Thermal independence of muscle tissue metabolism in the leatherback turtle, Dermochelys coriacea.
ABSTRACT Metabolic rates of animal tissues typically increase with increasing temperature and thermoregulatory control in an animal is a regional or whole body process. Here we report that metabolic rates of isolated leatherback turtle (Dermochelys coriacea) pectoralis muscle are independent of temperature from 5-38 degrees C (Q10 = 1). Conversely, metabolic rates of green turtle (Chelonia mydas) pectoralis muscle exhibit a typical vertebrate response and increase with increasing temperature (Q10 = 1.3-3.0). Leatherbacks traverse oceanic waters with dramatic temperature differences during their migrations from sub-polar to equatorial regions. The metabolic stability of leatherback muscle effectively uncouples resting muscle metabolism from thermal constraints typical of other vertebrate tissues. Unique muscle physiology of leatherbacks has important implications for understanding vertebrate muscle function, and is another strong argument for preservation of this endangered species.
- SourceAvailable from: Diogo Cardoso[Show abstract] [Hide abstract]
ABSTRACT: Many studies on risk assessment of pesticides on non-target organisms have been performed based on standardized protocols that reflect conditions in temperate climates. However, the responses of organisms to chemical compounds may differ according to latitude and thus predicting the toxicity of chemicals at different temperatures is an important factor to consider in risk assessment. The toxic effects of the pesticide carbaryl were evaluated at different temperature regimes, which are indicative of temperate and tropical climates and are relevant to climate change predictions or seasonal temperature fluctuations. Four standard organisms were used (Folsomia candida, Eisenia andrei; Triticum aestivum and Brassica rapa) and the effects were assessed using synergistic ratios, calculated from EC/LC50 values. When possible, the MIXTOX tool was used based on the reference model of independent action (IA) and possible deviations. A decrease on carbaryl toxicity at higher temperatures was found in F. candida reproduction, but when the mixtox tool was used no interactions between these stressors (Independent Action) was observed, so an additive response was suggested. Synergistic ratios showed a tendency to synergism at high temperatures for E. andrei and B. rapa and antagonism at low temperatures for both species. T. aestivum showed to be less affected than expected (antagonism), when exposed to both low and high temperatures. The results showed that temperature may increase the deleterious effects of carbaryl to non-target organisms, which is important considering both seasonal and latitude related differences, as well as the global climate change context.Ecotoxicology and Environmental Safety 05/2014; · 2.48 Impact Factor
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ABSTRACT: A common, long-held belief is that metabolic rate drives the rates of various biological, ecological and evolutionary processes. Although this metabolic pacemaker view (as assumed by the recent, influential 'metabolic theory of ecology') may be true in at least some situations (e.g. those involving moderate temperature effects or physiological processes closely linked to metabolism, such as heartbeat and breathing rate), it suffers from several major limitations, including: (i) it is supported chiefly by indirect, correlational evidence (e.g. similarities between the body-size and temperature scaling of metabolic rate and that of other biological processes, which are not always observed) - direct, mechanistic or experimental support is scarce and much needed; (ii) it is contradicted by abundant evidence showing that various intrinsic and extrinsic factors (e.g. hormonal action and temperature changes) can dissociate the rates of metabolism, growth, development and other biological processes; (iii) there are many examples where metabolic rate appears to respond to, rather than drive the rates of various other biological processes (e.g. ontogenetic growth, food intake and locomotor activity); (iv) there are additional examples where metabolic rate appears to be unrelated to the rate of a biological process (e.g. ageing, circadian rhythms, and molecular evolution); and (v) the theoretical foundation for the metabolic pacemaker view focuses only on the energetic control of biological processes, while ignoring the importance of informational control, as mediated by various genetic, cellular, and neuroendocrine regulatory systems. I argue that a comprehensive understanding of the pace of life must include how biological activities depend on both energy and information and their environmentally sensitive interaction. This conclusion is supported by extensive evidence showing that hormones and other regulatory factors and signalling systems coordinate the processes of growth, metabolism and food intake in adaptive ways that are responsive to an organism's internal and external conditions. Metabolic rate does not merely dictate growth rate, but is coadjusted with it. Energy and information use are intimately intertwined in living systems: biological signalling pathways both control and respond to the energetic state of an organism. This review also reveals that we have much to learn about the temporal structure of the pace of life. Are its component processes highly integrated and synchronized, or are they loosely connected and often discordant? And what causes the level of coordination that we see? These questions are of great theoretical and practical importance.Biological reviews of the Cambridge Philosophical Society 05/2014; · 6.63 Impact Factor
- Marine Ecology Progress Series 01/2002; 230:289-293. · 2.64 Impact Factor
,. I’ :1’ ..
