,
641–647.
Heilmayer, O., Honnen, C., Jacob, U., Chiantore, C., CattaneoVietti, R., Brey, T., 2005. Temperature effects on summer
growth rates in the Antarctic scallop, Adamussium colbecki.
Polar Biology 28, 523–527.
Heise, K., 2005. Interaction of oxygen supply, oxidative stress,
and molecular defence systems in fishes during cold and heat
stress in a latitudinal cline. Dissertation, University of
Bremen.
Heise, K., Puntarulo, S., Nikinmaa, M., Abele, D., Pörtner,
H.O., 2006. Oxidative stress during stressful heat exposure
and recovery in the North Sea eelpout (Zoarces viviparus).
Journal of Experimental Biology 209, 353–363.
Hemmingsen, A.M., 1960. Energy metabolism as related to
body size and respiratory surface and its evolution.
Rep. Steno Memorial Hosp. Nord. Insulin Laboratory 9,
1–110.
Hiscock, K., Southward, A., Tittley, I., Hawkins, S., 2004.
Effects of changing temperature on benthic marine life in
Britain and Ireland. Aquatic Conservation in Marine and
Freshwater Ecosystems 14, 333–362.
Hochachka, P.W., Somero, G.N., 2002. Biochemical Adaptation:
Mechanism and Process in Physiological Evolution. Oxford
University Press, Oxford.
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
Hodell, D.A., Kanfoush, S.L., Shemesh, A., Crosta, X., Charles,
C.D., Guilderson, T.P., 2001. Abrupt cooling of Antarctic
surface waters and sea ice expansion in the South Atlantic
sector of the Southern Ocean at 5000 cal yr B.P. Quaternary
Research 56, 191–198.
Hofmann, G.E., Buckley, B.A., Airaksinen, S., Keen, J.E.,
Somero, G.N., 2001. Heat-shock protein expression is absent
in the Antarctic fish Trematomus bernacchii (family Nototheniidae). Journal of Experimental Biology 203, 2331–2339.
Holeton, G.F., 1974. Metabolic cold adaptation of polar fish: fact
or artefact? Physiological Zoology 47, 137–152.
Hummel, H., Sommer, A., Bogaards, R.H., Pörtner, H.O., 1997.
Variation in genetic traits of the lugworm Arenicola marina:
temperature related expression of mitochondrial allozymes?
Marine Ecology Progress Series 159, 189–195.
Jensen, M.N., 2003. Consensus on ecological impact remains
elusive. Science 299, 38.
Jobling, M., 1997. Temperature and growth: modulation of
growth rate via temperature change. In: Wood, C.M.,
McDonald, D.G. (Eds.), Global Warming: implications for
Freshwater and Marine Fish. Cambridge University Press,
Cambridge, pp. 225–253.
Johnston, I.A., 1989. Antarctic fish muscles—structure, function
and physiology. Antarctic Science 1, 97–108.
Johnston, I.A., Johnson, T.P., Battram, J.C., 1991. Low
temperature limits burst swimming performance in Antarctic
fish. In: di Prisco, G., Maresca, B., Tota, B. (Eds.), Biology of
Antarctic Fish. Springer, Berlin, pp. 179–190.
Johnston, I.A., Calvo, J., Guderley, H., Fernandez, D., Palmer,
L., 1998. Latitudinal variation in the abundance and oxidative
capacities of muscle mitochondria in perciform fishes. Journal
of Experimental Biology 201, 1–12.
Johnson, F.B., Sinclair, D.A., Guarente, L., 1999. Molecular
Biology of Aging. Cell 96, 291–302.
Kaplan, A., Kushnir, Y., Cane, M.A., Blumenthal, M.B., 1997.
Reduced space optimal analysis for historical data sets: 136
years of Atlantic sea surface temperature. Journal of
Geophysical Research 102, 27835–27860.
Kaplan, A., Cane, M.A., Kushnir, Y., Clement, A.C., Blumenthal, M.B., Rajagopalan, B., 1998. Analyses of global sea
surface temperature 1856–1991. Journal of Geophysical
Research 103, 18567–18589.
Katz, S.L., 2002. Design of heterothermic muscle in fish. Journal
of Experimental Biology 205, 2252–2266.
Kawall, H.G., Torres, J.J., Sidell, B.D., Somero, G.N., 2002.
