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First published online August 9, 2007
Journal of Experimental Biology 210, 2932-2938 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.008391
Beneficial acclimation: sex specific thermal acclimation of metabolic capacity in the striped marsh frog (Limnodynastes peronii)
Integrative Physiology, School of Biological Sciences A08, The University of Sydney, NSW 2006, Australia
* Author for correspondence (e-mail: fseebach{at}bio.usyd.edu.au)
Accepted 4 June 2007
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Summary |
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Key words: temperature, reproduction, mitochondria, fitness, oxygen consumption, amphibia
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Introduction |
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). When
temperature decreases, enzyme-catalysed rate processes and diffusion rates
also decrease, thereby reducing the metabolic capacity of animals. Many
species are able to overcome this effect by increasing the amount or type of
metabolic enzymes expressed (Hochachka and
Somero, 2002), and by altering the composition of cellular
membranes to maintain the activity of membrane-bound enzymes
(Wodtke, 1981;
Guderley et al., 1997). These
molecular changes will affect metabolism at tissue and whole animal levels so
that physiological processes can proceed at a constant or near constant rate,
despite pronounced temperature fluctuations.
Thermal compensation of ATP production may be beneficial by increasing
components of fitness such as survival and reproductive success, and if
acclimation of metabolic capacity is beneficial it should increase the
relative fitness of the individual (Huey
et al., 1999; Seebacher and
Wilson, 2006). However, thermal acclimation of metabolism may also
represent a cost that is incurred by the energy required for increased rates
of transcription and translation
(Guderley, 2004), and by the
damage caused to membranes by the increase in reactive oxygen species
(Guderley and St-Pierre, 2002;
Brand et al., 2004). Hence,
acclimation may vary according to relative benefits and costs, and it would be
advantageous if acclimation occurred selectively in the tissues, pathways or
sex where it is most beneficial. Detection of acclimation will also depend on
choosing appropriate traits for investigation
(Kingsolver and Huey, 1998).
For example, resting oxygen consumption represents an energetic cost of living
(Hulbert and Else, 2000;
Clarke, 2003), and it may be
more beneficial for ectotherms to downregulate resting metabolic rates
(Seebacher, 2005). On the
other hand, it may be beneficial to upregulate the capacity of processes or
pathways that are linked to fitness, such as locomotor performance or ATP
production, as environmental temperatures decrease.
The reproductive processes and behaviour of anurans are energetically
demanding, particularly for males (Kaplan,
1987; Ryan, 1991;
Searcy and Andersson, 1986).
Calling by anurans is one of the most energetically demanding activities in
ectotherms (Schwartz et al.,
1995; Taigen and Wells,
1985; Walsberg et al.,
1986), and maintaining ATP-producing processes at reduced
temperatures is essential for reproductive success. Males call to attract
females, and to establish and mark territories. Rate, duration and intensity
of calling influence attractiveness to females
(Gerhardt et al., 2000;
Klump and Gerhardt, 1987;
Wells, 1977), with preference
for energetically demanding call characteristics such as high frequency and
volume (Arak, 1983;
Sullivan, 1983). Additionally,
males call to inhibit other males, and also engage in `wrestling' with
conspecifics to control calling sites and capture females already in amplexus
with males (Wells, 1977).
Temperature also influences the reproductive output of female frogs by its
influence on clutch and egg size, and the survival and growth of the offspring
(Kaplan, 1987;
Parichy and Kaplan, 1995). 80%
of total protein in amphibian eggs
(Wallace, 1985) consists of
vitellogenin that females produce in the liver.
The marsh frog Limnodynastes peronii is widespread in Australia,
ranging from tropical to temperate regions
(Cogger, 2000). Even in
temperate areas of New South Wales, reproductive activities occur for 9 months
in the year and males maintain their calling performance across pronounced
seasonal temperature fluctuations. Hence, the species is ideal for testing the
hypotheses that acclimation of metabolic capacity occurs in traits that are
linked to reproductive success, and that the response is different between the
sexes.
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Materials and methods |
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Measurement of resting metabolic rate
Resting metabolic rate (RMR) was measured by closed-system respirometry.
