Comparative Biochemistry and Physiology, Part A 156 (2010) 389–393

Contents lists available at ScienceDirect

Comparative Biochemistry and Physiology, Part A

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c b p a

Effects of elevated temperature on coral reef fishes: Loss of hypoxia tolerance and
inability to acclimate
Göran E. Nilsson a,⁎, Sara Östlund-Nilsson a, Philip L. Munday b,c
a
Physiology Programme, Department of Molecular Biosciences, University of Oslo, P.O. Box 1041, NO-0316 Oslo, Norway
b
School of Marine and Tropical Biology, James Cook University, Australia
c
ARC Centre of Excellence for Coral Reef Studies, James Cook University, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Water temperature is expected to rise on coral reefs due to global warming. Here, we have examined if
Received 21 January 2010 increased temperature reduces the hypoxia tolerance of coral reef fish (measured as critical [O2]), and if
Received in revised form 10 March 2010 temperature acclimation in adults can change the resting rate of O2 consumption and critical [O2]. Two
Accepted 10 March 2010
common species from Lizard Island (Great Barrier Reef, Australia) were tested, Doederlein's cardinalfish
Available online 15 March 2010
(Ostorhinchus doederleini) and lemon damselfish (Pomacentrus moluccensis). In both species, a 3 °C rise in
Keywords:
water temperature caused increased oxygen consumption and reduced hypoxia tolerance, changes that were
Cardinalfish not reduced by acclimation to the higher temperature for 7 to 22 days. Critical [O2] increased by 71% in the
Climate change cardinalfish and by 23% in the damselfish at 32 °C compared to 29 °C. The higher oxygen needs are likely to
Coral reef fish reduce the aerobic scope, which could negatively affect the capacity for feeding, growth and reproduction.
Damselfish The reduced hypoxia tolerance may force the fishes out of their nocturnal shelters in the coral matrix,
Hypoxia exposing them to predation. The consequences for population and species survival could be severe unless
Metabolism developmental phenotypic plasticity within generations or genetic adaptation between generations could
Oxygen consumption
produce individuals that are more tolerant to a warmer future.
Thermal tolerance
© 2010 Elsevier Inc. All rights reserved.

1. Introduction uptake (aerobic scope) is expected to decrease (Pörtner, 2001; Pörtner

Tropical organisms are predicted to be especially sensitive to global
warming because they have evolved within a narrow and stable thermal
range (Huey and Hertz, 1984; Bush and Hooghiemstra, 2005; Hoegh-
Guldberg et al., 2007; Tewksbury et al., 2008), and therefore, might have
a narrow thermal tolerance range. This is true for corals, where just a
1–2 °C increase in maximum sea-surface temperature can cause
bleaching and death (Hoegh-Guldberg, 1999). While considerable
research effort has been directed at investigating the effects of elevated
ocean temperature on coral communities (e.g. Hoegh-Guldberg, 1999;
Hughes et al., 2003; Sheppard, 2003; Donner et al., 2005), much less is
known about the direct effects of increased temperature on fishes and
other organisms that inhabit coral reefs (Munday et al., 2008).
The effect of increasing temperature on aerobic performance is
thought to be the most important physiological mechanism determin-
ing the survival of fish populations faced with a rise in ocean
temperature (Pörtner, 2001; Pörtner and Knust, 2007; Pörtner and
Farrell, 2008). As temperature increases the span between resting
oxygen consumption (resting MO2) and the maximal rate of oxygen
⁎ Corresponding author. Tel.: + 47 92057838.
E-mail address: g.e.nilsson@imbv.uio.no (G.E. Nilsson).
and Farrell, 2008). A reduction in aerobic scope could cause a loss of
fitness because less energy would be available to devote to feeding,
growth and reproduction. The limited capacities of the circulatory and
ventilatory systems to keep pace with the increased oxygen demands of
basal metabolism at higher temperatures is thought to be the primary
reason for a reduction in aerobic scope (Fry, 1971; Pörtner and Knust,
2007). Indeed, a recent study of five coral reef fish species showed that
aerobic scope declined when ocean temperature was increased 2–4 °C
above summer average temperature, and it was primarily an elevation
of resting MO2 at higher temperatures that caused aerobic scope to
decline (Nilsson et al., 2009).
