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1 Department of Wildlife, Fish, and Conservation Biology, University of California, Davis, California 95616-8751; and 2 Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Cardioventilatory variables and blood-gas,
acid-base status were measured in cannulated white sturgeon
(Acipenser transmontanus) maintained at 19°C during
normocapnic and hypercapnic (PwCO2 ~20 Torr)
water conditions and after the injection of adrenergic analogs. Hypercapnia produced significant increases in arterial
PCO2, ventilatory frequency, and plasma
concentration of cortisol and epinephrine, and it produced significant
decreases in arterial pH and plasma concentration of glucose but no
change in arterial PO2, hematocrit, and
concentration of lactate or norepinephrine. Hypercapnia
significantly increased cardiac output (Q) by 22%, mean arterial
pressure (MAP) by 8%, and heart rate (HR) by 8%. However, gut blood
flow (GBF) remained constant. In normocapnic fish, phenylephrine
significantly constricted the splanchnic circulation, whereas
isoproterenol significantly increased Q and produced a systemic
vasodilation. During hypercapnia, propranolol significantly decreased
Q, GBF, MAP, and HR, whereas phentolamine significantly decreased MAP and increased GBF. These changes suggest that cardiovascular function in the white sturgeon is sensitive to both 
- and 
-adrenergic modulation. We found microspheres to be unreliable in predicting GBF on
the basis of our comparisons with simultaneous direct measurements of
GBF. Overall, our results demonstrate that environmental hypercapnia (e.g., as is experienced in high-intensity culture situations) elicits
stress responses in white sturgeon that significantly elevate
steady-state cardiovascular and ventilatory activity levels.
cardiac output; gut blood flow; blood pressure; Acipenser; acid-base
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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IN THE WILD, FISH CAN BE EXPOSED to environmental fluctuations in O2 and CO2 levels. In addition, the rearing of fish under intensive culture conditions is associated with major alterations in dissolved gas concentrations. For example, the high-density (~75 kg/m3) rearing of white sturgeon with the use of O2 injection and water recirculation results in extremely high water-CO2 levels (25-35 Torr PCO2) because of the metabolic production of large amounts of CO2 by the fish. CO2 is extremely soluble in both water and plasma, and it diffuses rapidly across gill membranes. Thus although the increased arterial PCO2 (PaCO2) induces hyperventilation (11), this response is ineffective in reducing PaCO2, and the resulting respiratory acidosis may significantly affect the cardiovascular system. Although the negative inotropic effects of hypercapnic acidosis on the teleost myocardium are well documented in vitro (13, 20), little is known of these effects in vivo where the possibility of ameliorative responses exists. Perry et al. (32) recently published a study on cardiovascular responses of rainbow trout Oncorhynchus mykiss to environmental hypercapnia, but there have been no reports on cardiovascular function in chondrostean (paddlefish and sturgeon) fishes when these species are exposed to stressful gas concentrations.
Teleosts and elasmobranchs respond to hypoxia and hypercapnia by
releasing catecholamines (33) and corticosteroids
(9, 26). Although we know much about the
adrenergic control of the cardiovascular system under normoxia and
hypoxia (13, 17, 18,
29, 31), scant data are available on the
adrenergic control of cardiovascular function in fishes under
hypercapnic conditions. On the basis of in vitro studies, adrenergic
stimulation of the teleost myocardium is protective of inotropic status
under hypercapnic acidosis (13). In contrast, high levels
of circulating catecholamines are likely to increase systemic
resistance and to alter regional blood distribution. Of particular
interest in the present study was the regulation of gut blood flow
(GBF) because a general problem found in high-intensity aquaculture
operations, including white sturgeon, is reduced growth and survival
rates (42). Early work on fishes demonstrated that blood
sampling from the intestinal vein was difficult during periods of high swimming activity, after stress, and after injection of catecholamine agonist drugs (34). The conclusions drawn from these
observations were that GBF was very labile and that a potent
-adrenergic vasoconstrictory mechanism existed in the gut
(7). These conclusions were confirmed in vivo on sea raven
Hemitripterus americanus (2), and later work
has further increased our knowledge of the control of GBF in both
elasmobranch and teleost examples (e.g., Refs. 21, 41). In the species
examined, brief stresses cause rapid decreases in GBF, whether the fish
is in a nonfeeding or postprandial state. Nothing is known about GBF
and its control in white sturgeon and, therefore, it is possible that
reduced growth rate under hypercapnia is a result of poor GBF limiting
the digestive process.