Frogs were fasted for 5 days before respirometry. Each frog was placed in a
respirometry container (550 ml) with 1 ml of water, and the chamber was
sealed. After 30 min, an oxygen sample was taken from the container using a
syringe with stopcock. The gas sample was drawn through Drierite® to
absorb moisture, and then Carbosorb® to absorb CO2, and again
through Drierite®. The oxygen concentration of the sample was determined
with an Amtek N-37M oxygen sensor attached to an Amtek S-3A/11 oxygen analyser
(Pittsburgh, PA, USA). Oxygen consumption rate of each frog was measured at
15°C and at 25°C in controlled temperature environments (4 h between
measurement at each temperature), and the order of test temperatures was
randomised for each individual. Resting metabolic rate (RMR) was calculated
according to Vleck (Vleck,
1987). To ensure that measurements reflected the resting metabolic
rate, respirometry trials were repeated 3-4 times for each individual (with 1
week between measurements) until animals reached a stable resting metabolic
rate (Iglesias et al.,
2003).
Tissue collection
After RMR measurements, animals were anaesthetised in a 0.5% solution of
MS222 (neutralised to pH 7), and euthanised by double pithing. Each animal was
weighed to 0.1 g, and snout-vent length was measured. The liver, gastrocnemius
muscle, extensor carpi radialis muscle and external oblique muscle were
dissected from the animal and frozen at -80°C. Additional samples of
liver, external oblique muscle and gastrocnemius muscle were collected to
isolate mitochondria. The remaining portion of each individual was weighed
again, and then dried at 60°C for 72 h, to provide an estimate of total
dry mass. We removed the eggs from gravid females to be weighed
separately.
Mitochondrial respiration
Tissue was homogenised in a glass homogeniser in 9 volumes of isolation
buffer (pH 7.3; 140 mmol l-1 KCl, 20 mmol l-1 Hepes, 10
mmol l-1 EDTA, 5 mmol l-1 MgCl2, 0.5% BSA).
The homogenate was centrifuged at 1400 g for 5 min, and the
supernatant was removed and centrifuged again at 9000 g for 7
min. The pellet was resuspended in assay buffer (10:1 buffer: initial tissue
mass, pH 7.3; 140 mmol l-1 KCl, 20 mmol l-1 Hepes, 5
mmol l-1 Na2HPO4, 0.5% BSA) to make up a
stock solution. The stock solution was further diluted by 9 volumes of assay
buffer for measurements of oxygen consumption in a temperature controlled
respiration chamber (Mitocell 200A, Strathkelvin, Scotland). Oxygen
consumption was measured with a microelectrode connected to an oxygen analyser
(model 1302, Strathkelvin). State 2 oxygen consumption rate was measured by
adding pyruvate (2.5 mmol l-1 final concentration), and malate (5
mmol l-1 final concentration) to spark the TCA cycle. Maximal
oxidation rate (state 3) was measured with the addition of ADP to the chamber
(3.8 mmol l-1 final concentration). The respiratory control ratio
(RCR) was calculated by the ratio of state 3 oxygen consumption to state 4
oxygen consumption when all ADP was consumed.
To determine protein concentration, 50 µl of mitochondrial solution was resuspended in 1 ml of BSA-free buffer, and centrifuged at 12000 g for 10 min. The pellet was retained and resuspended, and this process was repeated twice. The resulting solution was used to determine the protein concentration using the bicinchoninic acid method (Sigma, Sydney, Australia).
Enzyme assays
Tissue was homogenised in 99 volumes of extraction buffer (pH 7.5; 50 mmol
l-1 imidazole, 2 mmol l-1 MgSO4, 5 mmol
l-1 EDTA, 1 mmol l-1 glutathione, 0.1% Triton). The
homogenate was further diluted to 1:200 for lactate dehydrogenase (LDH)
assays. Enzyme activity was determined in a spectrophotometer (Ultrospec
2100pro, Amersham, Australia) with a temperature controlled cuvette holder.
Assays were conducted at 15°C and 25°C according to published methods
(Seebacher et al., 2003). All
chemicals were supplied by Sigma (Australia) and ICN Biochemicals (Australia),
and saturating substrate concentrations were determined before assays of
experimental tissues.
