Effects of temperature, epinephrine and Ca2+ on the hearts of yellowfin tuna (Thunnus albacares)
1 Tuna Research and Conservation Center, Stanford University, Hopkins Marine
Station, Oceanview Boulevard, Pacific Grove, CA 93950, USA
2 Comparative Physiology and Anatomy, Institute of Veterinary, Animal and
Biomedical Sciences, Massey University, New Zealand
* Author for correspondence (e-mail: bblock{at}stanford.edu )
Accepted 10 April 2002
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Summary |
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Key words: temperature, epinephrine, Ca2+, cardiac function, heart, yellowfin tuna, Thunnus albacares
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Introduction |
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While the oxidative slow-twitch muscle, viscera, brain and eyes are warmed
by conservation of metabolic heat with retia mirabilia
(Carey and Teal, 1969;
Linthicum and Carey, 1972
),
the coronary circulation receives blood directly from the gills to supply the
myocardium and must be at ambient temperature. Temperatures in the lumen of
the heart are determined by the efficiency and control of heat exchange in the
retia and are assumed to approach ambient water temperatures
(Carey et al., 1984
). No
measurements of myocardial temperatures in free-swimming fish have been made.
Electronic tagging studies indicate that bluefin, bigeye (Thunnus
obesus) and yellowfin (Thunnus albacares) tuna range into
surface waters as warm as 25-30 °C. Bluefin and bigeye tuna experience
waters between 2 and 30 °C during annual migrations and dives below the
thermocline (Carey and Lawson,
1973
; Block et al.,
1998
; Brill et al.,
1999
; Gunn and Block,
2001
; Marcinek et al.,
2001
). In contrast, yellowfin are primarily restricted to surface
water temperatures that range from 17 to 30 °C, despite occasional brief
dives to temperatures as low as 11 °C
(Block et al., 1997
). During
the prolonged dives of Atlantic bluefin, the heart is exposed to low ambient
temperatures for 12h or more while internal visceral temperatures remain at
20-25 °C or higher (Block et al.,
2001
). Bluefin have been recorded in surface temperatures of 8-12
°C for weeks at high latitudes (Block
et al., 2001
). The heart must pump blood in support of the high
metabolic rate of the bluefin's endothermic tissues while operating across
this wide range of ambient temperatures. This raises the possibility that
cardiac performance limits thermal niche utilization
(Korsmeyer et al., 1996
;
Brill et al., 1999
;
Marcinek, 2000
;
Brill and Bushnell, 2001
).
While cold surface waters and deep dives impose serious challenges on the
heart's capacity to supply oxygen to a warm body, the metabolic demands of
giant tuna on the warm temperate and tropical breeding grounds may impose the
most strenuous challenges for the cardiovascular system. Recent archival
tagging data indicate that bluefin internal temperatures exceed 29 °C in
the Gulf of Mexico breeding ground (Block
et al., 2001
).
How the hearts of tuna maintain function across this wide range of ambient
temperatures remains unknown. Studies of cardiac muscle strips in yellowfin
tuna indicate that peak force increases as temperature drops from 25 to 20
°C; however, optimal and peak frequencies decrease with falling
temperature, lowering overall power output
(Freund, 1999). Shiels et al.
(1999
) reported a drop in peak
force produced by yellowfin atrial strips as temperature increased from 15 to
25 °C. Korsmeyer et al.
(1997a
) measured relative
changes in cardiovascular parameters of swimming yellowfin tuna at
temperatures ranging from 18 to 28 °C, and found that an increase in
stroke volume accompanied a decrease in heart rate as temperature was reduced,
resulting in a net drop in cardiac output. Thus, taken together, the cardiac
strip and whole-animal performance experiments indicate that, as the
temperature drops, heart rate falls and the stroke volume of the tuna heart
increases.
