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First published online April 17, 2009
Journal of Experimental Biology 212, 1371-1376 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.030205
Thermal tolerance of crustacean larvae (zoea I) in two different populations of the kelp crab Taliepus dentatus (Milne-Edwards)
1 Estación Costera de Investigaciones Marinas and Center for Advanced
Studies in Ecology and Biodiversity, Departamento de Ecología, Facultad
de Ciencias Biológicas, Pontificia Universidad Católica de
Chile, Casilla 114-D, Santiago, Chile
2 Alfred-Wegener-Institut für Polar- und Meeresforschung, Marine Animal
Physiology, Postfach 120161, D-27515 Bremerhaven, Germany
* Author for correspondence (e-mail: Daniela.Storch{at}awi.de)
Accepted 6 February 2009
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: oxygen consumption, heart rate, swimming, mass, C:N ratio, zoea I, Taliepus dentatus, larvae, thermal tolerance, temperature
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Gaston, 2003;
Sanford et al., 2006).
Although evidence is mostly based on studies of thermal tolerance of adults,
water temperature can strongly influence planktonic larvae by affecting
survival, developmental time and growth, limiting recruitment and determining
species distribution (Gilman,
2006; Sanford et al.,
2006). However, our understanding of thermal tolerance and the
physiological limits of larval stages is quite limited, despite the fact that
larvae might experience stronger short- and long-term temperature fluctuations
and are more vulnerable to thermal and osmotic stresses than adults
(Anger et al., 2003).
Physiological studies can help to explain distribution patterns and understand
the mechanisms behind thermal sensitivity of organisms, which becomes
particularly important under a global warming scenario
(Pörtner and Knust,
2007).
A mismatch between oxygen demand and the limited capacity of oxygen supply
to tissues is hypothesized to be the first mechanism restricting survival at
the limits of the thermal tolerance window of marine organisms
(Frederich and Pörtner,
2000; Mark et al.,
2002; Pörtner,
2001; Pörtner,
2002; Pörtner and Knust,
2007). Thermal limitation becomes effective firstly at high
hierarchical levels of organization, the whole organism and its oxygen
delivery system and then at lower cellular and molecular levels
(Mark et al., 2002;
Pörtner et al., 2005).
Pejus temperatures are thought to represent the long-term physiological
temperature limits for a given species and are characterized by falling oxygen
levels in the body fluids (hypoxemia) and the resulting decrease in the
animal's aerobic scope. The progressively limited capacities of circulatory
and ventilatory mechanisms upon warming and cooling indicate a mismatch
between oxygen supply and demand (Frederich
and Pörtner, 2000). Further cooling or warming leads to low
or high critical threshold temperatures where aerobic scope vanishes and
transition to an anaerobic mode and progressive insufficiency of cellular
energy supply occurs (Pörtner,
2001; Pörtner et al.,
2005).
This recently developed conceptual framework of oxygen and capacity-limited
thermal tolerance was elaborated in adult individuals from various phyla but
has not yet been systematically explored in early life stages. In crustaceans,
thermal tolerance of larval stages is particularly interesting considering
their potential for dispersal and the strong short-term variations in
temperature that they may experience in the water column. We therefore
investigated whether a mismatch between oxygen demand and limited capacity of
oxygen supply to tissues occurs in larvae of a marine crustacean. We
determined the thermal tolerance of Taliepus dentatus (Milne-Edwards)
larvae (zoea I stage), integrating variables from organismal (whole animal
activity and oxygen consumption and body mass) to physiological [cardiac
performance: heart rate (fH), stroke volume
(VS) and cardiac output
(
)] and elemental levels [carbon (C)
and nitrogen (N) content]. We compared tolerance of acute temperature changes
in larvae from two different climatic zones in order to identify differences
in thermal adaptation. We used the kelp crab T. dentatus as a model
of a eurythermal species exhibiting a wide range of latitudinal distribution
along the coast of Chile. Two populations were chosen from southern and
central habitats more than 10 deg. apart in latitude along the Pacific coast
of Chile. To our knowledge our mechanistic analysis is the first to address
how temperature might affect the physiology of crab larvae and how the thermal
tolerance of the zoea might reflect the differentiation of the species into
thermally specialized sub-populations, thereby leading to a widening of the
distribution range of this species.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Ovigerous T. dentatus were collected
in southern Chile (SC) (Melinka, 43 deg.54'S, 73 deg.44'W)] and
central Chile (CC) (Las Cruces, 33 deg.29'S, 71 deg.38'W)] by
local professional divers during autumn/winter 2006 and brought to the
Estación Costera de Investigaciones Marinas of Las Cruces, Chile. Mean
annual seawater temperature ranges from 10.5°C in SC to 15.6°C in CC
(Astorga et al., 2003). Extreme
seawater temperatures varied between 8°C and 18°C at the southern
Chilean site and between 10°C and 21°C at the central Chilean site.