In addition to reducing aerobic scope, an increase in resting MO2 is
also likely to reduce the hypoxia tolerance of a fish, because a fish with a
higher basal metabolism will need to extract more oxygen from the
water to sustain its metabolic demands (Nilsson and Randall, 2010, for
review). So far, the effect of rising temperature on the hypoxia tolerance
of coral reef fishes has not been studied, although it is clear that coral
reefs can become severely hypoxic at night, and reef fishes rely on their
hypoxia tolerance to utilize the hypoxic coral matrix as a nocturnal
refuge from predators (Nilsson et al., 2007). Thus, coral reef fishes in
general display quite low critical oxygen concentrations ([O2]crit),
generally around 20–30% of air saturation at 29 °C (Nilsson and Östlund-
Nilsson, 2004). [O2]crit is the lowest [O2] at which resting MO2 can be
maintained.

1095-6433/$ – see front matter © 2010 Elsevier Inc. All rights reserved.
doi:10.1016/j.cbpa.2010.03.009
390 G.E. Nilsson et al. / Comparative Biochemistry and Physiology, Part A 156 (2010) 389–393
Ectothermic vertebrates living in temperate and subtropical cli-
mates, with considerable seasonal variation in ambient temperature,
show temperature acclimation: a suite of physiological and biochemical
adjustments that, usually within a week or less, reduce the acute in-
crease in metabolic rate and fall in hypoxia tolerance caused by a rise in
body temperature (Whittow, 1970; Barrionuevo and Fernandes, 1998;
Angilletta, 2009). However, ectothermic vertebrates that have evolved
at relatively constant temperatures generally show a low capacity for
temperature acclimation (Johnston and Bennett, 1996; Tewksbury et al.,
2008). Antarctic fishes are prime examples of such “stenothermal”
species (Somero and DeVries, 1967; Wilson et al., 2001, 2002; but see
Franklin et al., 2006). Similarly, tropical reptiles (Tsuji, 1988) and
tropical amphibians (Feder, 1982) have been found to lack the ability to
temperature acclimate. With regard to tropical coral reef teleosts, no
studies has so far examined their ability to acclimate to changing
temperatures, but there is one study on a coral reef elasmobranch, the
bamboo shark (Chiloscyllium plagiosum), suggesting that it has no
capacity for temperature acclimation (Tullis and Baillie, 2005). In
addition to temperature acclimation in adults, there is the possibility of
developmental acclimation occurring during early life stages, and, of
course, natural selection may promote genotypes with better suited
physiological temperature optima (Angilletta, 2009).
Average sea-surface temperatures in the vicinity of coral reefs are
projected to rise by at least several °C over the next 100 years due to
global warming (Guinotte et al., 2003; Lough, 2007; Munday et al.,
2009). If temperature induced increase in basal metabolic rate in coral
reef fishes cannot be counteracted by acclimation, a resultant reduction
in hypoxia tolerance and aerobic scope will inevitably have significant
effects on individual performance, with potential implications for long-
term population sustainability (Munday et al., 2008). Consequently, the
aims of the present study were: (1) to examine if increased temperature
reduces the hypoxia tolerance of coral reef fish (measured as [O2]crit),
and (2) if temperature acclimation in adults can change the resting MO2
and [O2]crit. Experiments were carried out at Lizard Island (Great Barrier
Reef, Australia) on two common species at this location representing
two families, Apogonidae and Pomacentridae: Doederlein's cardinalfish
(Ostorhinchus doederleini) and lemon damselfish (Pomacentrus moluc-
censis). Fish were either kept at 29 °C, which is the long-term average
summer sea-surface temperature at Lizard Island (Lough, 1999), or
allowed to acclimate for 7–22 days to 32 °C. This is within the range of
maximum summer sea-surface temperatures recorded for short periods
at Lizard Island (maximum 32.7 °C, Lough, 1999). Moreover, average
sea-surface temperatures on the GBR are predicted to increase by up to
3 °C over the next 50–100 years (Lough, 2007, 2008), therefore, 32 °C is
expected to be closer to the average sea-surface temperature at Lizard
Island by the end of this century.