Comparative Biochemistry and Physiology Part A 120 (1998) 399-403
Thermal independence of muscle tissue metabolism in the leatherback
g turtle, Dermochelys coriacea
David N. Peniclt ‘-"', James R. Spotila ‘, Michael P. O’Connor ", Anthony C. Steyermark “, .
Robert H. George ", Christopher J. Salice “, Frank V. Paladino °
- Department of Bioscience and Biotechnology, Drexcl University, Philadelphia. PA r9104, USA
" Virginia Institute. of Marine Science, Gloucxster Point. VA 23062, USA
‘Department of Biological Sciences, Purdue University, Fort Wayne. IN 46805, USA
Received 29 May 1997; accepted 20 January 1998
Metabolic rates of animal tissues typically increase with increasing temperature andthermoregulatory con-trol in an animal is . U
a regional or whole body process. Here we report that metabolic rates-of isolated leatherback ‘turtle (Dermochelys coriacea)
pectoralis muscle are independent of temperature from 5-38°C (Q0 2 1). Conversely, metabolic rates of green turtle (Chelonia
mydas) pectoralis muscle exhibit a typical vertebrate response and increase with increasing temperature (Q,,,= 1.3-3.0).
Leatherbacks traverse oceanic waters with dramatic temperature differences during their migrations from sub-polar, to equatorial
regions. The metabolic stability of leatherbaclc muscle effectively uncouples resting muscle metabolism from thermal constraints V
typical of other vertebrate tissues. Unique muscle physiology of leatherbaclrs has important implications for understanding
vertebrate muscle function, and is another strong argument for preservation of this endangered species. 0 1998 Elsevier Science
Inc. All rights reserved. ‘
Keywords: Orelania mydas; Dermochelys coriacea; Endangered species; Muscle; Sea turtle; Temperature; Thermal compensation;
Tissue metabolism :
Metabolic rates are among many physiological and
ecological processes. in reptiles that are temperature
dependent [14,15,8,26,37]. The importance of this ther-
mal dependence of physiological function is demon-
strated by the widespread occurrence of behavioral
thermoregulation among reptiles . Regulation of
body temperature may have evolved primarily as a
means of controlling rate functions in animals [7,2,5].
Other adaptations, including brain heater organs in
billﬁsh , regional endothermy in tunas,‘ sharks and
‘ Corresponding author. Present address: Department of Ecology
. and Evolutionary Biology, University of Connecticut, Storrs, CI‘
06259, USA. Tel: +1 860 4860811; fax: +1 860 486020; e-mail:
1095-6433/98/Sl9.00 O 1998 Elsevier Science Inc. All rights reserved.
turtles [3l,32,4], and countercurrent heat exchangers
 and gigantothermy in leatherback turtles (Der-
mochelys coriacea) , increase the ability of aquatic
vertebrates to function in cold water. Knowledge of the
physiological bases that underlie these adjustments is
fundamental to understanding the overall responses of
these organisms to‘ ﬂuctuating thermal environments
Leatherback turtles are among the largest living rep-
tiles, adults ranging in size from 250 to 900 kg [10,29].