The present study focused on comparing the cardiovascular status of white sturgeon during exposure to normocapnic and hypercapnic conditions. We hypothesized that the stress associated with hypercapnia would lead to significant changes in cardiac output (Q) and its distribution such that GBF would be significantly reduced. To begin to test this hypothesis, we measured Q and GBF with ultrasonic flow probes and regional blood flow with colored microspheres. Colored microspheres are regarded as a safe alternative to radiolabelled microspheres to examine regional blood flow in fish (4, 7, 23). Shifts in blood flow patterns were induced by hypercapnia and by adrenergic agonist and antagonist drug injections. To our knowledge, this is the first study involving simultaneous measurements of Q, GBF, blood pressure (BP), and blood gas, acid-base status in sturgeon.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals. White sturgeon (Acipenser transmontanus; 1.5-2.8 kg) were collected from a commercial sturgeon farm (Sierra Aquafarms; Elverta, CA) and quickly (<1 h) transferred to the University of California, Davis. Fish were transported in an oxygenated tank of well water from the farm and were placed outdoors in 1.3-m diameter fiberglass tanks (750 liter) receiving a continuous flow of aerated well water (19 ± 0.5°C). The fish were fed twice daily (Silvercup trout pellets) and were allowed at least 2 wk to recover from any transport-related stress.
Surgical procedures and recovery. Cardiovascular data were collected from 28 fish (1.8 ± 0.1 kg) that were subjected to one or more of the following surgical manipulations. Before surgical procedures, the fish were dip-netted and placed into a buffered (pH 7.0 with the use of NaHCO3) anesthetic water bath [3-aminobenzoic acid ethyl ester (MS-222), Sigma; 0.2 g/l] until ventilatory movements ceased. Fish were then weighed and placed on an operating table (dorsal recumbency), and retrograde ventilation was begun with an oxygenated, buffered anesthetic solution (MS-222; 0.1 g/l).
Cannulation of the dorsal aorta. Skin sutures (3-0 silk, Ethicon; Somerville, NJ) were placed between the first and third gill arches on the dorsal aspect of the buccal cavity and on the inside of the mouth. A 19-gauge hypodermic needle (Becton Dickinson Labware; Franklin Lakes, NJ) was used to puncture the cartilage between the second and third gill arches. Thereafter, a 1-m length of heparinized polyethylene tubing (PE-50, 0.58-mm ID, 0.965-mm OD; Clay Adams; Parsipanny, NJ) with an indwelling stainless steel wire was inserted into the dorsal aorta (DA). The wire was then removed, and the cannula was anchored in place with the preplaced sutures and led out of the mouth through a small-bore hole. The cannula was filled with heparinized saline (10 IU/ml, 0.9% NaCl) and regularly flushed to prevent clot formation. The DA cannula was used for arterial BP measurements, drug injections, and blood sampling. All 28 fish had a DA cannula, and of these, three had only a DA cannula.
Cardiac output. After dorsal aortic cannulation, the fish was placed on its side, and the gills and operculum were gently retracted to allow implantation of the ventral aorta (VA) flow probe for Q measurement. Access to the VA was achieved without disrupting the pericardium. A 1-cm incision was made in the isthmus parallel to the VA. The subdermal musculature and connective tissue were carefully teased apart with the use of blunt dissection to expose the VA, and an ultrasonic flow probe (3SB or 4SB, Transonic Systems; Ithaca, NY) was placed loosely around the vessel. Single silk sutures anchored the probe head onto the musculature of the isthmus, and the probe led to the inside of the opercular cavity and at two locations on the dorsal aspect of the body. Of the 28 fish tested, eight had a VA flow probe (DA + Q).