2. Materials and methods
All experiments were carried out between December 2008 and
January 2009 at Lizard Island Research Station (LIRS; www.lizardisland.
net.au) on the Northern Great Barrier Reef (14°40′S 145°28′E). Adults of
O. doederleini (weighing 1.49 ± 0.34 g) and P. moluccensis (weighing
3.34 ± 1.24 g; mean± S.D.) were caught in the Lizard Island lagoon,
either by hand nets at low tide at night or using a hand net after lightly
anaesthetizing them with clove oil while SCUBA diving at a depth of
2–5 m (see Nilsson & Östlund-Nilsson, 2004). All fish were immediately
transferred to 50 l shaded out-door aquaria continuously supplied with
fresh seawater pumped directly from the ocean. Water oxygen level in
the aquaria varied between 95 and 100% of air saturation. Controls were
kept at 28.5–29.5 °C, which was the current ocean temperature. Other
fish were kept in identical aquaria where the water temperature was
increased over 1–2 days with aquarium heaters to 32 °C (max daily
variation was ±0.5 °C). The fish were kept at each temperature for
approximately 7–22 days prior to experimentation. Due to a progressive
increase in mortality in O. doederleini after 8 days at 32 °C, indicating an
inability to tolerate this temperature for several days, this species could
not be tested after a longer acclimation period than 7 days. Fish were fed
twice daily to satiation with frozen blood worms and INVE Aquaculture
Nutrition NRD 12/20 fish pellets, but they were starved for 24 h before
determination of MO2 and [O2]crit. The measurements were carried out
in shaded daylight (09.00–18.00 h).
2.1. Respirometry for measuring resting MO2 and [O2]crit
This method has been described previously by Nilsson & Östlund-
Nilsson (2004). In short, each fish was allowed to acclimate in the
respirometer (with water flowing through) for 2–3 h, whereupon water
supply to the chamber (a 750 ml plexi glass cylinder with 80 mm inner
diameter) was closed off and the fall in water oxygen was continuously
recorded with an oxygen electrode for 10–20 min (OXI 340i from WTW,
Germany, calibrated daily). The respirometer was submerged in a tem-
perature-controlled aquarium. All recording were done at oxygen levels
of 70–100% of air saturation. Previous experiments have shown that
acclimation periods longer than 2 h in the chamber do not further
reduce MO2 (Nilsson and Östlund-Nilsson, 2004; Nilsson et al., 2009).
The experiments were terminated when [O2]crit had been reached. MO2
in mg O2 kg− 1 h− 1 (fish wet weight) was plotted against water [O2],
measured as % of air saturation. The [O2]crit was determined by fitting
two linear regression lines to the curve, one for the normoxic (oxygen
independent) part of the curve, and one for the steeply falling hypoxic
part. The point where these lines crossed was taken as the [O2]crit. Fish
kept at 29 °C were tested at 29, 31 and 32 °C, while fish acclimated to
32 °C were tested at 32 °C.
All values reported are means ± S.D. Graph-Pad In-Stat 2.01 was
used for statistical analysis. ANOVA followed by Student's Newman–
Keuls multiple comparisons test were used to compare result for 31 and
32 °C to the control temperature (29 °C), and for evaluating possible
effects of different acclimation times (0, 7, 10 or 22 days). In addition,
linear regression and correlation analysis was used to test for the
expected correlation between MO2 and [O2]crit. Statistical significance
level was P b 0.05.
3. Results
Both species of fish showed significant rises in MO2 and [O2]crit during
acute exposure to a higher temperature, and neither of them displayed
any significant signs of temperature acclimation of either MO2 or [O2]
crit. For 29 °C-acclimated P. moluccensis, MO2 rose from 283±56 mg
O2 kg− 1 h− 1 at 29 °C to 398±85 mg O2 kg− 1 h− 1 when acutely exposed
to 32 °C in the respirometer, and this rise persisted even after 10 and
22 days of acclimation to 32 °C (Fig. 1A). Similarly, for 29 °C-acclimated
P. moluccensis, [O2]crit increased from 25.6±3.5% of air saturation at 29 °C
to 31.5±3.4% of air saturation during acute exposure to 32 °C, and this rise
persisted after 10–22 days of acclimation to the higher temperature
(Fig. 1B). Indeed, with regard to both MO2 and [O2]crit of P. moluccensis,
there were no significant differences between the acclimation groups
(0, 10 and 22 days) when measured at 32 °C. The Q10 for resting MO2 of
P. moluccensis was 2.2 (calculated for the span 29–32 °C for fish measured
at their acclimation temperatures).