They are pelagic, traverse ranges of latitudes greater
than any other reptile, and inhabit waters of 0-30°C
[3,35]. In cold water, they maintain elevated body tem-
peratures (Tb) (25.5°C in 75°C seawater, ), yet in
the tropics have Tb only l~3°C above ocean tempera-
ture [~18]. Metabolic rates of adults at rest (0.387 W
400 ' " " ' D.N. Perrldc e!_aI./Comparative Br'odIanLrtry and Physiology, Part A I20 (1998) 399-403
- kg-.1 an_d.whﬂe as... (1.227 w k,;-*) are intermedi-
ate to thosepredicted by allometric relationships for
reptiles and mammals . These data and mathemati-
cal models indicate that they can use large body size,
circulatory changes, and peripheral insulation to main-
tain warm body temperatures -in frigid waters and to
avoid overheatingin tropical waters. In a preliminary
experiment we lowered the body temperature of two
- adult leatherbacks 5°C with no reduction in resting
metabolic rate (unpublished data). This suggests that
there may be some thermal independence in metabolic
rate of this species. ‘
The objective of this study was to determine the
extent to which the metabolic rates of muscle tissue
were affected by temperature in this animal.
We measured tissue metabolic rates of excised "pec-
toralis muscles from nine leatherback turtles (mass,
280-380 kg) nesting on Plays Langosta, Costa Rica.
We compared these data to metabolic rates of muscle
tissue from ll subadult green turtles (Chelonia mydas)
(mass, 20-30 kg) at the.Cayman Island Turtle Farm,
and to metabolic rates of muscle tissue from three
lizards (Clenosaunzs similis) and two marine toads
(Bufo marinas) tested simultaneously with leatherback
tissues in Costa Rica as controls. We removed
leatherback samples by surgical biopsy and obtained
green turtle samples from ‘farm-reared animals upon
their harvest . We removed muscle tissues from
lizards and toads after sacriﬁce by decapitation. Upon
removal, we placed samples in sterile ice cold, physio-
logic saline (0.9% pH 7.2) with 10 mM glucose added as
an energy substrate. We used sealed sterile saline be-
cause of concerns of bacterial contamination, and for
consistency under uncertain field conditions in the _trop—
ics. We prepared triplicate’ samples on ice and kept
them moist with-saline solution. We quickly trimmed
samples of fascia and vascular tissue, and blotted them
dry before weighing them to ;]:0.5 mg. We teased
samples apart longitudinally, cut them into .1 ~2 mm
long sections, and suspended them in the saline solution
[l1,33,l'7]. We then -placed samples (1 i 0.05 g) into 15
ml respirometry ﬂasks, brought preparation volumes to
3 ml, and immersed ﬂasks in a temperature controlled
water bath (i 0.5°C). We determined metabolic rate by
measuring 02 uptake at 10.20, and 30 min after a 15
min equilibration period at each temperature.
We measured oxygen consumption? in a Gilson Dif-
ferential Respirorneter using standard ‘techniques .
Three subsamples prepared for each tissue sample were
run independently. We used mean metabolic rate for
the three subsamples as the metabolic rate for each
a individual at each temperature (5, 12.5, 20, 27.5, 35, 38
and 40°C). The original temperature protocol‘ was from
S—35°C; the 38 and 40°C temperatures were added
when the '5—35°C trials revealed no signiﬁcant differ-
ence. This shift in temperature protocol for leatherback
samples was reflected in a decreased sample size at
higher temperatures (Fig. 1). Cautionmust be applied
when measuring metabolic rates of excised muscle tis-
‘sue. Ideally we should have measured the metabolic
rate of a whole muscle preparation since teasing apart
the muscle disrupts the cells (, p. 141). However, it
was not practical to measure the metabolism of an
entire pectoralis muscle of a leatherback turtle because
it may weigh as much as 25 kg, limiting diffusion of
nutrients, oxygen and carbon dioxide, and removal of
the entire muscle ‘would be lethal. Since this species is
endangered, this approach was ethically not acceptable.