Splanchnic blood flow. In white sturgeon, the celiacomesenteric artery (CMA) is a single, short, large-diameter vessel lying in a dorsoventral direction on the right side of the fish between the liver and pharynx. To expose the CMA, a 5- to 7-cm-long midventral incision was made posterior to the pectoral girdle, and the liver was gently retracted. GBF was measured with an ultrasonic blood flow probe (1.5 or 2 SB, Transonic Systems) that was placed around the CMA. The probe head was held in place by a silk suture in the intestinal wall and by one or two sutures in the dorsal aspect of the visceral wall. After the flow probe head was filled with acoustic gel and probe operation was verified, the incision was sutured (3-0 silk, Ethicon) closed with a slightly everted closure pattern while antibiotic powder (erythromycin) was dusted onto the surgical field. The probe lead was then anchored once to the skin on the fish's ventral surface and twice along the lateral aspect of the body. Of the 28 fish, 13 had a splanchnic flow probe, and 10 of these also had a VA flow probe for simultaneous measurement of Q and GBF (DA + Q + GBF).
Postoperative care. Surgery generally lasted <1.25 h (0.75- to 1.75-h range), and recovery from anesthesia was initiated by artificial ventilation with the use of aerated, anesthetic-free water. Once ventilatory activity returned (generally <5 min), the fish was placed into a Plexiglas holding chamber (triangular in cross section, 30 liter, 20 × 20 × 91 cm) that accommodated the extended pectoral fins of the sturgeon. The holding chamber was fully submersed in an insulated fiberglass tank (250 liter), and both the tank and holding chamber received a continuous flow of aerated well water (~5 liter/min). Continuous flows of water over and under the fish were achieved with the use of two vertically positioned inlet ports at the anterior end of each chamber (10 cm apart). The dorsoventral pattern of water flow through the chamber was used because it appeared to minimize confinement stress. Each chamber was partially covered with black plastic to shield the animal from laboratory activity. Fish were allowed at least 24 h to recover from surgery before experiments.
Cannulas were flushed regularly with heparinized saline (100 IU/ml, 0.9% NaCl) to minimize clotting and to avoid the formation of thrombi. To determine whether our cannulation technique caused significant tissue damage in the fish, we performed postexperimental examination of the cannulas' position. No animals were found with significant tissue damage resulting from cannulation.Experimental protocol.
During normocapnia, cardiovascular variables [Q, GBF, BP, and heart
rate (HR)] and ventilatory frequency (Vf, determined
visually by counting opercular movements) were continuously measured
both before and after the injection of two vasoactive substances
(Sigma; St. Louis, MO): the -adrenergic agonist phenylephrine
hydrochloride (PEPH, 0.1 mg/kg) and the -adrenergic agonist
isoproterenol hydrochloride (Iso, 1.0 µg/kg). In preliminary
experiments, cardiovascular responses to lower doses of PEPH and Iso
(0.025 and 0.05 mg/g) produced inconsistent responses, whereas higher
doses had prolonged cardiovascular effects. When fish struggled in the
chambers, all cardiorespiratory parameters were allowed to return to
baseline levels before drug injection. The cannula was flushed after
all drug injections (1.0 ml, 0.9% NaCl), and each drug injection was
followed by a recovery period of no less than 15 min, sufficient time
for all cardiovascular variables being measured (i.e., HR, Q, or BP) to
return to preinjection levels. After all drug injections in
normocapnia, a blood sample was withdrawn for analysis of various
hematological parameters.
-adrenergic antagonist phentolamine hydrochloride
(Phent, 0.1 mg/kg); and the -adrenergic antagonist propranolol
hydrochloride (Prop, 2 mg/kg). With the exception of the Prop
treatment, a recovery period of at least 15 min was allowed after each
drug injection. The responses to the antagonist Prop were measured
after 30 min when cardiovascular variables stabilized. A second blood
sample was taken for hematologic analysis after the Iso injection
during hypercapnia (~4 h after the initiation of hypercapnia).