To measure the effects of temperature on yellowfin tuna hearts, this study
used an in situ perfused preparation exposed to a range of
temperatures that yellowfin may experience in the wild (10-25 °C). In
situ perfused heart preparations have been used successfully to study
cardiac performance in a variety of fish species (Farrell et al.,
1985,
1989
;
Farrell, 1987
). In perfused
rainbow trout (Oncorhynchus mykiss) hearts, power production in the
isolated preparation can match the maximum power production achieved in
vivo (Milligan and Farrell,
1991
). However, only one study has applied this technique to tuna,
producing values of cardiac output similar to those determined in spinally
blocked fish at 25 °C (Farrell et al.,
1992
). By using this preparation on fish of 2.5-3.8 kg, we provide
data on cardiac performance parameters over a wide range of temperatures.
Many factors affect cardiac cell function and can influence cardiac
performance in vivo. Ca2+, epinephrine and temperature are
all known to play a role in modulating cardiac performance. Influx of
extracellular Ca2+ is essential for direct activation of the
myofibrils and for Ca2+-induced Ca2+ release from the
sarcoplasmic reticulum (Fabiato,
1983). Previous perfused heart preparations in yellowfin and
skipjack tuna have employed Ringer's solutions containing 1.9
mmoll-1 Ca2+; however, the blood Ca2+
concentration in skipjack tuna (Katsuwonis pelamis) has been reported
to be as high as 7.6 mmoll-1
(Sather and Rogers, 1967
).
Blood Ca2+ concentrations measured in captive yellowfin tuna vary
with handling and sampling methods, ranging from 3.2 mmoll-1 in
relatively undisturbed fish to 3.4 mmoll-1 in net-captured fish (S.
Fletcher, T. Williams and B. A. Block, unpublished data). Blood
Ca2+ concentrations of 4.7 mmoll-1 have been recorded in
wild bluefin tuna caught by hook and line
(Cooper et al., 1994
). Thus,
low Ca2+ concentrations may have depressed performance in previous
perfused heart preparations in tuna.
Several studies of tuna cardiac function have used spinally blocked fish
(Brill, 1987;
Bushnell et al., 1990
;
Bushnell and Brill, 1992
;
Jones et al., 1993
;
Lai et al., 1987
;
Brill et al., 1998
), which may
have resulted in high levels of circulating epinephrine during the experiment.
Epinephrine influences cardiac contractility by increasing the open
probability of L-type Ca2+ channels, thus increasing
Ca2+ influx into the myocytes
(Reuter et al., 1986
).
Blockade of adrenergic receptors produces small (6 %) decreases in heart rate
and ventral aortic pressure in skipjack and yellowfin, suggesting that resting
levels of epinephrine have little effect on the performance of tuna heart
(Keen et al., 1995
). However,
experiments on isolated atrial strips from skipjack tuna indicate that
contractile force can increase up to twofold with increasing epinephrine
concentrations up to 10-5 moll-1
(Keen et al., 1992
).
In the present study, we investigate the temperature-dependence of heart rate, stroke volume, cardiac output and myocardial power output of yellowfin tuna hearts in situ. In addition, we measure the response of these cardiac parameters to variation in Ca2+ and epinephrine concentrations. Together, these data indicate the scope of cardiac performance in yellowfin tuna over a range of conditions likely to be encountered in the wild.
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Materials and methods |
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Fish handling and surgery
Fish were captured in a nylon sling, transported out of the tank in an
envelope of sea water and killed by pithing. In some preparations, the spinal
cord was ablated by insertion of a 25 cm piece of 120 kg test monofilament to
eliminate postmortem swimming motions. Surgical procedures were
similar to those of Farrell et al.
(1992). The dorsal hepatic
vein was ligated, and the sinus venosus was cannulated and perfused
via the central hepatic vein. A second cannula was inserted into the
ventral aorta to receive output from the heart. In some preparations, the
coronary artery was cannulated with a small polyethylene tube and perfused
with oxygenated Ringer. In all preparations, the pericardium was kept intact.
After surgery, the entire fish was transferred to a 751 insulated water bath
filled with saline at 20 °C. The input cannula was connected to three 500
ml perfusate reservoirs, and recycling of perfusate was initiated by moving
the output tubing back to the perfusate reservoirs, which set output pressure
at approximately 6 kPa.