LDH activity (forward direction: pyruvate to lactate) was determined by monitoring the absorbance of NADH at 340 nm. This assay was completed in potassium phosphate buffer (pH 7.0) containing 0.16 mmol l-1 NADH and 0.4 mmol l-1 pyruvate. The activity for the reverse direction (lactate to pyruvate) was measured in a Tris buffer (pH 9.3) with 50 mmol l-1 lactate, 10 mmol l-1 NAD+, as the appearance of NADH at 340 nm.
Citrate synthase (CS) activity was monitored by the change in absorbance of 5,5'-dithio-bis(2-nitrobenzoic acid) (DTNB) at 512 nm, in Tris buffer (pH 8.0) containing 0.1 mmol l-1 DTNB, 0.1 mmol l-1 acetyl-CoA, and 0.15 mmol l-1 oxaloacetate (omitted for controls). Any activity detected in control assays was subtracted from the experimental assays.
Cytochrome c oxidase (CCO) activity was assayed by monitoring the change in absorbance of reduced cytochrome c (0.05 mmol l-1) in potassium phosphate buffer (pH 7.5) at 550 nm. Cytochrome was reduced by addition of sodium thiosulfate, and excess sodium thiosulfate was removed by bubbling with air.
ß-hydroxyacyl CoA dehydrogenase (HOAD) activity was assayed in imidazole buffer (50 mmol l-1 imidazole, 1 mmol l-1 EDTA, pH 8) containing 0.16 mmol l-1 NADH, 0.1 mmol l-1 aceto-acetyl-CoA, and 1 mmol l-1 KCN. The activity of HOAD was measured by the depletion of NADH at 340 nm.
Statistical analysis
Oxygen consumption was log10 transformed and analysed using a
repeated-measures analysis of covariance (RM-ANCOVA) with sex, test
temperature and acclimation treatment as factors, and dry mass
(log10 transformed) as a covariate. A power analysis was used to
estimate the probability of detecting a 20% difference between treatments, to
ensure that lack of differences between acclimation treatments is not due to
lack of statistical power. Mitochondrial respiration data were analysed in a
repeated-measures multivariate analysis of variance (RM-MANOVA) for each
respiration state, with acclimation group, sex and test temperature (repeated)
as factors. Respiratory control ratio was analysed in a RM-MANOVA, with
acclimation group, sex and test temperature (repeated) as factors. Enzyme data
were analysed with a RM-MANOVA for each enzyme, with acclimation group and
test temperature (repeated) as factors. Fisher's protected LSD (corrected by
sequential Bonferroni test) was used to separate the effects of acclimation
and sex from each MANOVA and ANCOVA. The proportion of egg mass to gravid
female mass was calculated as a proportion of total dry body mass (including
eggs). Assumptions of normality and homogeneity of variance were tested, and
log10 and square-root transformations were used to correct
non-normal data and differences in variance between groups, but
non-transformed data are shown. Significance was set at P<0.05,
where Bonferroni correction was applied, the original F value is
shown but P is corrected for multiple tests. Analyses were performed
in Genstat© (VSN International Ltd., Hemel Hempstead) or R© (R
Foundation for Statistical Computing, Vienna, Austria).
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The respiratory control ratio (RCR) differs significantly between acclimation groups in liver at both 15°C and 25°C, and in external oblique muscle at 15°C (Bonferroni-corrected LSD, P<0.05; Table 1). There is no change in RCR with acclimation in the gastrocnemius muscle at either 15°C or 25°C (Bonferroni-corrected LSD, P<0.05; Table 1).
Metabolic enzymes
In the gastrocnemius muscle, acclimation treatment does not have a
significant effect on enzyme activities, except for LDH where activity
(pyruvate
lactate) is greater in cold-acclimated than in warm-acclimated
frogs at 15°C (Bonferroni-corrected LSD, P<0.05;
Table 2). Similarly, enzyme
activities in liver are not affected by acclimation treatment, except that
cold-acclimated frogs have significantly greater CCO activity at 15°C,
than warm-acclimated frogs (Bonferroni-corrected LSD, P<0.05), but
there are no differences between sexes (Bonferroni-corrected LSD,
P>0.05; Table
2).