In 29 °C-acclimated O. doederleini, MO2 rose from 266 ± 33 mg
O2 kg− 1 h− 1 at 29 °C to 356 ± 92 mg O2 kg− 1 h− 1 when acutely
exposed to 32 °C in the respirometer, and this rise persisted after
7 days of acclimation to 32 °C (Fig. 2A). For this species [O2]
crit increased from 28.2 ± 2.8 to 48.3 ± 10.0% of air saturation when
29 °C-acclimated fish were acutely exposed to 32 °C, and [O2]crit
remained high after 7 days of acclimation to 32 °C (Fig. 2B). As
mentioned, it was not possible to acclimate O. doederleini for longer
periods as fish started dying after 8 days at 32 °C. No such mortality
was seen in fish kept at 29 °C. At 32 °C, O. doederleini showed no
significant differences in MO2 and [O2]crit between the acclimation
groups (0 and 7 days). The Q10 for resting MO2 of O. doederleini was
 G.E. Nilsson et al. / Comparative Biochemistry and Physiology, Part A 156 (2010) 389–393
Fig. 1. A–B. MO2 (A) and [O2]crit (B) in P. moluccensis at 29 °C (current ocean
temperature; n = 12) and at two higher temperatures. The fish were either acutely
exposed to 31 °C (n = 6) or 32 °C (n = 6) in the respirometer, or allowed to acclimate to
32 °C for 10 (n = 6) or 22 days (n = 9) before measured at this temperature. The highest
temperature caused a significant rise in MO2 and [O2]crit in all three acclimation
groups, while there were no significant differences between the acclimation groups. For
clarity, the 32 °C groups have been spread out along the x-axis. Values are means ± S.D.
* = P b 0.05; ** = P b 0.01; *** = P b 0.001.
6.1 (calculated for the span 29–32 °C for fish measured at their accli-
mation temperatures).
Since it is likely that much of the temperature induced rise in [O2]crit is
related to the increased MO2 seen at higher temperatures, the correlation
between these variables was examined. For both species the correlation
was highly significant, with r2 =0.285 for P. moluccensis (Pb 0.0005;
Fig. 3) and r2 =0.359 for O. doederleini (Pb 0.001; Fig. 4).
4. Discussion
Our results indicate that the two coral reef fish species studied lack the
ability to acclimate their metabolic rate (measured as oxygen consump-
tion) and hypoxia tolerance to an increase in ambient temperature, at
least as adults. P. moluccensis and O. doederleini represent two major
families of coral reef fish, damselfishes (Pomacentridae) and cardinal
fishes (Apogonidae), respectively. The inability of the apogonid to tolerate
more than a week at 32 °C corroborates previous findings that cardinal
fishes are particularly sensitive to a rise in ambient temperature (Nilsson
et al., 2009). Furthermore, in this study, increased water temperature had
a larger effect on hypoxia tolerance in the cardinalfish than it did in the
damselfish. An increase of 3 °C caused [O2]crit to increase by 71% in the
391
Fig. 2. A–B. MO2 (A) and [O2]crit (B) in O. doederleini at 29 °C (current ocean
temperature; n = 8) and at two higher temperatures. The fish were either acutely
exposed to 31 °C (n = 7) or 32 °C (n = 6) in the respirometer, or allowed to acclimate to
32 °C for 7 days (n = 6) before measured at this temperature. The highest temperature
caused a significant rise in MO2 and [O2]crit in all three acclimation groups ([O2]crit was
also significantly increased at 31 °C), while there were no significant differences
between the acclimation groups. For clarity, the 32 °C groups have been spread out
along the x-axis. Values are means ± S.D. * = P b 0.05; ** = P b 0.01.
cardinalfish, from 28.2% to 48.3% of air saturation, but only by 23%, from
25.6% to 31.5% of air saturation, in the damselfish. This is further evidence
that responses to global warming will vary among species and that
cardinalfishes may be one of the most thermally sensitive groups of coral
reef fishes.