Solutions
For the temperature experiments, the perfusate consisted of (in mmol
l-1) 185.7 NaCl, 1.1 MgCl2, 7.0 KCl, 3.22
CaCl2, 10 sodium pyruvate and 10 Hepes. The pH was adjusted to 7.8
at 20 °C by addition of NaOH. Epinephrine was maintained in the solution
at 1 nmol l-1. For the epinephrine experiments, the perfusate
contained 1.84 mmol l-1 CaCl2, and the epinephrine
concentration in the perfusate was varied between 1 and 100 nmol
l-1. For the Ca2+ experiments, the nominal
Ca2+ concentration was 1.84, 3.68 or 7.36 mmol l-1, and
epinephrine concentration was maintained at 1 nmol l-1. Saline for
the 751 bath was made up as a 1:3 mixture of sea water with tap water (with
ice as needed). The perfusate was bubbled with 100 % oxygen throughout the
experiments.
Cardiac performance tests
Once the fish had been placed into the saline bath and the heart was
successfully recycling fluid to the reservoir, a set of tests was completed:
measurements under standard conditions, at maximum flow, at maximum output
pressure, at maximum power and again under standard conditions. Standard
conditions entailed an input pressure of 0-0.05 kPa and an output pressure of
approximately 6 kPa. To determine the maximum flow the heart could produce,
input pressure was elevated to 0.6 kPa and cardiac output was allowed to
stabilize. Input pressure was returned to 0 kPa and output pressure was
elevated in steps of 1-2 kPa until the heart could no longer beat rhythmically
or cardiac output was reduced by 50 %. Following a brief recovery period,
input pressure was again elevated to 0.6 kPa and output pressure was
simultaneously increased to approximately 10 kPa and elevated in additional 1
kPa steps to estimate maximum power production. Standard conditions were
intended to approximate in vivo conditions for a fish in a relaxed
state, while conditions of maximal flow and pressure were intended to evoke
the maximal performance of the heart, thus simulating a high-activity
state.
Temperature experiments
With input and output pressures at standard conditions, the temperatures of
the bath saline and perfusate were simultaneously adjusted over a period of
3-5 min, and the preparation was allowed to equilibrate for 3-5 min prior to
measurements at the new temperature. Control tests at 20 °C were completed
between measurements at each test temperature. In cases in which cardiac
output under standard conditions declined by more than 10 % from the initial
control test value (up to 31 %), data at the test temperature were normalized
by the ratio of initial values to control values bracketing the test
temperature. Experiments were completed within 90-180 min following
surgery.
Epinephrine and Ca2+ experiments
Following surgery, initial measurements were made using a perfusate
containing 1.84 mmol l-1 CaCl2 and 1 nmol l-1
epinephrine. Following the set of performance tests described above,
epinephrine was added to the perfusate to a final concentration of 10 or 100
nmol l-1. After 3-5 min, the performance tests were repeated.
Following the epinephrine tests, the perfusate reservoirs were drained, and
the fluid was replaced with fresh Ringer's solution containing 1 nmol
l-1 epinephrine for control tests. The performance tests were
repeated, and CaCl2 was then added (from a 1.84 mol l-1
stock) to 3.68 mmol l-1 or 7.36 mmol l-1. Performance
tests were repeated at each of these Ca2+ concentrations. The
reservoirs were again drained, and the perfusate was replaced with Ringer
containing 1.84 mmol l-1 CaCl2 and 1 nmol l-1
epinephrine for final control tests. Data were corrected for the decline in
performance of the preparation as described above.
Instrumentation, calibrations and analysis
Flows were measured with a 4 mm Zepeda electromagnetic cannulating flow
probe connected to a Zepeda SWF 5 flow meter. Input and output pressures were
measured with Statham P23XL pressure transducers through a Neurolog NL900-424
preamplifier (Neurolog DC preamplifier, Digitimer, UK). Flow and pressure
signals were read by a Maclab 8s hooked to a PowerMacintosh (1400cs) computer
running Maclab 3.5.4/s software (AD Instruments, Sydney, Australia). Flow
signals were calibrated by weighing the saline output over a measured time.