Metabolic cold adaptation in Antarctic fishes: evidence from
enzymatic activities of brain. Marine Biology 140, 279–286.
Kock, K.H., Everson, I., 1998. Age, growth and maximum size of
Antartic notothenioid fish—revisited. In: di Prisco, G.,
Pisano, E., Clarke, A. (Eds.), Fishes of Antarctica. A
biological Overview. Springer, Milano, Italia, pp. 29–40.
Korsmeyer, K.E., Dewar, H., Lai, N.C., Graham, J.B., 1996. The
aerobic capacity of tunas: adaptation for multiple metabolic
demands. Comparative Biochemistry and Physiology 113A,
12–24.
La Mesa, M., Vacchi, M., 2001. Review. Age and growth of high
Antarctic notothenioid fish. Antarctic Science 13, 227–235.
Lannig, G., Bock, C., Sartoris, F.J., Pörtner, H.O., 2004. Oxygen
limitation of thermal tolerance in cod, Gadus morhua L.
studied by non-invasive NMR techniques and on-line venous
oxygen monitoring. American Journal of Physiology 287,
R902–R910.
1101
Lannig, G., Storch, D., Pörtner, H.O., 2005. Aerobic mitochondrial capacities in Antarctic and temperate eelpout (Zoarcidae) subjected to warm versus cold acclimation. Polar Biology
28, 575–584.
Lucassen, M., Schmidt, A., Pörtner, H.O., 2003. Cold induced
mitochondrial proliferation in Zoarces viviparus: changes in
enzyme activities and mRNA levels. American Journal of
Physiology 258, R1410–R1420.
Lucassen, M., Koschnick, N., Eckerle, L.G., Pörtner, H.O., 2006.
Mitochondrial mechanisms of cold adaptation in cod (Gadus
morhua) populations from different climatic zones. Journal of
Experimental Biology 209, 2462–2471.
Mark, F.C., Bock, C., Pörtner, H.O., 2002. Oxygen limited
thermal tolerance in Antarctic fish investigated by magnetic
resonance imaging (MRI) and spectroscopy (31P-MRS).
American Journal of Physiology 283, R1254–R1262.
Mark, F.C., Hirse, T., Pörtner, H.O., 2005. Thermal sensitivity of
cellular energy budgets in some Antarctic fish hepatocytes.
Polar Biology, Doi:10.1007/s00300-005-0018-0.
Marsh, A.G., Maxson, R.E., Manahan, D.T., 2001. High
macromolecular synthesis with low metabolic cost in Antarctic sea urchin embryos. Science 291, 1950–1952.
Maslowski, W., Marble, D., Walczowski, W., Schauer, U.,
Clement, J.L., Semtner, A.J., 2004. On climatological
mass, heat and salt transports through the Barents Sea and
Fram Strait from a pan-Arctic coupled ice-ocean model
simulation. Journal of Geophysical Research 109, C03032,
(1–16).
McClain, C.R., Rex, M.A., 2001. The relationship between
dissolved oxygen concentration and maximum size in deepsea turrid gastropods: an application of quantile regression.
Marine Biology 139, 681–685.
Melzner, F., Bock, C., Pörtner, H.O., 2006. Critical temperatures
in the cephalopod Sepia officinalis investigated using in vivo
31
P NMR spectroscopy. Journal of Experimental Biology 209,
891–906.
Mente, E., Legeay, A., Houlihan, D.F., Massabuau, J.C., 2003.
Influence of oxygen partial pressure in protein synthesis in
feeding crabs. American Journal of Physiology 284,
R500–R510.
Mitchell, S.E., Lampert, W., 2000. Temperature adaptation in a
geographically widespread zooplankter, Daphnia magna.
Journal of Evolutionary Biology 13, 371–382.
North, A.W., 1998. Growth of young fish during winter and
summer at South Georgia, Antarctica. Polar Biology 19,
198–205.
O’Brien, K.M., Skilbeck, C., Sidell, B.D., Egginton, S., 2003.
Muscle fine structure may maintain the function of oxidative
fibres in haemoglobinless Antarctic fishes. Journal of Experimental Biology 206, 411–421.