As expected, there was a significant correlation between the increase
in MO2 and [O2]crit for both species of fish. A straightforward expla-
nation for this is that a higher minimum level of oxygen will be needed
to sustain a higher rate of oxygen consumption, and this type of rela-
tionship has been observed previously (Fry and Hart, 1948; Schurmann
and Steffensen, 1997; Sollid et al., 2005). Thus, the high [O2]crit at 32 °C
is most likely an effect of the temperature induced elevation of MO2.
Having a high [O2]crit could be problematic for many reef fish species.
Coral reef fish in general have been found to have a strikingly low [O2]
crit (at present day ocean temperature) (Nilsson and Östlund-Nilsson,
2004), and this widespread hypoxia tolerance is probably needed to
allow them to seek nocturnal shelter from predators in the coral
matrix — a habitat that can become severely hypoxic at night (Nilsson et
al., 2007). Thus, a future loss of hypoxia tolerance could force coral reef
fishes out of their nocturnal shelters and thereby expose them to an
increased risk of predation, with potentially negative consequences at
392 G.E. Nilsson et al. / Comparative Biochemistry and Physiology, Part A 156 (2010) 389–393
Fig. 3. Correlation between MO2 and [O2]crit in P. moluccensis. The material includes all
fishes tested at 29, 31 and 32 °C, and all three acclimation groups.
the population and species level. Reduced hypoxia tolerance at elevated
temperatures could therefore be a contributing factor to the range of
geographic locations that populations of thermally sensitive species can
persist in a warmer climate.
Our results suggest that adult coral reef fishes have no significant
capacity to acclimate to elevated water temperatures as adults. This is
perhaps not surprising as they live in a relatively stenothermal environ-
ment. Thermal acclimation demands a suite of enzymes with different
thermal optima, and enzymatic systems that are capable of optimizing
the lipid composition of cellular and subcellular membranes (Battersby
and Moyes, 1998; Watabe, 2002; Gracey et al., 2004). If the ancestors of
coral reef fishes had such systems, these may have been lost after many
generations at the relatively constant temperature of tropical coral reefs.
Although we found no evidence of thermal acclimation in adult fishes, it
is possible that some acclimation could occur through the process of
Fig. 4. Correlation between MO2 and [O2]crit of O. doederleini. The material includes all
fishes tested at 29, 31 and 32 °C, and both acclimation groups.
developmental plasticity. Exposure to elevated temperatures early in
life may condition enzymatic systems to operate more efficiently at
elevated temperature. Future studies could rear coral reef fishes from
birth at control and elevated temperatures to investigate if there is any
capacity for thermal developmental plasticity in these species and if this
can confer some degree of adaptive thermal acclimation.
We kept fish at 32 °C for 7 to 22 days, which should be sufficient time
for temperature acclimation to become apparent. In fishes that are able
to acclimate to an increase in water temperature, the process usually
takes 1 week or less (while cold-acclimation takes longer) and in the
case of a tropical freshwater fish where temperature acclimation has
been observed, it is completed in just 1–2 days (Barrionuevo and
Fernandes, 1998, for review). Our data is also in line with the only
previous examination of metabolic temperature acclimation in a coral
reef fish, the bamboo shark. Like the coral reef teleosts we studied, this
elasmobranch was found to lack the ability to acclimate to a rise in water
temperature over a period of days to weeks (Tullis and Baillie, 2005).
Indeed, our data is in line with several previous studies revealing a lack
of capacity for temperature acclimation in stenothermal vertebrates,
including tropical amphibians and reptiles, and Antarctic fishes (Somero
and DeVries, 1967; Johnston and Bennett, 1996; Wilson et al., 2001,
2002; Tewksbury et al., 2008).
To conclude, our study of two species of coral reef fish revealed that a
3 °C rise in water temperature induces an increase in oxygen needs and
a loss of hypoxia tolerance, changes that were not reduced by accli-
mation to the higher temperature for 7 to 22 days. The rise in oxygen
needs are likely to reduce the aerobic scope of the fishes, thereby
reducing the amount of energy that can be allocated to feeding, growth
and reproduction, while the loss of hypoxia tolerance may force the
fishes out of their nocturnal shelters in the coral matrix, exposing them
to predation. The consequences of these changes for population and
species survival could be severe. Long-term rearing experiments are
now needed to test if phenotypic plasticity during development, or
natural selection favoring warm water tolerant genotypes, could com-
pensate for the short-term physiological effects of global warming on
coral reef fishes.