Five female crabs from each site were held individually in 50 l aquaria set up
with running seawater at 11°C, 34 psu, constant aeration and a 12 h:12 h
light:dark photoperiod until spawning. Newly hatched larvae were transferred
to 0.5 l culture vessels with a constant density of 20 individuals. Culture
water was changed once every 24 h by transferring all individuals using a
glass pipette to a clean vessel containing filtered, well-aerated seawater and
freshly hatched Artemia nauplii (Sanders Brine Shrimp Company, Ogden,
UT, USA). The larvae were starved for one day prior to experimentation in
order to provide uniform conditions. Experiments were conducted between autumn
and spring 2006.
The experimental protocol was standardized with respect to temperature
changes and acclimation time, and measurements of all parameters were taken
synchronously. All experiments were conducted within two days using
9–10-day-old zoea I because thermal tolerance might change during the
zoea l stage, depending on larval age. The 10th day is the middle of the
developmental period of zoea I, which lasts around 20 days at a rearing
temperature of 11°C (D.S., K.C. and M.F., in preparation). The rearing
temperature of 11°C will be referred to as the control temperature.
Immediately after the measurements at 11°C were finished, the system was
cooled/warmed to the next experimental temperature. One set of larvae was
progressively cooled from 11°C to 3°C and the second set was warmed
from 11°C to 27°C, at a rate of 4°C within two hours. Experimental
temperatures were 11°, 7° and 3°C for cooling experiments and
11°, 15°, 19°, 23° and 27°C for warming experiments.
Therefore, the number of replicates was doubled at 11°C. Larvae were
allowed to acclimate at each temperature for two hours before continuing to
decrease or increase temperature to the next experimental period. At each
experimental temperature, we measured: (1) larval activity, (2) oxygen
consumption rate, (3) cardiac performance, and (4) C:N ratio. Larval activity
(maxilliped and abdomen beat rates), oxygen consumption and cardiac
performance (fH, VS and
) were determined in individual zoea.
Five larvae from the different experimental mothers of each population were
used for each experimental condition. Five replicates from each population
were also used for fresh mass (FM), dry mass (DM) and C:N ratios, although in
this case, a pool of zoea larvae from each female was used.
Larval activity
Maxilliped and abdomen beat rates were monitored using a video flex camera
(Ken-A-Vision Mfg. Co. Inc., Kansas City, MO, USA). The camera was mounted
onto a binocular and connected to a time-lapse video recorder (Sony
Deutschland GmbH, Berlin, Germany). During the experiment, larvae were placed
beneath the binocular in a temperature-controlled microchamber filled with
seawater, which allowed the temperature to be changed according to the
experimental protocol without disturbing the larvae. The zoea was positioned
in the centre of the microchamber by gluing the dorsal spine of the
cephalothorax to a thin glass spine using rapid glue. The glass spine, in
turn, was attached to a glass table. The zoea was allowed to freely move its
maxillipeds and abdomen in the experimental chamber filled with filtered
seawater. The glass chamber was enclosed by aluminium foil to avoid visual
disturbance. After a 2 h recovery period from handling stress, the experiment
started at the control temperature. Afterwards, temperature was changed
according to the protocol (see above). At each experimental temperature, the
zoea was videotaped for 2 min. Maxilliped beating was calculated as the mean
number of beats per minute (beats min–1) from three 10 s
intervals. The beating of the abdomen was counted over a 90 s time interval
and was calculated as beats min–1. The timeframe for
measurements was adjusted based on the frequency of each movement. A two-way
analysis of variance (ANOVA) was conducted to test for the effect of site of
origin and temperature on maxilliped and abdomen beating. Maxilliped beat data
were square-root-transformed to meet the homocedasticity assumptions of the
ANOVA. Tukey tests were conducted for a posteriori analysis.
Oxygen consumption
Oxygen consumption rates were measured in individual zoea using a closed
respirometry system. Hamilton microliter precision syringes (volume: 500
µl; Hamilton Bonaduz AG, Bonaduz, Switzerland) were used as chambers.