Water-CO2 levels in the fish holding chambers were
controlled with an equilibration column with the use of counterflows of water and gas upstream from the chambers. Normocapnic water was equilibrated with air, whereas hypercapnic water was produced with a
10% CO2-90% air mixture. The mixture came from either
premixed gas cylinders or by combining pure gases with an electronic
gas mixer (Cameron Instrument, model GF-2; Port Aransas, TX). This method yielded the same PwCO2 of 20 Torr.
Measurement and calculation of cardiorespiratory parameters. During experiments, BP and HR were monitored by connecting the fish's DA cannula to a Statham P23B (Oxnard, CA) pressure transducer, and Q and GBF were monitored by connecting the flow probes to a two-channel small animal blood flowmeter (T-206, Transonic Systems). Signals from the pressure transducers and the flowmeter were displayed on a Gilson (Middleton, WI) ICT-5H multichannel recorder, and these recordings were used directly for the measurement of all cardiovascular parameters.
The factory-calibrated flow probes were periodically checked by securing each probe around a short section of polyethylene tubing (Transonic Systems) and pumping saline through the tubing with the use of a multistaltic pump (model 426-2000, Haake Buchler Institute; Saddlebrook, NJ). Probes used in this study were in excellent agreement (e.g., r2 = 0.995) with the known flows generated by the peristaltic pump. Pressure transducers were calibrated daily with the use of a static water column. Values for HR, arterial BP, and Vf were determined by measuring 30-s intervals. Mean arterial pressure (MAP, mmHg) was calculated as MAP = diastolic pressure + 1/3 pulse pressure (pulse pressure = systolic pressure
diastolic pressure).
Chart records of 5-min periods of Q and GBF were digitized and
integrated to obtain blood flow values (in ml · min
1 · kg1). Cardiac stroke volume
(SV; in ml · beat1 · kg1) was
calculated as SV = Q/HR, and systemic vascular resistance (Rsys; in mmHg · ml1 · min1 · kg1) was calculated with the
use of the formula Rsys = MAP/Q. Splanchnic vascular
resistance (Rspl; in mmHg · ml1 · min1 · kg1) was determined with the
use of MAP/GBF. Relative GBF (rGBF) was calculated as (GBF/Q) × 100, and it is the percentage of Q going to the liver, spleen, stomach,
and intestine. Artifacts associated with struggle episodes were avoided
when selecting traces to measure control HR, MAP, and blood flows, by
allowing sufficient time for all cardiovascular variables being
measured (i.e., HR, Q, or BP) to return to prestruggle levels. However, the data after each struggle were analyzed to evaluate the effect of
struggling on cardiovascular function.
Regional blood flow measurements.
Colored microspheres [NuFlow microspheres, Interactive Medical
Technologies (IMT); Los Angeles, CA] were used to measure regional blood flow distribution in white sturgeon (n = 5, 1.4 ± 0.3 kg) at 19°C. Microspheres were suspended in a
solution of saline and 0.01% Tween 80 to a final concentration of
2.5 × 106 ml, and 200-µl samples of the solution
were injected into the fish. Before the injections, which occurred at
the same time of day for each fish (~1130, 1530, and 1630), the
solutions were vigorously shaken for 1 min. Colored microspheres (25 µm in diameter) were injected via the DA cannula during normocapnia
(control, violet), after 2-h exposure to hypercapnia (pink), and 5 min
after Phent injection during hypercapnia (blue). A 1.0-ml reference blood sample was taken 10 min after the injection of each of the colored microspheres. At the end of the experiment, fish were humanely
killed (overdose of MS-222), and the tissues and organs of interest
were dissected from the animal. The head, white and red muscles,
skeleton, ventricles, liver, spleen, stomach, intestine, kidney,
gonads, and a reference blood sample were individually weighed. The
heart, kidney, and reference blood samples were placed into 15-ml
polypropylene centrifuge tubes (weighed tissue <5 g). Organs >10 g
(liver, muscle, stomach, intestine, and gonads) were minced, and
subsamples (n 
4) were placed into 50-ml polypropylene centrifuge tubes (weighed tissue <8 g). Each tube was filled with diluted alkaline solution (IMT), stored at room temperature for 1 wk,
and shipped to IMT for tissue processing and sphere extraction and
counting. GBF (ml · min1 · g1
tissue) with the use of colored microspheres was determined by converting sphere deposition values (percent of total spheres recovered) to spheres/g tissue and correcting for Q with the use of:
GBF = Q × wt × FQ, where Q is the mean cardiac output,
wt is the body weight of the fish (kg), and FQ is the fraction of Q/g
tissue (5). The sum of individual flows for the liver, spleen, stomach, and intestine represented total GBF. All procedures were approved by the University of California Davis Animal Use and Care
Administrative Advisory Committee.