A similar technique was used by West et al.  to
study in‘ vitro glucose uptake in trout (Oncorhynchus
mykiss) skeletal muscle, by Oikawa and Itazawa [22,23]
to measure the in vitro metabolic rate of muscle tissue
from ﬁsh, and by Penick et al.  to study tissue
metabolism of green turtles. Schmidt-Nielsen  and
Burggren and Roberts  discuss the value of this type
of data on muscle metabolism in their discussions of
scaling and the relationship between metabolism and
body size. While the results reported here may not.
represent the truesresting metabolic rates of muscle in
vivo, they do provide a valid indicator of the relative
metabolic response to temperature of muscles from the
species tested. . -
‘ Given the limitations of this technique, we also com-
pleted several experiments to reduce the error in these
experiments. These controls showed that: (1) There was
no signiﬁcant difference in tissue metabolic rates if
temperature order was randomized (n = 4), or returned
0 10 20 30 40
Fig. 1. Oxygen consumption of pectoralis muscle from green (,1 .~. 11
except at 35°C where 11:4) and leatherback turtles (n=9 from
5—27.5°C. l1==4 at 35°C and n=5 at 38 and 40°C). Error bars
represent 131 SE.
mv. muck er al. /Canlplaratloe Biochernirlry and Physiology, Part A 120 (1993) 399-4433 401
to starting position after -completion of all temperatures
(n=5). This control indicated that while there may
have been some disruption of cellular integrity, the
muscle was still viable;.(2)' There was no difference in
metabolic rate of tissue that were > l0 h old. This
control indicated that tissues remained viable for a time
greater than thatnequired for the experimental proto-
col; (3) There was no difference in metabolic rate when
a turtle Ringer’s solution» (100 mM NaCl, 4 mM KC],
10 mM NaHCO,, 5 mM Nazi-IP04, 2 mM Nal-11014,
0.75 mM CaCl,_ 10 mM ‘glucose and 30 mEq Na
HEPES Buffer) was used instead of the glucose and
saline solution. This indicated that the saline solution
was a sufficient medium for this experiment; (4) There
was no signiﬁcant difference in pH of saline solution
over the course of the run; (-5) There was no difference
in tissue, metabolic rate when lidocaine was used prior
to excising tissues; (6) There was no difference between
expected and observed patterns of metabolic rates of
toad, Bufo marinas, thigh muscle and lizard, Ctenosau-
rus similis, quadriceps musclemeasured simultaneously
with and by identical techniques as the leatherback
We found signiﬁcant differences (P=0.05) in tissue
metabolic rates of green turtle and leatherback muscle
using repeated measures analysis of variance
3. Results A
We found that temperature signiﬁcantly affected
metabolism of subadult green turtle muscle (repeated
measures ANOVA, F = 226, P < 0.0001 for 11 individ-
uals at 5—27.5°C) with values of 30.1 pl 02 g“' h"
(wet mass) at 5°C to 119.5 [1102 g" h" at 35°C (Fig.
1). Metabolic rates were similar at 27.5 and 35°C.
Thermal dependence of tissue metabolism, computed as
Q“, was 2.97 from 5—l2.5°C, 1.56 from l2.5—20°C,
1.31 from 20—27.5’C, and 1.00 from 27.5—35°C. Con-
versely, metabolic rates of leatherback pectoralis muscle
were completely insensitive to temperature from 5-
35°C (57.0—60.S pl 02 g" h"), became variable at
38°C (Qm = 1 from 5—38°C) and decreased signiﬁcantly
at 40°C (33.9 pl 0, .g-'1 11°‘). Metabolic rates of thigh
muscles from the toad, -Bufo marinas, and quadriceps
muscles from the lizard, Ctcnosaurus similis, "used as
controls and measured simultaneously with leatherback
samples, responded as expected‘ for vertebrate tissue
with metabolic rates increasing from‘94 pl 0, g‘ ‘ _h“‘
at 5°C to 145 pl 0, g“ h" at 25°C for the‘ toad and
from 27.5 p10, g”‘ hr? at 5°C to 74.7 pl 0; g"‘ h"
. at 35s@ for the lizard [n¢2 and 3, respectively).
Metabolic rate of leatherback pectoralis muscle’ was
higher than that of green turtle muscle at 5?’C', similar
at 12.5°C,'and lower at higher temperatures,
Untilhnow, temperature dependence of vertebrate
tissue metabolism (0, consumption) over a broadrange
of temperatures was almost universal, and a basic
paradigm of comparative physiology [27,28,7]. Temper-
ature independence of leatherback pectoralis muscle
metabolism is a rare example of perfect metabolic
compensation of tissue metabolic rate over the range of
environmental temperatures experienced by a verte-
brate. Temperature dependence of green turtle pec-
toralis muscle using identical protocols, and Bufo and
Ctenosaurus muscles. using identical test conditions and
run concurrently with leatherback tissues is persuasive
that this phenomenon is real and not a procedural
artefaot. In addition, our extensive controls also sup-
port this conclusion.