Pressure signals were calibrated with a water manometer. Mean flow, pressures,
power and heart rate were calculated from five or six beats using the Powerlab
program. Power output is expressed as mW g-1 heart mass (ventricle
plus atrium). Single-factor analyses of variance (ANOVAs) and regression
analysis were performed with temperature, epinephrine concentration or
Ca2+ concentration as the independent variable for each set of
conditions. Significance was assessed at P0.05.
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Results |
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Stroke volume was inversely affected by temperature (Fig. 1B; Table 1). Mean stroke volume increased from 0.41 ml kg-1 at 25 °C to 1.01 ml kg-1 at 10 °C under standard conditions. However, under maximal cardiac output conditions, stroke volume was greatest at 15 °C (1.42 ml kg-1) and showed no further increase at 10 °C. Stroke volume varied among individual fish, which probably reflects differences in the success of the surgery. Coronary perfusion had no observable effect on cardiac performance.
The increase in stroke volume with decreasing temperature was insufficient to compensate for the decline in heart rate. As a result, cardiac output was reduced significantly between 15 and 10 °C under standard conditions and with each decrease in temperature under maximal flow conditions (Fig. 1C; Table 1). The highest cardiac output (97.6±20.0 ml kg-1 min-1) was recorded under maximal flow conditions at 25 °C. Q10 values under standard conditions ranged from 1.14 (15-20 °C) to 2.58 (10-15 °C). The decline in cardiac output at lower temperatures was more pronounced when filling pressure was elevated to achieve maximal flow condition, with Q10 values ranging from 1.64 (20-25 °C) to 4.59 (10-15 °C). All fish showed a similar response to temperature; however individual values of cardiac output ranged from 69 to 115 ml kg-1 min-1 at 25 °C.
Maximal power output was highest at 25 °C and was 5.5±1.1 mW g-1 heart tissue. Myocardial power output showed a significant temperature-dependence, decreasing at lower temperatures under both conditions (Table 1). This effect was most pronounced under maximal power conditions (Fig. 1D), when both input and output pressures were elevated.
Effects of Ca2+ and epinephrine
Increasing the concentration of perfusate Ca2+ from 1.84 to 3.68
and 7.36 mmol l-1 by addition of a concentrated Ca2+
stock solution produced significant increases in stroke volume, cardiac output
and myocardial power output under maximal flow and maximal power conditions
(Fig. 2). Values recorded under
standard conditions were unaffected.
|
Increasing epinephrine concentration from 1 to 100 nmol l-1 had no significant effect on any cardiac parameter (Fig. 3). Epinephrine trials took place prior to Ca2+ trials using the same fish, so values of cardiac parameters recorded at maximal [epinephrine] and maximum [Ca2+] are not directly comparable.
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Discussion |
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Temperature
Changes in ambient temperatures had profound effects on all cardiac
parameters. Heart rate showed a linear dependence on temperature, falling to
19.6±3.2 beats min-1 at 10°C under standard conditions.
No arrhythmias were noted at the lowest temperatures tested (10 and 7°C),
which match the lowest ambient water temperatures encountered in acoustic and
archival pop-up satellite tracks of yellowfin tuna
(Block et al., 1997; K. Weng,
M. J. W. Stokesbury, A. M. Boustany and B. Block, in preparation). Stroke
volume increased as temperature decreased, such that decreasing temperatures
had little effect on cardiac output until temperature dropped below 15°C
under standard conditions. The increase in stroke volume with decreasing
temperature is consistent with results from ventricular strips
(Freund, 1999
) and direct
measurements of stroke volume changes in swimming yellowfin
(Korsmeyer et al., 1997a
). The
results from whole-animal and tissue studies indicate that changes in stroke
volume are likely to be an important factor in maintaining cardiac output in
tuna during ambient temperature changes, as is the case for other teleosts
including rainbow trout (Farrell et al.,
1996
).