Blood analysis.
Blood samples (0.7 ml) were taken with the use of a gas-tight
glass syringe to determine blood gas and hematologic parameters. Arterial pH (pHa) was measured with the use of an acid-base
analyzer and thermostated electrodes (Radiometer PHM73/G297/K497;
Copenhagen, Denmark) calibrated with temperature-corrected precision
buffers (Radiometer). Arterial PO2
(PaO2) and PaCO2 were measured with the use of the acid-base analyzer with thermostated electrodes (Radiometer E5046/D616 and E5036/D616, respectively). These electrodes were calibrated with the use of humidified N2 and air, and
with a 10% CO2-90% air mixture before each measurement,
respectively. Hematocrit (percent packed red cells after centrifugation
for 3 min at 11,000 g) and whole blood concentration of
lactate (mM) and glucose (mM) (YSI 2700 Select analyzer) were
immediately measured. The remaining blood was centrifuged at 4,500 g for 5 min, and the plasma was extracted, preserved with an
equal volume of sodium metabisulfite (1 mM, an antioxidant), and stored
(<30 days) at 70°C until analyses were performed.
Water analysis. Water PO2 and PCO2 were measured with use of the Radiometer acid-base analyzer. Water pH was measured with a hand-held pH meter (Corning PS-15; Corning, NY) that was calibrated with commercial buffer solutions (Fisher Scientific; Pittsburgh, PA) before each measurement. Water temperature was measured daily with the use of a mercury thermometer and maintained at 19 ± 1°C with the use of chillers (Elkay ER-10; Lanark, IL) and thermostated (YSI 72; Yellow Springs, OH) submersible heaters. Water quality [Cl2] and [NH3/NH4+] was measured daily with the use of Cl2 (Hach; Loveland, CO) and ammonia (Chemetrics; Calverton, VA) test kits, respectively. Values were always <0.01 and 0.2 parts/million, respectively.
Statistical analysis. Normocapnic and hypercapnic values for blood gas, acid-base, stress hormone, and respiratory data in resting sturgeon were compared with the use of paired t-tests. Control values (values before drug injections or struggle episodes) for hemodynamic data (Q, HR, SV, MAP, Rsys, GBF) during normocapnia and hypercapnia were compared with the use of a one-way, repeated-measures ANOVA followed by the Bonferroni multiple comparisons procedure (SigmaStat statistical software, Jandel Scientific; San Rafael, CA). Cardiovascular responses to drug injections were compared with the control values preceding the injection with the use of a paired t-test. In all cases, statistical significance was taken as P < 0.05. All data presented in figures and throughout the text are means ± SE.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Normocapnia.