Overpeck, J., Hughen, K., Hardy, D., Bradley, R., Case, R.,
Douglas, M., Finney, B., Gajewski, K., Jacoby, G., Jennings,
A., Lamoureux, S., Lasca, A., MacDonald, G., Moore, J.,
Retelle, M., Smith, S., Wolfe, A., Zielinski, G., 2003. Arctic
environmental change of the last four centuries. Science 278,
1251–1256.
Parmesan, C., Yohe, G., 2003. A globally coherent fingerprint of
climate change impacts across natural systems. Nature 421,
37–42.
Peck, L.S., 1998. Feeding, metabolism and metabolic scope. In:
Pörtner, H.O., Playle, R.C. (Eds.), Cold Ocean Physiology.
Cambridge University Press, Cambridge, pp. 365–390.
ARTICLE IN PRESS
1102
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
Peck, L.S., 2002. Ecophysiology of Antarctic marine ectotherms:
limits to life. Polar Biology 25, 31–40.
Peck, L.S., 2005. Prospects for surviving climate change in
Antarctic aquatic species. Frontiers in Zoology 2, 9.
Peck, L.S., Bullough, L.W., 1993. Growth and population
structure in the infaunal bivalve Yoldia eightsi in relation to
iceberg activity at Signy Island, Antarctica. Marine Biology
117, 235–241.
Peck, L.S., Conway, L.Z., 2000. The myth of metabolic cold
adaptation: oxygen consumption in stenothermal Antarctic
bivalves. In: Harper E., Crame, A.J. (Eds.), Evolutionary
Biology of the Bivalvia. Geological Society, London, Special
Publications 177, pp. 441–450.
Peck, L.S., Colma, J.G., Murray, A.W.A., 2000. Growth
and tissue mass cycles in the infaunal bivalve Yoldia
eightsi at Signy Island, Antarctica. Polar Biology 23,
420–428.
Peck, L.S., Pörtner, H.O., Hardewig, I., 2002. Metabolic demand,
oxygen supply and critical temperatures in the Antarctic
bivalve, Laternula elliptica. Physiological and Biochemical
Zoology 75, 123–133.
Peck, L.S., Webb, K.E., Bailey, D., 2004a. Extreme sensitivity of
biological function to temperature in Antarctic marine
species. Functional Ecology 18, 625–630.
Peck, L.S., Ansell, A.D., Webb, K.E., Hepburn, L., Burrows, M.,
2004b. Burrowing in Antarctic bivalve molluscs. Polar
Biology 27, 357–367.
Philipp E., 2005. Strategies of cellular ageing in polar and marine
invertebrates. Dissertation, University of Bremen.
Philipp, E., Brey, T., Pörtner, H.O., Abele, D., 2005a.
Chronological and physiological ageing in a polar and a
temperate mud clam. Mechanisms of Ageing and Development 126, 598–609.
Philipp, E., Pörtner, H.O., Abele, D., 2005b. Mitochondrial
ageing of a polar and a temperate mud clam. Mechanisms of
Ageing and Development 126, 610–619.
Philipp, E., Brey, T., Heilmayer, O., Abele, D., Pörtner, H.O.,
2006. Physiological ageing in a polar and a temperate
swimming scallop. Marine Ecology Progress Series 307,
187–198.
Place, S.P., Zippay, M.L., Hofmann, G.E., 2004. Constitutive
roles for inducible genes: evidence for the alteration in
expression of the inducible hsp70 gene in Antarctic notothenioid fishes. American Journal of Physiology 287,
R429–R436.
Pörtner, H.O., 2001. Climate change and temperature-dependent
biogeography: oxygen limitation of thermal tolerance in
animals. Naturwissenschaften 88, 137–146.
Pörtner, H.O., 2002a. Climate variations and the physiological
basis of temperature dependent biogeography: systemic to
molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology 132, 739–761.
Pörtner, H.O., 2002b. Physiological basis of temperature
dependent biogeography: tradeoffs in muscle design and
performance in polar ectotherms. Journal of Experimental
Biology 205, 2217–2230.
Pörtner, H.O., 2002c. Environmental and functional limits to
muscular exercise and body size in marine invertebrate
athletes. Comparative Biochemistry and Physiology 133A,
303–321.
Pörtner, H.O., 2004. Climate variability and the energetic
pathways of evolution: the origin of endothermy in mammals
and birds. Physiological and Biochemical Zoology 77,
959–981.