Data on other reptiles indicate that their muscle
tissues exhibit temperature dependent metabolic rates in
vitro like those of green turtles, ‘ctenosaurs and marine
toads. I-Ioskins and Alelcsiuk  report the inﬂuence of
temperature (4—34°C), photoperiod and season on oxy-
gen consumption of several different tissues of the
garter snake, Thamnophis sirtalis. There are signiﬁcant
changes in Q“, with temperature and season, with Q“,
values of g:6.5 at low temperatures (4-20°C) and z 2
at_ higher temperatures (20~34°C). This compares with ~
a Q“, of‘2.97 for’5-l2.5°C, 1.56 for 12.5-20°C, 1.31
for 20-27.5°C and l.0 for 27.5—35°C for the green
turtle and a Q", of l.0 for 5—35°C in leatherback turtle
muscle. Morris  reports metabolic-rates for eight
tissues, including muscle of the eurythermic lizard Leia-
plopisma zelandica, from 5—40°C. The Q“, values range
from 2 to 4, indicating a greater thermal dependence
than we measured in green turtle muscle.
Fish tissues generally exhibit temperature dependent
metabolic rates in vitro . However, skipjack tuna
(Katsuwonus pelamis) white muscle in vitro has a con-
stant oxidative metabolism from 5—25°C which in-
creases from 25 to 35°C. Tuna’ red muscle has a very
high metabolic rate which increases dramatically from 5
to 25°C, and is temperature independent from 25 to
35°C. However, this apparent temperature indepen-
dence of tuna muscle is difficult to interpret because of
relatively high variability in metabolic rates and low
sample size [ll].
Standard metabolic rates of some marine inverte-
brates (e.g. sea anemone Actinia, crustacean Nephrops,
snail Littorina, and clam Cardium) are very low, and
relatively independent of temperature over their daily
temperature range, but are thennally sensitive at more
extreme temperatures [l-9-21]. This adaptation allows
muscle operation over changing temperatures without
5 changes in muscle function [l9—2l].
The potential ecological signiﬁcance of this metabolic
phenomenon is illustrated by comparing the natural
402 D.N. Penick er al. Comparative ﬂiodravsértry and Phyﬂobgy, Part A 120 (1998) 399-403
history of leatherbaeks and green turtles. Leatherbacks
are largely .pelagic and frequently occur in extreme,
sub—polar waters. Green turtles inhabit warm, shallow
coastal waters and maintain body temperatures l—3°C
warmer than water temperature . Temperature sen-
sitivity of green turtle muscle tissue may explain their
tropical and sub-tropical distribution. It may also be
responsible for their susceptibility to cold stunning, a
winter phenomenon in which they lose the ability to
swim and dive when exposed to cold water [36,25]. The
metabolic stability of resting leatherback muscle may
facilitate? survival in both cold and warm water, allow-
ing use of a broad thermal niche, not only by adapta-
tions for heat retention [24,4,9], but also by direct
regulation of tissue metabolism, such that pectoralis
muscle functions independently of its thermal
Additional experiments are needed to elucidate the
functional signiﬁcance of this ﬁnding and its molecular
mechanisms. Key rate limiting enzymes in metabolic
pathways need to be assessed with regard to tempera-
ture, K,,,, V,,,_,,, enzyme-substrate affinity, andnumber
of isozymes. Molecular studies are also needed on gene
regulation involved in this system.
We thank the ‘following for technical assistance: M.
Boza, M.T. Koberg, P. Patillo, R. Arauz, R. Byles, J.
and F. Wood, G. Serrano, G. Marin, V. Lance, I.
Naranjo-Arauz, A. List, and our EARTHWATCH and
Drexel volunteers. Protocols were approved by animal
care committees of Drexel and Purdue Universities.
Research supported by NSF (DCB-9019780), National
Geographic Society, EARTHWATCH, and by the Betz
Chair endowment of Drexel University. '
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