Normocapnic sturgeon had a pHa of 7.76 ± 0.18, a
PaCO2 of 2.8 ± 0.7 Torr, and a
PaO2 of 116.6 ± 4.1 Torr. In addition, plasma concentration of lactate was 0.52 ± 0.10 mM, plasma concentration of glucose was 5.2 ± 0.4 mM, and hematocrit was 21.6 ± 0.6%. Plasma stress-hormone concentrations under normocapnic
conditions were 41.5 ± 5.5 nM epinephrine, 96.5 ± 12.0 nM
norepinephrine, and 215.8 ± 38.5 ng/ml cortisol. Some fish
underwent more extensive surgery than others, and this is reflected in
the measured values of the concentration of epinephrine and cortisol
(Fig. 1, B
and C). Plasma concentrations of epinephrine and cortisol
were significantly lower for DA + GBF fish than for DA + Q + GBF fish. Vf was 58.5 breaths/min in normocapnic
fish, and Q, HR, and SV were 36.1 ± 2.3 ml · min1 · kg1, 48.0 ± 1.2 beats/min, and 0.83 ± 0.1 ml · beat1
· kg1, respectively (Fig.
2,
A-C). GBF in normocapnic fish was 8.9 ± 1.1 ml · min1 · kg1 (Fig.
3A).
This represented ~20% of Q. Control MAP and
Rsys were 21.9 ± 0.7 mmHg and 0.66 ± 0.03 mmHg · ml1 · min1 · kg1, respectively (Figs. 4,
A and B).
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1 · kg1) and rGBF (to
3.3% of Q). GBF was normally restored to control levels within 4 to 6 min after a struggle during normocapnia unless another struggle ensued.
An example of the effect of a struggle on GBF in a hypercapnic sturgeon
is shown in Fig. 5.
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-adrenoceptors are involved in vasoconstrictory control of the systemic circulation. Because PEPH injections
significantly increased Rspl by threefold (Fig.
3B), decreasing GBF by 40% and rGBF from 20 to 10%, it
appears that a significant proportion of the -adrenergic control of
MAP was located within the splanchnic circulation. Iso injections
significantly increased Q (by 12%), HR (by 9%), and SV (by 13%)
(Fig. 2), and it significantly decreased Rsys and MAP (by
12 and 14%, respectively) (Fig. 4). These results suggest that
-adrenoceptors are involved in vasodilatory control of the systemic
circulation and stimulation of cardiac activity. In contrast to PEPH,
Iso did not affect Rspl, GBF, or rGBF.
Hypercapnia. Hypercapnia resulted in a respiratory acidosis in white sturgeon. Four hours of hypercapnic exposure significantly increased PaCO2 (to 19.5 ± 0.7 Torr) and significantly decreased pHa (to 7.36 ± 0.08), without affecting plasma concentration of lactate (0.35 ± 0.1 mM). As expected, hypercapnia stimulated a 60% increase in Vf (to 95.5 ± 1.7 breaths/min). There was a small but statistically significant reduction in plasma concentration of glucose (to 4.5 ± 0.3 mmol/l) and significant increases in concentrations of cortisol (DA + GBF fish and mean values of all fish, Fig. 1) and of epinephrine (DA + GBF fish only, Fig. 1) with hypercapnic exposure. On the other hand, PaO2, concentration of norepinephrine, and hematocrit were unaffected during hypercapnia.
Before initiating hypercapnia, values for Q, HR, SV, MAP, and Rsys were not significantly different from those measured at the start of the experiments. Two hours of hypercapnia significantly increased Q (by 31%), HR (8%), and SV (41%) (Fig. 2). Initially, (~0.5 h) hypercapnia-mediated increases in MAP (to 22.6 ± 0.8 mmHg) reflected increases in Q not alterations in Rsys. However, after 2 h of hypercapnia, MAP remained elevated (at 22.5 ± 0.8 mmHg; Fig. 3) despite a significant (20%) decrease in Rsys. Hypercapnia did not significantly affect GBF, rGBF, or Rspl. Struggles were more frequent during hypercapnia than during normocapnia. Possibly as a result, values for Q recorded before struggling episodes were significantly higher (67.2 ± 7.4 ml · min1 · kg1) than the other
control values during hypercapnia (Fig. 2A). Struggles
during hypercapnia significantly increased Q (by 14.6 ± 4.5 ml · min1 · kg1). Although
hypercapnic struggles did not reduce absolute GBF or rGBF to levels
(2.9 ± 1.0 ml · min1 · kg1 and 9%, respectively) that were lower than observed
during normocapnia, struggles that reduced GBF by 50% were more
frequent (2.2 h during hypercapnia compared with 0.82 h during
normocapnia) and significantly longer (10-14 min during
hypercapnia compared with 4-6 min during normocapnia). During
hypercapnia, GBF was on average disturbed to some degree for 22 to 31 min in any given hour (2.2 struggles/h × 10-14 min in
duration). In contrast, the disturbance to GBF (3-5 min) was
almost an order of magnitude less during normocapnia (0.8 struggles/h × 4-6 min in duration).