Pörtner, H.O., Mark, F.C., Bock, C., 2004. Oxygen limited
thermal tolerance in fish? Answers obtained by Nuclear
Magnetic Resonance techniques. Respiratory Physiology and
Neurobiology 141, 243–260.
Pörtner, H.O., Knust, R., unpublished. Cod and climate in a
latitudinal cline: developing a cause and effect understanding.
Pörtner, H.O., Hardewig, I., Sartoris, F.J., van Dijk, P.L.M.,
1998. Energetic aspects of cold adaptation: critical temperatures in metabolic, ionic and acid-base regulation?
In: Pörtner, H.O., Playle, R.C. (Eds.), Cold Ocean
Physiology. Cambridge University Press, Cambridge,
pp. 88–120.
Pörtner, H.O., Peck, L.S., Zielinski, S., Conway, L.Z., 1999a.
Intracellular pH and energy metabolism in the highly
stenothermal Antarctic bivalve Limopsis marionensis as a
function of ambient temperature. Polar Biology 22, 17–30.
Pörtner, H.O., Hardewig, I., Peck, L.S., 1999b. Mitochondrial
function and critical temperature in the Antarctic bivalve,
Laternula elliptica. Comparative Biochemistry and Physiology
124A, 179–189.
Pörtner, H.O., Van Dijk, P.L.M., Hardewig, I., Sommer, A.,
2000. Levels of Metabolic Cold Adaptation: Tradeoffs in
Eurythermal and Stenothermal Ectotherms. In: Davison, W.,
Williams, C.W. (Eds.), Antarctic Ecosystems: Models for a
Wider Understanding. Caxton Press, Christchurch, New
Zealand, pp. 109–122.
Pörtner, H.O., Berdal, B., Blust, R., Brix, O., Colosimo, A., De
Wachter, B., Giuliani, A., Johansen, T., Fischer, T., Knust,
R., Naevdal, G., Nedenes, A., Nyhammer, G., Sartoris, F.J.,
Serendero, I., Sirabella, P., Thorkildsen, S., Zakhartsev, M.,
2001. Climate effects on growth performance, fecundity and
recruitment in marine fish: developing a hypothesis for cause
and effect relationships in Atlantic cod (Gadus morhua) and
common eelpout (Zoarces viviparus). Continental Shelf
Research 21, 1975–1997.
Pörtner, H.O., Lucassen, M., Storch, D., 2005a. Metabolic
biochemistry: its role in thermal tolerance and in the
capacities of physiological and ecological function. In: Farrell
A.P., Steffensen, J. F. (Eds.), The Physiology of Polar Fishes.
Fish Physiology (Randall, D.R., Farrell, A.P., Eds.), vol. 22,
pp. 79–154.
Pörtner, H.O., Storch, D., Heilmayer, O., 2005b. Constraints and
trade-offs in climate dependent adaptation: energy budgets
and growth in a latitudinal cline. Scientia Marina 69 (Suppl.
2), 271–285.
Pörtner, H.O., Bennett, A.F., Bozinovic, F., Clarke, A., Lardies,
M.A., Lucassen, M., Pelster, B., Schiemer, F., Stillman, J.H.,
2005c. Trade-offs in thermal adaptation: the need for a
molecular to ecological integration. Physiological and Biochemical Zoology 79, 295–313.
Pörtner, H.O., Peck, L.S., Hirse, T., 2006. Hyperoxia alleviates
thermal stress in the Antarctic bivalve, Laternula elliptica:
evidence for oxygen limited thermal tolerance. Polar Biology
[doi:10.1007/S00300-005-0106-1].
Poulin, E., Feral, J.P., 1996. Why are there so many species of
brooding Antarctic echinoids? Evolution 50, 820–830.
Robertson, R.F., El-Haj, A.J., Clarke, A., Peck, L.S., Taylor,
E.W., 2001. The effects of temperature on metabolic rate and
protein synthesis following a meal in the isopod Glyptonotus
antarcticus Eights (1852). Polar Biology 24, 677–686.
ARTICLE IN PRESS
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosenzweig,
C., Pounds, J.A., 2003. Fingerprints of global warming on
wild animals and plants. Nature 421, 57–60.
Roy, K., Jablonski, D., Martien, K.K., 2000. Invariant sizefrequency distributions along a latitudinal gradient in marine
bivalves. Proceedings of the National Academy of Sciences
USA 97, 13150–13155.