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In outer oblique (calling) muscle, cold-acclimated frogs have higher activity of CCO (F1,18=10.73, P<0.05), CS (F1,18=8.53, P<0.05), and HOAD (F1,18=11.99, P<0.01; Table 3). Additionally, sex has a significant effect on the activity of these enzymes (CCO: F1,18=12.42, P<0.05. CS: F1,18=7.87, P<0.05. HOAD: F1,18= 54.93, P<0.05), and there is an interaction between sex and acclimation groups (CCO: F1,9=13.13, P<0.05. CS: F1,9=11.59, P<0.05. HOAD: F1,9=20.88, P<0.01). Male frogs have significantly greater CCO and CS activities than females, and activity of these enzymes increases with cold acclimation in males (Bonferroni-corrected LSD, P<0.05). There is no difference in CCO or CS activity between cold- and warm-acclimated females (Bonferroni corrected LSD, P>0.05). Males have significantly higher HOAD activity than females (Bonferroni-corrected LSD, P<0.05), and there are significant differences between acclimation treatments in males (Bonferroni-corrected LSD, P<0.05). Thermal acclimation has no effect on the activity of HOAD in outer-oblique muscle in females (P>0.05).
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There is no effect of acclimation treatment on enzyme activity in the extensor carpi radialis muscle (Table 4), but there are differences between sexes in the activity of enzymes. Males have higher LDH activity than females for both pyruvate reduction (F1,18=9.54, P<0.05) and lactate oxidation (F1,18=34.78, P<0.05). Males also have significantly higher CS activity than females (F1,18=14.78, P<0.05).
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Egg mass
There is no significant difference in the percentage of body mass of
females comprising eggs between the two acclimation treatments (cold:
26.4±6.7%, warm: 22.3±2.0%; F1,6=1.04,
P>0.05).
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Discussion |
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; Martin and Gans,
1972), and male anurans often have higher activities of metabolic
enzymes in this muscle than females (Given
and McKay, 1990; Marsh and
Taigen, 1987). Additionally, citrate synthase activity is a
correlate of calling ability in Pseudacris crucifer
(Zimmitti, 1999). The calling
muscles are highly aerobic muscles that can contract repeatedly over long
periods (Marsh, 1999), so that
temperature compensation in oxidative pathways ensures the supply of ATP used
in muscular contraction. Upregulation of metabolic capacity of this muscle
maximises call volume and frequency, both of which are determinants of
reproductive success in male anurans (Arak,
1983; Klump and Gerhardt,
1987; Gerhardt et al.,
2000). The increases in aerobic metabolic enzyme activities in
males provide the capacity to maintain calling despite seasonally lowered
temperature. Female anurans prefer males whose calls reflect increased
energetic costs (Arak, 1983;
Sullivan, 1983), so that males
that do not undergo acclimation in the calling muscle may lose the opportunity
to mate when environmental temperature decreases. It seems likely that sex
hormones may regulate the difference in acclimation response between male and
females, given that testosterone increases muscle contractile abilities in
Hyla chrysoscelis (Girgenrath and
Marsh, 2003).
In contrast, there were no sex-specific differences in acclimation of state
3 oxygen consumption rate of mitochondria and enzyme activities in liver.
State 3 rates and LDH activities also increased in external oblique and
gastrocnemius muscles of females, respectively. Thermal acclimation of
metabolism in females will be advantageous to maintain ATP supply for
locomotion and growth of reproductive tissues in thermally variable
environments (Guderley and Johnston,
1996; St-Pierre et al.,
1998). Skeletal muscle has limited ability to store glycogen, and
stores of glycogen in muscle can limit activity
(Guppy, 1988). The liver is
essential in the synthesis and release of glucose to other parts of the body
(Bollen et al., 1998), and
upregulation of metabolic capacity in the liver may be important to support
calling, locomotion and growth. Gravid female L. peronii produce up
to 25% of dry body mass in eggs, and exposure to cold does not affect the egg
mass produced. The synthesis of vitellogenin represents an energetic cost that
can be met at lowered temperature by upregulating metabolic capacity in the
liver (Wallace, 1985), so that
thermal compensation of metabolism in females may have fitness benefits by
maintaining egg production in cooler environments.
Surprisingly, the activity of LDH increases in the gastrocnemius muscle
with cold acclimation, although Limnodynastes peronii shows no
acclimation of either burst swimming or jumping performance
(Wilson and Franklin, 2000),
both of which rely on force production by the gastrocnemius muscle. Animals
used in the current study were from the same population as those used by
Wilson and Franklin (Wilson and Franklin,
2000). Hence, L. peronii from the same population undergo
thermal acclimation of LDH activity in the gastrocnemius muscle, but not
acclimation of locomotor performance, which indicates that LDH activity is not
related to jumping and burst swimming performance.