PEPH injections produced qualitatively and quantitatively similar
responses under hypercapnia. There was no effect on Q, SV, or HR, but
Rsys and MAP increased significantly (by 17 and 24%, respectively). Similarly, Rspl increased by 2.3-fold,
absolute GBF decreased by 42%, and rGBF decreased from 12 to 5% (Fig.
3). Furthermore, Phent injections significantly decreased
Rsys, MAP, and Rspl by 22, 25, and 34%,
respectively, without affecting Q. These results suggest that the
systemic circulation is under tonic -adrenergic vasoconstriction and
that a significant component of this -adrenergic tone is found in
the splanchnic circulation. Struggle responses after Phent were not
frequent, and the magnitude of the reduction in GBF (22%) was
considerably less than that after PEPH injection (data not shown).
Cardiovascular responses to Iso injection during hypercapnia were
different than those observed during normocapnia (Figs. 2-4). Iso
injection during hypercapnia did not affect Q, MAP, or Rsys
and may have resulted because -adrenergic stimulation of the heart
was approaching its maximum. Prop significantly decreased Q (16%), HR
(22%), and MAP (30%) without affecting Rsys (Fig. 2,
A and B; Fig. 4, A and B).
In contrast to normocapnia, Iso injection reduced Rspl (by
28%) and significantly increased both absolute GBF (by 40%) and rGBF
(from 19 to 28%). Prop did not affect either Rspl or rGBF.
Therefore, the significant decrease in GBF (35%) after Prop injection
must have resulted from the decrease in Q. During normocapnia and
hypercapnia, we occasionally observed short-term (<10 min) sinusoidal
oscillations in MAP and GBF (Mayer waves). During these periods, the
pressure and blood flow patterns were in phase, and the frequency of
oscillations was always slower than Vf. An example of the
sinusoidal oscillation of GBF is shown in Fig.
6.
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Regional blood flow.
Organs and tissues (wet masses, including blood) were dissected from 20 sturgeon (1.6 ± 0.10 kg) to indirectly assess regional blood
flow. The head, skeleton, and skin comprised 59% of body mass but were
not processed for microspheres. These tissues were extremely difficult
to digest so that microspheres could not be counted. Combined red and
white muscle represented 35% of body mass, whereas viscera and
remaining blood constituted the remaining 6%. The muscles, heart,
gills, gonads, and kidney were individually processed for microspheres,
but regional blood flow (ml · min1 · g1) to these tissues was not significantly altered by our
experimental protocol (data not shown). The regional blood flow results
for the splanchnic organs (liver, spleen, stomach, and intestine) are
presented in Fig. 7. Unfortunately, the
microsphere data provided a pattern of total GBF that was qualitatively
and quantitatively different from the direct measurements obtained with
the ultrasonic flow probes (Fig. 3). Normocapnic GBF (total) measured
with the use of microspheres was ~3 ml · min1 · kg1, nearly 5 ml · min1 · kg1 less than the value
measured simultaneously with the ultrasonic flow probes (Fig.