Sapolsky, R.M., 2004. Organismal stress and telomeric aging: An
unexpected connection. Proceedings of the National Academy
of Sciences USA 101, 17323–17324.
Sartoris, F.J., Bock, C., Serendero, I., Lannig, G., Pörtner, H.O.,
2003. Temperature dependent changes in energy metabolism,
intracellular pH and blood oxygen tension in the Atlantic cod,
Gadus morhua. Journal of Fish Biology 62, 1239–1253.
Scarabello, M., Heigenhauser, G.J.F., Wood, C.M., 1992. Gas
exchange, metabolite status and excess post-exercise oxygen
consumption after repetitive bouts of exhaustive exercise in
juvenile rainbow trout. Journal of Experimental Biology 167,
155–169.
Schauer, U., Fahrbach, E., Osterhus, S., Rohardt, G., 2004.
Arctic warming through the Fram Strait—oceanic heat
transport from three years of measurements. Journal of
Geophysical Research, C. Oceans, 109 (C06026), 1–14,
Doi:10.1029/2003JC001823.
Scholander, P.F., Flagg, W., Walters, V., Irving, L., 1953.
Climatic adaptation in arctic and tropical poikilotherms.
Physiological Zoology 26, 67–69.
Seebacher, F., Davison, W., Lowe, C.J., Franklin, C.E., 2005. A
falsification of the thermal specialization paradigm: compensation for elevated temperatures in Antarctic fish. Biology
Letters 2, 151–154.
Sidell, B.D., 1998. Intracellular oxygen diffusion: the roles of
myoglobin and lipid at cold body temperature. Journal of
Experimental Biology 201, 1118–1127.
Small, D.J., Moylan, T., Vayda, M.E., Sidell, B.D., 2003. The
myoglobin gene of the Antarctic icefish, Chaenocephalus
aceratus, contains a duplicated TATAAAA sequence that
interferes with transcription. Journal of Experimental Biology
206, 131–139.
Sokolova, I.M., Pörtner, H.O., 2003. Metabolic plasticity and
critical temperatures for aerobic scope in a eurythermal
marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. Journal of Experimental
Biology 206, 195–207.
Somero, G.N., 2003. Protein adaptations to temperature and
pressure: complementary roles of adaptive changes in amino
acid sequence and internal milieu. Comparative Biochemistry
and Physiology B 136, 577–591.
Somero, G.N., Childress, J.J., 1990. Scaling of ATP-supplying
enzymes, myofibrillar proteins and buffering capacity in fish
muscle: relationship to locomotory habit. Journal of Experimental Biology 149, 319–333.
Somero, G.N., De Vries, A.L., 1967. Temperature tolerance of
some Antarctic fishes. Science 156, 257–258.
Somero, G.N., Dahlhoff, E., Lin, J.J., 1996. Stenotherms and
eurytherms: mechanisms establishing thermal optima and
tolerance ranges. In: Johnston, I.A., Bennett, A.F. (Eds.),
Animals and Temperature: Phenotypic and Evolutionary Adaptation. Cambridge University Press, Cambridge, pp. 53–57.
Somero, G.N., Fields, P.A., Hofmann, G.E., Weinstein, R.B.,
Kawall, H., 1998. Cold adaptation and stenothermy in
Antarctic notothenioid fishes: what has been gained and
1103
what has been lost. In: di Prisco, G., Pisano, E., Clarke, A.
(Eds.), Fishes of Antarctica: a Biological Overview. Springer,
Milano, pp. 97–109.
Sommer, A., Klein, B., Pörtner, H.O., 1997. Temperature
induced anaerobiosis in two populations of the polychaete
worm Arenicola marina. Journal of Comparative Physiology
B 167, 25–35.
Sommer, A.M., Pörtner, H.O., 2002. Metabolic cold adaptation
in the lugworm Arenicola marina: comparison of a North Sea
and a White Sea population. Marine Ecology Progress Series
240, 171–182.
Sommer, A.M., Pörtner, H.O., 2004. Mitochondrial function in
seasonal acclimatisation versus latitudinal adaptation to cold,
in the lugworm Arenicola marina (L.). Physiological and
Biochemical Zoology 77, 174–186.
Speers-Roesch, B., Ballantyne, J.S., 2005. Activities of antioxidant enzymes and cytochrome c oxidase in liver of Arctic and
temperate teleosts. Comparative Biochemistry and Physiology
A 140, 487–494.