The size (Kirby, 1983;
Yekta and Blackburn, 1992) and
contractile properties (Peters and Aulner,
2000) of extensor carpi radialis muscle of male anurans are
enhanced compared to females, and metabolic capacity (LDH and CS activity) of
extensor carpi muscle is higher in male L. peronii than in females.
This muscle is used in amplexus (Peters
and Aulner, 2000) and for bouts of `wrestling' between males
competing for mates or calling positions
(Clyne, 1967;
Schäuble, 2004). The
increased enzyme activity in this muscle in males is another specialisation of
muscle phenotype for sexual selection. One of the assumptions of previous
calculations of the energetic costs of amplexus is that anaerobic metabolic
pathways do not contribute to the energetics of amplexus
(James, 2003). However, the
difference between males and females in LDH activity means that glycolysis
does have a significant role in amplexus, although it may be important only
for male-male physical competition.
A single measurement of metabolism is unlikely to be adequate to test for
the occurrence of thermal acclimation, and measurements of resting oxygen
consumption may be particularly unsuited. Despite significant acclimation of
oxidative phosphorylation in mitochondria, and acclimation of several
metabolic enzymes, there was no change in resting oxygen consumption. Resting
oxygen consumption does not reflect metabolic capacity, but is a measure of
the `cost of living' incurred by the energetic cost of proton leak, protein
synthesis and Na+,K+-ATPase activity to maintain
membrane potentials (Hulbert and Else,
2000). Although there may be a correlation between resting oxygen
consumption and metabolic capacity (Gomes
et al., 2004), ideally selection should minimise the former while
maximising the latter. Hence, it is inappropriate to use resting oxygen
consumption as a measure of acclimation or adaptive response to environmental
change.
Acclimation of metabolic capacity will permit reproductive activity in
varying thermal environments, which allows ectotherms such as L.
peronii to extend their `fundamental' ecological niche
(Kearney and Porter, 2004)
both temporally and spatially. Hence, at least in L. peronii, the
capacity for reversible phenotypic plasticity should be viewed as a trait that
is under selection for the fitness benefits it confers. Additionally, the
potential for plasticity must be considered in models that attempt to predict
species' responses to climate change. Climate has never been stable during
evolutionary history so that selection would favour plastic rather than fixed
phenotypes, even in environments that are relatively stable at present
(Seebacher et al., 2005).
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Arak, A. (1983). Sexual selection by male male competition in natterjack toad choruses. Nature 306,261 -262.[CrossRef]
Bollen, M., Keppens, S. and Stalmans, W. (1998). Specific features of glycogen metabolism in the liver. Biochem. J. 336,19 -31.[Medline]
Brand, M. D., Affourtit, C., Esteves, T. C., Green, K., Lambert, A. J., Miwa, S., Pakay, J. L. and Parker, N. (2004). Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic. Biol. Med. 37,755 -767.[CrossRef][Medline]
Clarke, A. (2003). Costs and consequences of evolutionary temperature adaptation. Trends Ecol. Evol. 18,573 -581.[CrossRef]
Clyne, D. (1967). Australian Frogs. Melbourne: Periwinkle Books.
Cogger, H. G. (2000). Reptiles and Amphibians of Australia. Sydney: Reed New Holland.
Gerhardt, H. C., Tanner, S. D., Corrigan, C. M. and Walton, H.
C. (2000). Female preference functions based on call duration
in the gray tree frog (Hyla versicolor). Behav.
Ecol. 11,663
-669.
Girgenrath, M. and Marsh, R. L. (1997). In vivo performance of trunk muscles in tree frogs during calling. J. Exp. Biol. 200,3101 -3108.[Abstract]
Girgenrath, M. and Marsh, R. L. (2003). Season and testosterone affect contractile properties of fast calling muscles in the gray tree frog Hyla chrysoscelis. Am. J. Physiol. 284,R1513 -R1520.