Importantly, the maximal cardiac output generated at each temperature
dropped sharply, with a Q10 of 1.6 (20-25°C) to 4.6
(10-15°C) (Table 1) under
maximal flow conditions. This result indicates that the scope for increase in
cardiac output is greatly reduced at low temperatures, as shown in
Fig. 4. This lack of scope
in situ supports the hypothesis that temperature-related reductions
in cardiac output may be responsible for the thermal limitation seen in
acoustic and archival tag recordings of yellowfin tuna
(Block et al., 1997;
Brill et al., 1999
;
Marcinek, 2000
). Tuna range
through a thermally variable environment while relying on their metabolic and
vascular specializations to maintain relatively constant temperatures for the
viscera, swimming muscles and brain (Carey
and Teal, 1969
). Although much of the tuna body is protected from
changes in ambient temperature (Marcinek
et al., 2001
), the heart must meet the demands of high metabolic
rates in the face of sudden shifts in ambient temperature during deep dives or
when crossing frontal regions.
|
Ca2+
Increases in external Ca2+ concentration produced significant
increases in stroke volume, cardiac output and myocardial power output at
conditions of maximal flow and power in yellowfin tuna hearts. These results
are in accord with previous experiments showing that increasing
Ca2+ concentration increased isometric force in atrial strips from
skipjack tuna (Keen et al.,
1992) and in intact hearts of a variety of other teleosts
(Driedzic and Gesser, 1985
).
Keen et al. (1992
) also
reported that increased [Ca2+] shortened the activation and
relaxation kinetics for isolated atrial strips. However, differences in heart
rate with varying [Ca2+] in this study were not significant.
Contraction of cardiomyocytes is initiated by the influx of extracellular
Ca2+ through L-type Ca2+ channels, which stimulates the
myofibrils directly and/or opens Ca2+-release channels in the
sarcoplasmic reticulum (Fabiato,
1983). The relative importance of these two functions varies among
taxa. Recent studies indicate that tuna myocytes rely on intracellular
Ca2+ stores to a larger extent than myocytes of other teleosts
(Freund, 1999
;
Shiels et al., 1999
); however,
extracellular [Ca2+] modulates contractility. Blood
[Ca2+] may rise with exercise in teleosts
(Ruben and Bennett, 1981
),
suggesting that exercise-induced changes in blood [Ca2+] may play a
role in increasing cardiac output. The magnitude and importance of such
changes in tuna are unknown. Reported blood Ca2+ levels vary more
than twofold among tuna species (Sather
and Rogers, 1967
; Cooper et
al., 1994
) and could influence cardiac contractility. However
these differences may reflect different holding and sampling conditions rather
than interspecific variation. Thus, while the potential influence of external
[Ca2+] levels on cardiac contractility is clear, its relevance
in vivo remains to be determined.
Epinephrine
There were no significant effects of epinephrine on any cardiac parameters,
although upward trends were evident in heart rate, cardiac output and power
output with increasing epinephrine concentrations
(Fig. 3). The lack of an
epinephrine effect is at odds with previous studies on isolated atrial strips
(Keen et al., 1992). This
discrepancy may result from the different epinephrine concentrations used in
the two studies. We used three different epinephrine concentrations (1, 10 and
100 nmol l-1), while Keen et al.
(1992
) saw large effects of
epinephrine at 10 mmol l-1. Little is known about circulating
epinephrine concentrations in tuna, but Keen et al.
(1995
) reported levels ranging
from 3.5 to 55 nmol l-1 in anesthetized, spinally blocked
yellowfin. Although Watson
(1990
) measured millimolar
levels of catecholamines in blood from stressed tuna, no values are available
for free-swimming tuna, so it is possible that millimolar concentrations of
epinephrine influence heart function in vivo.
The low external Ca2+ concentration (1.84 mmol l-1) used in these preliminary experiments may have limited the effects of epinephrine, which acts to increase the open probability of voltage-gated Ca2+ channels. Thus, it is possible that simultaneous elevation of epinephrine and Ca2+ levels would exert synergistic effects on the tuna heart.
Spinally blocked tuna have mass-specific stroke volumes near our recorded
maxima and show very limited scope for modulation of stroke volume
(Bushnell and Brill, 1992).
Our lower stroke volume values may reflect the possible limitations of
perfused preparations, which include incomplete perfusion of the myocardium.
In addition, hormones released from the heart into the recirculating perfusate
may have exerted pharmacological effects on our preparation. Alternatively,
this difference may suggest that measurements on spinally blocked fish do not
represent routine values, as suggested by Korsmeyer et al.