Acknowledgements
We thank the LIRS staff for enthusiastic help and great hospitality. This
study was supported by funding from the University of Oslo to G. E. N. and
from the Australian Research Council to P. L. M. The experiments followed
ethical guidelines from James Cook University.
References
Angilletta Jr, M.J., 2009. Thermal adaptation: a theoretical and empirical synthesis.
Oxford University Press, Oxford.
Barrionuevo, W.R., Fernandes, M.N., 1998. Time-course of respiratory metabolic adjust-
ments of a South American fish, Prochilodus scrofa, exposed to low and high temper-
atures. J. Appl. Ichthyol. 14, 37–41.
Battersby, B.J., Moyes, C.D., 1998. Influence of acclimation temperature on mitochon-
drial DNA, RNA, and enzymes in skeletal muscle. Am. J. Physiol. Regul. Integr. Comp.
Physiol. 275, R905–R912.
Bush, M.B., Hooghiemstra, H., 2005. Tropical biotic responses to climate change. In:
Lovejoy, T.E., Hannah, L. (Eds.), Climate Change and Biodiversity. Yale University
Press, New Haven, pp. 125–137.
Donner, S.D., Skirving, W.J., Little, C.M., Oppenheimer, M., Hoegh-Guldberg, O., 2005.
Global assessment of coral bleaching and required rates of adaptation under climate
change. Global Change Biol. 11, 1–15.
Feder, M.E., 1982. Environmental variability and thermal acclimation of metabolism in
tropical anurans. J. Therm. Biol. 7, 23–28.
Franklin, C.E., Davison, W., Seebacher, F., 2006. Antarctic fish can compensate for rising
temperatures: thermal acclimation of cardiac performance in Pagothenia borch-
grevinki. J. Exp. Biol. 210, 3068–3074.
Fry, F.E.J., 1971. The effect of environmental factors on the physiology of fish. Fish Physiol.
VI, 1–98.
Fry, F.E.J., Hart, J.S., 1948. The relation of temperature to oxygen consumption in the
goldfish. Biol. Bull. 94, 509–519.
Gracey, A.Y., Fraser, E.J., Li, W.Z., Fang, Y.X., Taylor, R.R., Rogers, J., Brass, A., Cossins, A.R.,
2004. Coping with cold: an integrative, multitissue analysis of the transcriptome of
a poikilothermic vertebrate. Proc. Natl. Acad. Sci. USA 101, 16970–16975.
 G.E. Nilsson et al. / Comparative Biochemistry and Physiology, Part A 156 (2010) 389–393
Guinotte, J.M., Buddemeier, R.W., Kleypass, J.A., 2003. Future coral reef habitat marginality:
temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22,
551–558.
Hoegh-Guldberg, O., 1999. Climate change, coral bleaching and the future of the world's
coral reefs. Mar. Freshw. Res. 50, 839–866.
Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greenfield, P., Gomez, E.,
Harvell, C.D., Sale, P.F., Edwards, A.J., Caldeira, K., Knowlton, N., Eakin, C.M., Iglesias-
Prieto, R., Muthiga, N., Bradbury, R.H., Dubi, A., Hatziolos, M.E., 2007. Coral reefs under
rapid climate change and ocean acidification. Science 318, 1737–1742.
Huey, R.B., Hertz, P.E., 1984. Is a jack-of-all temperatures a master of none? Evolution
38, 441–444.
Hughes, T.P., Baird, A.H., Bellwood, D.R., Card, I.M., Connolly, S.R., Folke, R., Grosberg, R.,
Hoegh-Guldberg, O., Jackson, J.B.C., Kleypas, J., Lough, J.M., Marshall, P., Nyström, M.,
Palumbi, S.R., Pandolfi, J.M., Rosen, B., Roughgarden, J., 2003. Climate change, human
impacts, and the resilience of coral reefs. Science 301, 929–933.
Johnston, I.A., Bennett, A.F., 1996. Animals and temperature: phenotypic and evolutionary
adaptation. Cambridge University Press, Cambridge.
Lough, J.M., 1999. Sea surface temperatures on the Great Barrier Reef: a contribution to
the study of coral bleaching. GBRMPA Research Publication, 57. Great Barrier Reef
Marine Park Authority, Townsville, pp. 1–31.