Spicer, J.I., Morritt, D., 1996. Ontogenic changes in cardiac
function in Crustaceans. Comparative Biochemistry and
Physiology A 114, 81–89.
Stanwell-Smith, D.P., Peck, L.S., 1998. Temperature and
embryonic development in relation to spawning and field
occurrence of larvae of 3 Antarctic echinoderms. Biological
Bulletin 194, 44–52.
Steffensen, J.F., 2002. Metabolic cold compensation of polar fish
based on measurements of aerobic oxygen consumption: fact
or artefact? Artefact!. Comparative Biochemistry and Physiology A 132, 789–795.
Stegen, E., Grieshaber, M.K., 2001. Adenosine increases ventilation rate, cardiac performance and haemolymph velocity in
the American lobster Homarus americanus. Journal of
Experimental Biology 204, 947–957.
Stillman, J.H., Somero, G.N., 2000. A comparative analysis of
the upper thermal tolerance limits of eastern Pacific porcelain
crabs, genus Petrolisthes: influences of latitude, vertical
zonation, acclimation, and phylogeny. Physiological and
Biochemical Zoology 73, 200–208.
Storch, D., Pörtner, H.O., 2003. The protein synthesis machinery
operates at the same expense in eurythermal and cold
stenothermal pectinids. Physiological and Biochemical Zoology 76, 28–40.
Storch, D., Heilmayer, O., Hardewig, I., Pörtner, H.O., 2003. In
vitro protein synthesis capacities in a cold stenothermal and a
temperate eurythermal pectinid. Journal of Comparative
Physiology B 173, 611–620.
Storch, D., Lannig, G., Pörtner, H.O., 2005. Temperature
dependent protein synthesis capacities in Antarctic and
temperate (North Sea) fish (Zoarcidae). Journal of Experimental Biology 208, 2409–2420.
Sukhotin, A.A., Abele, D., Pörtner, H.O., 2006. Ageing and
metabolism of Mytilus edulis in a latitudinal cline. Journal of
Shellfish Research, in press.
Thatje, S., Lovrich, G.A., Torres, G., Hagen, W., Anger, K.,
2004. Changes in biomass, lipid, fatty acid and elemental
composition during the abbreviated larval development of the
subantarctic shrimp Campylonotus vegans. Journal of Experimental Marine Biology and Ecology 301, 159–174.
Thatje, S., Anger, K., Calcagno, J.A., Lovrich, G.A., Pörtner,
H.O., Arntz, W.E., 2005. Challenging the cold: crabs reconquer the Antarctic. Ecology 86, 619–625.
ARTICLE IN PRESS
1104
H.O. Pörtner / Deep-Sea Research II 53 (2006) 1071–1104
Tomanek, L., 2005. Two-dimensional gel analysis of the heatshock response in marine snails (genus Tegula): interspecific
variation in protein expression and acclimation ability.
Journal of Experimental Biology 208, 3133–3143.
Troen, B.R., 2003. The Biology of Aging. The Mount Sinai
Journal of Medicine 70, 3–22.
Tschischka, K., Abele, D., Pörtner, H.O., 2000. Mitochondrial
oxyconformity and cold adaptation in the polychaete Nereis
pelagica and the bivalve Arctica islandica from the Baltic and
White Seas. Journal of Experimental Biology 203, 3355–3368.
Urban, H.J., 1998. Upper temperature tolerance of two Antarctic
molluscs (Laternula elliptica and Nacella concinna) from
Potter Cove, King George Island, Antarctic Peninsula.
Berichte zur Polarforschung 299, 230–236.
Van Dijk, P.L.M., Hardewig, I., Pörtner, H.O., 1998. Exercise in
the cold: high energy turnover in Antarctic fish. In: diPrisco,
G., Pisano, E., Clarke, A. (Eds.), Fishes of Antarctica: A
Biological Overview. Springer, Milano, pp. 225–236.
Van Dijk, P.L.M., Tesch, C., Hardewig, I., Pörtner, H.O., 1999.
Physiological disturbances at critically high temperatures: a
comparison between stenothermal Antarctic and eurythermal
temperate eelpouts (Zoarcidae). Journal of Experimental
Biology 202, 3611–3621.