Oxygen partial pressures were recorded by oxygen micro-optodes (needle-type,
fiber-optic microsensor, flat broken tip, diameter: 140 µm) connected to a
Microx TX2 (PreSens GmbH, Regensburg, Germany). Syringes were placed upside
down in a temperature-controlled seawater bath, containing air-saturated,
filtered (0.45 µm filter) seawater (salinity: 34 psu). The needle of the
microsensor was inserted from the side of the cannula. Prior to insertion,
optodes were calibrated in the same temperature-controlled seawater bath where
measurements took place. Larvae were carefully introduced into the barrel by
removing the plunger. After larvae were placed in the syringe, the plunger was
inserted and carefully brought to the desired volume of 40 µl. The
procedure took place entirely underwater to avoid introducing air bubbles.
Subsequently, the optode was inserted and the sensitive tip was positioned in
the middle of the respiration chamber. During the experimental trials, maximum
oxygen depletion did not exceed 20%. Maintaining oxygen levels above 80% of
saturation minimizes stress effects and the effects of hypoxia on thermal
tolerance. In order to correct for bacterial oxygen consumption, blanks were
run before and after measurements took place. At the end of the experiments,
larvae were taken out of the chambers, carefully dried with a paper towel and
weighed on a Sartorius bp 211 D balance (Göttingen, Germany). The overall
picture of temperature-dependent oxygen consumption of the zoea did not change
when expressed as µg O2 per fresh mass (µg O2
FM–1), µg O2 per dry mass (µg O2
DM–1) or µg O2 per individual (µg
O2 individual–1). Therefore, mean rates of oxygen
consumption are given as µg O2 per mg fresh mass per hour (µg
O2 mg FM–1 h–1) to highlight the
variation in mass-specific physiological rates, which is crucial to
understanding the underlying physiological mechanisms when comparing the two
populations. A two-way ANOVA was conducted to test for the effect of site of
origin and temperature on larval oxygen consumption. Data were log-transformed
to meet the assumptions of the ANOVA. A posteriori analysis (Tukey test) was
used to assess the differences among treatment levels.
Cardiac performance
fH and VS were determined using the
same video sequences as for maxilliped and abdominal activity. The zoea stage
of T. dentatus is transparent and the beating heart is clearly
visible. fH was obtained by using frame-by-frame analysis
of the videotape on an editing tape player counting the number of contractions
per unit time. The fH was calculated as the mean number of
beats min–1 from three 10 s intervals for each zoea.
VS was determined by advancing the tape frame-by-frame
until the heart reached its maximal dimension (end-diastolic volume) and its
minimal dimension (end-systolic volume). The images of a 10 s video sequence
were captured using a video frame grabber and digitizing program. The
dimensions of the heart were measured and used in a geometric equation to
calculate cardiac volumes. The heart was modelled as a prolate spheroid
[V=(4/3)
ab2 according to Harper and Reiber
(Harper and Reiber, 2004)],
where V is the cardiac volume, a is the length and
b is the height of the heart). VS was calculated
as the difference between end-diastolic and end-systolic ventricular volume
and expressed as nl per beat (nl beat–1).
was calculated as the product of
fH and VS.
A two-way ANOVA was conducted to test for the effects of site of origin and
temperature on fH, VS and
. For a posteriori analysis, Tukey
tests were used.
Larval mass and C:N ratio
Larval FM was measured in samples containing between 45 and 50 individuals,
which were carefully dried with a paper towel and weighed using a Sartorius bp
211D balance. In order to measure DM and C and N contents, we followed a
standard method; samples of five zoea were briefly rinsed in distilled water,
blotted dry on paper and subsequently frozen for storage at –20°C in
pre-weighed tin cartridges. Later, samples were dried to constant mass at
60°C, weighed on a microbalance (Sartorius) and analyzed for C:N ratio on
a Euro EA CHNSO Analyser (HEKAtech GmbH, Wegberg, Germany), using acetanilide
as the standard. DM is reported as µg per individual (µg
individual–1) and as a % of FM. The commonly used C:N ratio
was calculated to assess the differences in the lipid:protein ratio between
temperature and populations.
A two-way ANOVA was conducted to test for the effects of site of origin and temperature on larval FM and DM, C and N contents and C:N ratio. Data were not transformed as the assumptions of the ANOVA were met. Tukey tests were used for a posteriori analysis.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The influence of temperature was less pronounced on abdominal beat rate of the zoea than on maxilliped beat rate but was still significant (F=3.85; d.f.=6,66; P=0.002) (Fig. 1B). Lower abdomen beat rates were found at the extreme temperatures of 3°, 7° and 27°C (Tukey test, P<0.05). The highest abdomen beat rates were observed at the intermediate temperatures of 11°, 15°, 19° and 23°C (Fig. 1B) (P<0.05). No differences were detected between sites of origin (F=2.04; d.f.=1,66; P=0.16) and the interaction term was not significant (F=0.10; d.f.=6,66; P=0.99).