Given, M. F. and McKay, D. M. (1990). Variation in citrate synthase activity in calling muscles of carpenter frogs, Rana virgatipes. Copeia 1990,863 -867.[CrossRef]
Gomes, F. R., Chaui-Berlinck, J. G., Bicudo, J. E. P. W. and Navas, C. A. (2004). Intraspecific relationships between resting and activity metabolism in anuran amphibians: influence of ecology and behavior. Physiol. Biochem. Zool. 77,197 -208.[CrossRef][Medline]
Guderley, H. (2004). Metabolic responses to low temperature in fish muscle. Biol. Rev. 79,409 -427.[Medline]
Guderley, H. and Johnston, I. A. (1996). Plasticity of fish muscle mitochondria with thermal acclimation. J. Exp. Biol. 199,1311 -1317.[Abstract]
Guderley, H. and St-Pierre, J. (2002). Going
with the flow or life in the fast lane: contrasting mitochondrial responses to
thermal change. J. Exp. Biol.
205,2237
-2249.
Guderley, H., Pierre, J. S., Couture, P. and Hulbert, A. J. (1997). Plasticity of the properties of mitochondria from rainbow trout red muscle with seasonal acclimatization. Fish Physiol. Biochem. 16,531 .[CrossRef]
Guppy, M. (1988). Limiting carbohydrate stores: alleviating the problem in the marathon runner, a hibernating lizard, and the neonate brain. Can. J. Zool. 66,1090 -1097.
Hochachka, P. W. and Somero, G. N. (2002). Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford: Oxford University Press.
Huey, R. B., Berrigan, D., Gilchrist, G. W. and Herron, J. C. (1999). Testing the adaptive significance of acclimation: a strong inference approach. Am. Zool. 39,323 -338.
Hulbert, A. J. and Else, P. L. (2000). Mechanisms underlying the cost of living in animals. Annu. Rev. Physiol. 62,207 -235.[CrossRef][Medline]
Iglesias, S., Thompson, M. B. and Seebacher, F. (2003). Energetic cost of a meal in a frequent feeding lizard. Comp. Biochem. Physiol. 135A,377 -382.
James, D. M. (2003). The metabolic cost of amplexus in the grey tree frog (Hyla versicolor): assessing the energetics of male mating success. Can. J. Zool. 81, 388.
Kaplan, R. H. (1987). Developmental plasticity and maternal effects of reproductive characteristics in the frog, Bombina orientalis. Oecologia 71,273 .[CrossRef]
Kearney, M. and Porter, W. P. (2004). Mapping the fundamental niche: physiology, climate, and the distribution of a nocturnal lizard. Ecology 85,3119 -3131.[CrossRef]
Kingsolver, J. G. and Huey, R. B. (1998). Evolutionary analyses of morphological and physiological plasticity in thermally variable environments. Am. Zool. 38,545 -560.
Kirby, A. C. (1983). Physiology of the sternoradialis muscle: sexual dimorphism and role in amplexus in the leopard frog (Rana pipiens). Comp. Biochem. Physiol. 74A,705 -709.[Medline]
Klump, G. M. and Gerhardt, H. C. (1987). Use of non-arbitrary acoustic criteria in mate choice by female gray tree frogs. Nature 326,286 .[CrossRef]
Marsh, R. L. (1999). Contractile properties of muscles used in sound production and locomotion in two species of gray tree frog. J. Exp. Biol. 202,3215 -3223.[Abstract]
Marsh, R. L. and Taigen, T. L. (1987). Properties enhancing aerobic capacity of calling muscles in gray tree frogs Hyla versicolor. Am. J. Physiol. 252,R786 -R793.[Medline]
Martin, W. F. and Gans, C. (1972). Muscular control of the vocal tract during release signaling in the toad Bufo valliceps. J. Morphol. 137,1 -28.[CrossRef][Medline]
Parichy, D. M. and Kaplan, R. H. (1995). Maternal investment and developmental plasticity: functional consequences for locomotor performance of hatchling frog larvae. Funct. Ecol. 9,606 -617.[CrossRef]
Peters, S. E. and Aulner, D. A. (2000). Sexual dimorphism in forelimb muscles of the bullfrog, Rana catesbeiana: a functional analysis of isometric contractile properties. J. Exp. Biol. 203,3639 -3654.[Abstract]