Lough, J., 2007. Climate and climate change on the Great Barrier Reef. In: Johnson, J.E.,
Marshall, P.A. (Eds.), Climate Change and the Great Barrier Reef. Great Barrier Reef
Marine Park Authority and Australian Greenhouse Office, Townsville, pp. 15–50.
Lough, J.M., 2008. Shifting climate zone for Australia's tropical marine ecosystems.
Geophys. Res. Lett. 35, L14708.
Munday, P.L., Jones, G.P., Pratchett, M.S., Williams, A.J., 2008. Climate change and the future
for coral reef fishes. Fish and Fish. 9, 261–285.
Munday, P.L., Leis, J.M., Lough, J.M., Paris, C.B., Kingsford, M.J., Berumen, M.L., Lambrechts, J.,
2009. Climate change and coral reef connectivity. Coral Reefs 28, 379–395.
Nilsson, G.E., Östlund-Nilsson, S., 2004. Hypoxia in paradise: widespread hypoxia
tolerance in coral reef fishes. Proc. Roy. Soc. Ser. B, Biol. Lett. Suppl. 271, S30–S33.
Nilsson, G.E., Randall, D.J., 2010. Adaptations to hypoxia in fishes. In: Nilsson, G.E. (Ed.),
Respiratory Physiology of Vertebrates. Cambridge University Press, Cambridge.
Nilsson, G.E., Hobbs, J.-P.A., Östlund-Nilsson, S., 2007. Respiratory ecophysiology of coral-
reef teleosts. J. Exp. Biol. 210, 1673–1686.
393
Nilsson, G.E., Crawley, N., Lunde, I.G., Munday, P.L., 2009. Elevated temperature reduces
the respiratory scope of coral reef fishes. Global Change Biol. 15, 1405–1412.
Pörtner, H.O., 2001. Climate change and temperature-dependent biogeography: oxygen
limitation of thermal tolerance in animals. Naturwissenschaften 88, 137–146.
Pörtner, H.O., Farrell, A.P., 2008. Physiology and climate change. Science 322, 690–692.
Pörtner, H.O., Knust, R., 2007. Climate change affects marine fishes through oxygen
limitation of thermal tolerance. Science 315, 95–97.
Schurmann, H., Steffensen, J.F., 1997. Effects of temperature, hypoxia and activity on the
metabolism of juvenile Atlantic cod. J. Fish Biol. 50, 1166–1180.
Sheppard, C.R.C., 2003. Predicted recurrences of mass coral mortality in the Indian
Ocean. Nature 425, 294–297.
Sollid, J., Weber, R.E., Nilsson, G.E., 2005. Temperature alters the respiratory surface area of
crucian carp Carassius carassius and goldfish Carassius auratus. J. Exp. Biol. 208,
1109–1116.
Somero, G.N., DeVries, A.L., 1967. Temperature tolerance of some Antarctic fishes. Science
156, 257–258.
Tewksbury, J.J., Huey, R.B., Deutsch, C.A., 2008. Putting the heat on tropical animals.
Science 320, 1296–1297.
Tsuji, J.S., 1988. Thermal acclimation of metabolism in sceloporus lizards from different
latitudes. Physiol. Zool. 61, 241–253.
Tullis, A., Baillie, M., 2005. The metabolic and biochemical responses of tropical
whitespotted bamboo shark Chiloscyllium plagiosum to alterations in environmen-
tal temperature. J. Fish Biol. 67, 950–968.
Watabe, S., 2002. Temperature plasticity of contractile proteins in fish muscle. J. Exp.
Biol. 205, 2231–2236.
Whittow, G.C., 1970. Comparative Physiology of Thermoregulation, vol. 1. Invertebrates
and Nonmammalian Vertebrates. Academic Press, New York.
Wilson, R.S., Franklin, C.E., Davison, W., Kraft, P., 2001. Stenotherms at sub-zero temper-
atures: thermal dependence of swimming performance in Antarctic fish. J. Comp.
Physiol. 171B, 263–269.
Wilson, R.S., Kuchel, L.J., Franklin, C.E., Davison, W., 2002. Turning up the heat on subzero
fish: thermal dependence of sustained swimming in an Antarctic notothenioid. J.
Therm. Biol. 27, 381–386.