Oxygen consumption
Oxygen consumption rates did not follow a typical exponential function,
which is expected if standard metabolic rate is measured under rising
temperature. As the zoea is actively swimming in the water column, larval
oxygen consumption comprises standard metabolism and oxygen demand for
swimming, thereby including a term for temperature-dependent performance.
Oxygen consumption rates were significantly lower in zoea from CC than from SC
(F=16.42; d.f.=1,66; P<0.001)
(Fig. 2). Temperature affected
oxygen consumption rates of the larvae (F=20.34; d.f.=1,66;
P<0.001), following a similar pattern at both sites (the
interaction term was not significant; F=0.45; d.f.=6,66;
P<0.85) (Fig. 2).
The lowest temperature of 3°C showed the lowest oxygen consumption rates
(P<0.05) (Fig. 2).
Oxygen consumption increased significantly between 3°C and 7°C
(P<0.05), levelled off between 7°C and 11°C
(P>0.05) and increased again at 15°C (P<0.05)
(Fig. 2). The highest oxygen
consumption rates were found between 19°C and 23°C
(P<0.05). Then oxygen consumption rates dropped at 27°C
(P<0.05) (Fig. 2)
in zoea from SC whereas no changes were observed for zoea from CC between
15°C and 27°C (P>0.05).
|
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followed the trend of
fH and oxygen consumption rates. A significant interaction
between site of origin and temperature in the ANOVA precluded us from testing
the main effects (F=2.36; d.f.=6,66; P=0.04)
(Fig. 3C). The interaction was
significant because the differences between sites varied among temperatures.
was two times higher in larvae from
SC at 3°, 7° and 11°C (P<0.05) whereas no significant
differences among sites were found at the higher temperatures
(P>0.05) (Fig. 3C).
The lowest was observed in larvae
from CC exposed to 3°C (P<0.05).
Mass and elemental composition
Temperature had no effect on FM, DM, C and N contents and on C:N ratio of
zoea I in the acute thermal tolerance experiment whereas the site of origin
had a clear effect on larval FM and DM as well as on C and N contents (Tables
1 and
2). Larvae from SC exhibited
higher FM, DM and higher C and N contents (P always<0.05). It
should be noted that no difference between sites was found for the % DM of FM
and the C:N ratio (Tables 1 and
2). In all cases, the
interaction terms were not significant
(Table 1).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Pörtner et al.,
2005), resulting in narrow temperature tolerance windows for
maxilliped beat rates. Temperature-dependent oxygen consumption rates
(indicating aerobic oxygen demand) were reflected in
(indicating a key role for oxygen
delivery capacities). VS and mass were insensitive to
acute temperature changes but showed differences between populations. By
contrast, elemental composition was insensitive to both acute and long-term
temperature changes.
The increase in oxygen consumption rates with rising temperature is
typically exponential within the passive thermal tolerance window set by upper
and lower critical temperatures
(Pörtner et al., 2005;
Wittmann et al., 2008). Such
an exponential increase was not observed in larval T. dentatus,
indicating that animals were not displaying standard metabolic rate.
Non-exponential temperature-dependent oxygen consumption has previously been
detected in larvae of Cancer irroratus
(Sastry, 1979). Planktonic
zoea of T. dentatus and C. irroratus swim actively in the
water column. Therefore, oxygen consumption comprises the energy demand for
both maintenance and swimming activity and thus includes elements of
performance or aerobic scope that are crucial in setting zoea l thermal
tolerance at ecosystem level (Pörtner
and Knust, 2007; Pörtner
and Farrell, 2008). The decrease in aerobic scope affects higher
functions such as activity and behavior and sets the lower and upper so-called
pejus temperatures for long-term survival of a species
(Pörtner and Knust, 2007;
Wang and Overgaard, 2007).
This was observed in zoea I of T. dentatus; constantly low maxilliped
beat rates as oxygen consumption rates increase at temperature >15°C
suggest that increasing baseline oxygen demand constrains aerobic scope and
limits the level of maxilliped activity.
A further decrease in the capacity of zoea to perform aerobically is
indicated by the levelling-off in oxygen consumption at 19°C. Such a
pattern has been shown to denote the critical temperature beyond which
anaerobic metabolism sets in and supports only short-term survival
(Frederich and Pörtner,
2000; Mark et al.,
2002). Oxygen consumption remained constant even though
and fH continued
to increase beyond 19°C. This suggests that oxygen supply through the
cardio-respiratory system becomes insufficient beyond critical temperatures
when oxygen concentration in the hemolymph has fallen to critically low levels
no longer fully supporting aerobic metabolism
(Frederich and Pörtner,
2000). As a corollary, our finding in zoea I supports our
hypothesis and demonstrates that thermal tolerance is oxygen- and
capacity-limited in larvae of marine decapod crustaceans.