Ryan, M. J. (1991). Sexual selection and communication in frogs. Trends Ecol. Evol. 6, 351.[CrossRef]
Schäuble, C. S. (2004). Variation in body size and sexual dimorphism across geographical and environmental space in the frogs Limnodynates tasmaniensis and L. peronii. Biol. J. Linn. Soc. Lond. 82,39 -56.[CrossRef]
Schwartz, J. J., Ressel, S. J. and Bevier, C. R. (1995). Carbohydrate and calling: depletion of muscle glycogen and the chorusing dynamics of the neotropical treefrog Hyla microcephala.Behav. Ecol. Sociobiol. 37,125 .[Medline]
Searcy, W. A. and Andersson, M. (1986). Sexual selection and the evolution of song. Annu. Rev. Ecol. Syst. 17,507 -533.[CrossRef]
Seebacher, F. (2005). A review of thermoregulation and physiological performance in reptiles: what is the role of phenotypic flexibility? J. Comp. Physiol. B 175,453 -461.[CrossRef][Medline]
Seebacher, F. and Wilson, R. S. (2006). Fighting fit: thermal plasticity of metabolic function and fighting success in the crayfish Cherax destructor. Funct. Ecol. 20,1045 -1053.[CrossRef]
Seebacher, F., Guderley, H., Elsey, R. M. and Trosclair, P. L.,
III (2003). Seasonal acclimatisation of muscle metabolic
enzymes in a reptile (Alligator mississippiensis). J. Exp.
Biol. 206,1193
-2000.
Seebacher, F., Davison, W., Lowe, C. J. and Franklin, C. E. (2005). A falsification of the thermal specialization paradigm: compensation for elevated temperatures in Antarctic fishes. Biol. Lett. 1,151 -154.[CrossRef][Medline]
Somero, G. N. (1997). Temperature relationships: from molecules to biogeography. In Handbook of Physiology. Vol. 2 (ed. W. H. Dantzler), pp. 1391-1444. Oxford: Oxford University Press.
St-Pierre, J., Charest, P. and Guderley, H. (1998). Relative contribution of quantitative and qualitative changes in mitochondria to metabolic compensation during seasonal acclimatisation of rainbow trout Oncorhynchus mykiss. J. Exp. Biol. 201,2961 -2970.[Abstract]
Sullivan, B. K. (1983). Sexual selection in the great plains toad (Bufo cognatus). Behaviour 84,258 -264.
Taigen, T. and Wells, K. (1985). Energetics of vocalization by an anuran amphibian Hyla versicolor. J. Comp. Physiol. B 155,163 .[CrossRef]
Vleck, D. (1987). Measurement of O2
consumption, CO2 production, and water vapor production in a closed
system. J. Appl. Physiol.
62,2103
-2106.
Wallace, R. A. (1985). Vitellogenesis and oocyte growth in non-mammalian vertebrates. Dev. Biol. N. Y. 1,127 -177.
Walsberg, G. E., Lea, M. S. and Hillman, S. S. (1986). Individual variation in maximum aerobic capacity: cardiovascular and enzymatic correlates in Rana catesbeiana. J. Exp. Zool. 239,1 -5.[CrossRef][Medline]
Wells, K. D. (1977). Social-behavior of anuran amphibians. Anim. Behav. 25,666 -693.[CrossRef]
Wilson, R. S. and Franklin, C. E. (2000). Inability of adult Limnodynastes peronii (Amphibia: Anura) to thermally acclimate locomotor performance. Comp. Biochem. Physiol. 127A,21 -28.[CrossRef][Medline]
Wodtke, E. (1981). Temperature adaptation of biological membranes. Compensation of the molar activity of cytochrome c oxidase in the mitochondrial energy-transducing membrane during thermal acclimation of the carp (Cyprinus carpio L.). Biochim. Biophys. Acta 640,710 -720.[Medline]
Yekta, N. and Blackburn, D. (1992). Sexual dimorphism in mass and protein content of the forelimb muscles of the northern leopard frog Rana pipiens. Can. J. Zool. 70,670 -674.
Zimmitti, S. J. (1999). Individual variation in morphological, physiological, and biochemical features associated with calling in spring peepers (Pseudacris crucifer). Physiol. Biochem. Zool. 72,666 -676.[CrossRef][Medline]
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