(1997a
). Spinally blocked fish
may operate near their maximal cardiac output because of the stress of the
procedures (and adrenergic stimulation), and their hearts are therefore thus
comparable with those in our maximal flow or maximal power conditions. Our
in situ hearts set cardiac output and stroke volume at `standard'
conditions in response to adjustments of input and output pressures and
reflect `standard' performance only in so far as these pressures are
physiological. In contrast to stroke volume and cardiac output, accurate
ventral aortic pressures of yellowfin tuna measured in situ (10-11
kPa; Brill and Bushnell, 2001
)
and in swimming fish (12.2 kPa; Korsmeyer
et al., 1997b
) are similar to the pressures generated by our
in situ hearts at maximal power outputs (output pressure at maximal
power output 12.18±2.68 kPa; range 8.17-15.4 kPa, N=6), but
much higher than the 6 kPa set for standard conditions. Blood pressures in
spinally blocked fish may represent elevated values, as with stroke volume and
cardiac output. The absence of reliable measurements of cardiac output or
stroke volume in free-swimming tuna prevents us from distinguishing among
these hypotheses.
Cardiac performance in other Thunnus species
Electronic tagging data indicate that yellowfin tuna are restricted in
their ambient temperature preferences in comparison with bluefin and big-eye
tuna (Block et al., 1997,
2001
;
Brill et al., 1999
). At the
northern extent of their range, where yellowfin are likely to encounter the
coolest temperatures, acoustic tracks indicate that yellowfin venture into
cool waters (to 11 °C) below the thermocline only occasionally and return
to the surface after relatively short periods (<7 min) at depth
(Block et al., 1997
). More
extensive recordings from pop-up satellite archival tags indicate similar
temperature limitations for yellowfin tuna in the Gulf of Mexico (K. Weng, M.
Stokesbury, A. M. Boustany and B. A. Block, personal communication). Our data
supports the hypothesis that cardiac limitations restrict the thermal range of
yellowfin tuna.
In contrast to yellowfin, northern and southern bluefin tuna have
successfully invaded cooler waters and encounter cold temperatures while
foraging for extended periods in deeper waters. Atlantic bluefin tuna migrate
rapidly from waters at 22-29 °C in the breeding grounds to northern
feeding areas, where they spend extended periods in cold surface waters (8-12
°C) and encounter waters as cold as 2-4 °C at depth without apparent
compromise (Block et al., 2001;
B. A. Block, unpublished data). This raises the question of what physiological
specializations of the heart, if any, are associated with the wide thermal
tolerance within the Thunnus lineage.
Warm extremes of ambient temperatures may pose a greater challenge to tuna
than cold ambient temperatures. Warm temperatures increase the oxygen demand
of aerobic tissues, requiring increased cardiac output through increased heart
rate. However, the accompanying decline in stroke volume observed in the
present study suggests that the ability of yellowfin tuna to elevate cardiac
output is limited at high temperatures, as is the case in trout hearts near
their upper lethal limit of temperature
(Farrell et al., 1996). Adult
bluefin tuna breed in waters of 23-29 °C
(Block et al., 2001
). To
support the high metabolic rates of giant bluefin tuna at high ambient
temperatures, high cardiac outputs and correspondingly high heart rates are
required. High-frequency hearts require more rapid Ca2+ cycling and
increased expression of excitation/contraction coupling proteins
(Lillywhite et al., 1999
).
Although little is known about the function of the sarcoplasmic reticulum
Ca2+-release channel or the Ca2+ ATPase in tuna hearts,
preliminary data indicate that both the tropical yellowfin and skipjack have a
significant reliance on internal sarcoplasmic-reticulum-mediated
Ca2+ release (Keen et al.,
1992
; Freund,
1999
; Shiels et al.,
1999
). We hypothesize that the need for rapid Ca2+
cycling has resulted in the evolution of increased reliance on sarcoplasmic
reticulum Ca2+ release and re-uptake at both warm and cold
temperatures. Further investigation will be required to measure cardiac
performance in a variety of tuna species and to determine the underlying
cellular mechanisms enabling high performance across a range of
temperatures.
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