Vaughan, D.G., Marshall, G.J., Connolley, W.M., King, J.C.,
Mulvaney, R., 2001. Devil in the detail. Science 293,
1777–1779.
Vernberg, F.J., 1959. Studies on the physiological variation
between tropical and temperate zone fiddler crabs of the
genus Uca. II. Oxygen consumption of whole organisms.
Biological Bulletin 117, 163–183.
Vernberg, F.J., Vernberg, W.B., 1964. Metabolic adaptation of
animals from different latitudes. Helgoländer Wissenschaftliche Meeresuntersuchungen 9, 476–487.
Vernberg, F.J., Costlow Jr., J.D., 1966. Studies on the
physiological variation between tropical and temperate zone
fiddler crabs of the genus Uca. IV. Oxygen consumption of
larvae and young crabs reared in the laboratory. Physiological
Zoology 39, 36–52.
Vetter, R.A.H., Buchholz, F., 1998. Kinetics of enzymes in coldstenothermal invertebrates. In: Pörtner, H.O., Playle, R.C.
(Eds.), Cold Ocean Physiology. Cambridge University Press,
Cambridge, pp. 190–211.
Vogt, M., 2004. Wachstumsschwankungen der antarktischen
Muschel Laternula elliptica in den letzten vierzig Jahren im
Gebiet von King George Island. Diplomarbeit Rostock.
Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C.,
Beebee, T.J.C., Fromentin, J.M., Hoegh-Guldberg, O.,
Bairlein, F., 2002. Ecological responses to recent climate
change. Nature 416, 389–395.
Weibel, E.R., Taylor, C.R., Hoppeler, H., 1991. The concept of
symmorphosis: a testable hypothesis of structure-function
relationship. Proceedings of the National Academy of
Sciences, USA 88, 10357–10361.
Wells, R.M.G., Ashby, M.D., Duncan, S.J., Macdonald, J.A.,
1980. Comparative study of the erythrocytes and haemoglobins of nototheniid fishes from Antarctica. Journal of Fish
Biology 17, 517–527.
Wittmann, A., 2005. Bestimmung des sauerstofflimitierten
Temperaturtoleranzfensters beim Wattwurm Arenicola marina (L.). Diploma Thesis, Bremen.
Whiteley, N.M., Taylor, E.W., el Haj, A.J., 1996. A comparison
of the metabolic cost of protein synthesis in stenothermal and
eurythermal isopod crustaceans. American Journal of Physiology 271, R1295–R1303.
Wieser, W., 1986. Bioenergetik. Thieme, Verlag, Stuttgart,
245pp.
Wieser, W., 1995. Energetics of fish larvae, the smallest
vertebrates. Acta Physiologica Scandinavica 154, 279–290.
Wohlschlag, D.E., 1964. Respiratory metabolism and ecological
characteristics of some fishes in McMurdo Sound, Antarctica.
Antarctic Research Series. American Geophysical Union 1,
33–62.
Zakhartsev, M.V., De Wachter, B., Sartoris, F.J., Pörtner, H.O.,
Blust, R., 2003. Thermal physiology of the common eelpout
(Zoarces viviparus). Journal of Comparative Physiology B
173, 365–378.
Zakhartsev, M., Johansen, T., Pörtner, H.O., Blust, R., 2004.
Effects of temperature acclimation on lactate dehydrogenase of cod (Gadus morhua): genetic, kinetic and thermodynamic aspects. Journal of Experimental Biology 207,
95–112.
Zielinski, S., Pörtner, H.O., 1996. Energy metabolism and ATP
free-energy change of the intertidal worm Sipunculus nudus
below a critical temperature. Journal of Comparative
Physiology B 166, 492–500.
Zielinski, S., Pörtner, H.O., 2000. Oxidative stress and antioxidative defense in cephalopods: a function of metabolic rate or
age? Comparative Biochemistry and Physiology B 125,
147–160.
Zimmermann, C., Hubold, G., 1998. Respiration and activity of
Arctic and Antarctic fish with different modes of life: a
multivariate analysis of experimental data. In: di Prisco, G.,
Pisano, E., Clarke, A. (Eds.), Fishes of Antarctica. A
Biological Overview. Springer, Italia, pp. 163–174.

Download Report

Climate-dependent evolution of Antarctic ectotherms: An integrative

Paperzz.com

Your Paperzz