At first sight, lower temperature sensitivity of abdominal activity in
comparison with maxilliped beat rates seems to contradict the hypothesis.
However, in addition to eliciting locomotion in the water column, the abdomen
also serves to provide additional oxygen to the larvae as demonstrated for
zoea from Nephrops norwegicus
(Spicer and Eriksson, 2003).
Movements of the abdomen might improve diffusion gradients for oxygen and may
therefore be maintained beyond high and low pejus temperatures, when
maxilliped activity is already constrained.
The thermal tolerance window of zoea from SC was found to be shifted to
lower temperatures when compared with those from CC. Larval functions in zoea
from SC displayed cold compensation indicated by higher maxilliped beat rates,
oxygen consumption rates and better cardiac performance at the same
temperatures. Oxygen demand for maintenance and activity at low temperatures
(3–11°C) was covered by enhanced oxygen delivery evidenced by
increased fH, VS and
in larvae from SC. High cardiac
performance at 3°C may enable larvae from SC to remain as active as larvae
from CC at 11°C. In contrast to zoea from SC, zoea from CC showed
increased maxilliped beating when temperature was reduced from 11°C to
7°C. This suggests that larvae are stimulated by temperature change, which
might serve to escape unfavourably low temperatures and to return to warmer
physiologically tolerable water masses. These observed activity responses in
zoea of T. dentatus resulted in comparable oxygen consumption rates
at 7°C and 11°C. The oxygen demand for swimming at 7°C is
supported by maintaining fH and
as high as under control conditions
at 11°C.
Interestingly, at 7°C significantly higher mass-specific oxygen
consumption rates at similar activity rates (maxilliped and abdominal) were
found in larvae from SC than from CC. This suggests that tissue oxygen demand
for maintenance in the southern population is higher, which is characteristic
of metabolic cold adaptation. Higher FM and DM and similar C:N ratios suggest
that the composition (water content:DM) and the lipid:protein ratio (C:N) of
the larvae remain unchanged whereas body size increases in the cold (D.S.,
K.C. and M.F., unpublished data) providing more space for mitochondrial
proliferation. A rise in mitochondrial densities and increased mitochondrial
capacities to compensate for the cold-induced slowing of metabolism increases
the costs of mitochondrial maintenance and whole organism oxygen demand
(Sommer and Pörtner,
2004; Tschischka et al.,
2000). It would also explain the observed increase in oxygen
consumption of cold eurythermal zoea from the south.
At high temperatures, zoea from CC perform slightly better than zoea from SC suggested by: (1) higher maxilliped beat rates in zoea from CC, which can be related to higher capacities to perform aerobically, and (2) constant maxilliped beating of zoea from CC between 11°C and 15°C, which contrasts the drastic decrease in zoea from SC. Improved cardiac performance of zoea from SC compared with zoea from CC at low temperatures cannot be preserved at higher temperatures, resulting in the same cardiac outputs at high temperatures in larvae from both populations. This represents a decrease in aerobic performance for larvae in the southern population to similar values as found in the central population.
As a corollary, we have demonstrated how zoea I from the temperate and southern T. dentatus populations responded to acute experimental and latitudinal temperature variations. Thermal limits in zoea of T. dentatus become visible at the highest organizational level and are seen in decreasing activity followed by a reduction in cardio-respiratory performance. On evolutionary timescales, larvae from different populations adjust not only the cardio-respiratory system but they also adjust mass and size to adapt to their prevailing environmental temperature regime (D.S., unpublished observations). Adaptive plasticity in maintaining fitness according to climate is reflected in constant C:N ratios between populations. The small but clear shift between thermal tolerance windows between populations suggests an optimization of reaction norms and local adaptation in larvae of T. dentatus. Lower mean annual seawater temperatures and lower extreme temperatures match the shifted temperature tolerance windows reported in the present study for larvae from the SC site. Therefore, this differentiation allows the species to cover a wider range of distribution than when restricted to one and the same thermal window for all populations. This also means that larvae of T. dentatus from one population, although having a great potential for dispersal by wind-driven transport along the Chilean coast, seem to be restricted to the environmental thermal regime they developed and hatched in. Further comparative studies of thermal tolerance of crustacean larvae within and between populations are needed to confirm this observation as a unifying principle.
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Footnotes |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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