3A). Although hypercapnia did not affect GBF when measured
with the use of flow probes, microsphere counts indicated that total
blood flow to the splanchnic organs increased by 11 ml · min1 · kg1. Finally, after Phent
injection, total blood flow to the splanchnic organs (20 ml · min1 · kg1) was much greater than
that measured directly with the implanted flow probes.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Normocapnic state. In a preliminary in vivo study at Sierra Aquafarms, we found that white sturgeon had high PaCO2 and low blood pH values (C.E. Crocker and J.J. Cech, Jr. unpublished data). Thus we were concerned that residual effects from these rearing conditions would influence the responses of our fish to acute, hypercapnic exposure. However, it appears that the 2-wk (minimum) acclimation period at the University of California in Davis was sufficient to clear any residual volatile or fixed acid loads and that our fish were physiologically similar to those used in other studies. The control arterial PO2, PCO2, pH, hematocrit, and Vf data are consistent with the values reported for quiescent normocapnic-raised white sturgeon by Crocker and Cech (19°C; Ref. 11) , and our arterial pH was similar to that of normocapnic Adriatic sturgeon A. naccarii (25°C; Ref. 34). In addition, the arterial pH, plasma concentration of lactate, PaO2, plasma concentration of glucose, and hematocrit reported for our sturgeon are characteristic of teleost fish (42). Whether some of the responses of our fish to hypercapnia reflected hypercapnic preconditioning as a result of the rearing conditions will require further study.
We made every effort to minimize disturbance of the fish during data collection. Nevertheless, concentrations of plasma with concentrations of epinephrine, norepinephrine, and cortisol indicate that our sturgeon were experiencing a significant level of stress under control conditions. Gamperl et al. (19) report that resting catecholamine levels in cannulated teleosts and elasmobranchs are typically <10 nM. In addition, resting hormone levels reported in this study are higher than those reported for cannulated white sturgeon (11), Siberian sturgeon A. baeri (25), and Adriatic sturgeon (35). In particular, the mean cortisol concentration during normocapnia was significantly higher than concentrations previously reported for normocapnic white sturgeon (<40 ng/ml; Ref. 11) and for normocapnic Siberian sturgeon (<10 ng/ml; Ref. 25). We suspect that the elevated levels of stress hormones in our fish resulted from the invasive surgery required to make the cardiovascular measurements. Therefore, although we report the first measurements of Q and GBF in any species of sturgeon, these values should be considered representative of moderately stressed fish. We anticipate that as surgical procedures and holding aquaria become refined, resting values of stress hormones will be reduced significantly. A primary objective of this study was to make the first direct measurements of Q in white sturgeon. Agnisola et al. (1) studied the effects of dietary polyunsaturated fatty acids on cardiac performance in Adriatic sturgeon and reported in vivo Q values of ~13 ml · min1 · kg1 in
anesthetized fish (~1 kg; 23 ± 1.0°C). Control Q in the
present study (36.1 ± 2.3 ml · min1 · kg1) was almost three times higher than this value, and
poststruggle measurements of Q during hypercapnia (81.8 ± 7.0 ml · min1 · kg1) were nearly
six times the resting Q reported by Agnisola et al. (1).
Because control Q in the present study at 19°C was comparable to
values reported for resting chinook salmon (Oncorhynchus tshawytscha, 8-11°C, 33 ml · min1
· kg1; Ref. 39) and leopard shark (Triakis
semifasciata, 20°C, 33.1 ml · min1 · kg1; Ref. 24), and sixfold increases in Q have not been
reported previously for fish (16), we suspect that the Q
value reported for anesthetized Adriatic sturgeon greatly
underestimates resting Q in sturgeon. Although, resting values for MAP
and Rsys (22 ± 1.0 mmHg and 0.63 ± 0.0 mmHg ml · min1 · kg1,
respectively) were within the range of values reported for resting fishes (7, 15), they are closer to values
found in elasmobranchs than in teleosts.
Although the control of HR in fish is accomplished by intrinsic,
neural, and humoral mechanisms (15), it has been suggested that resting HR in sturgeon is set by excitatory sympathetic tone (27). For example, Agnisola et al. (1)
reported that Adriatic sturgeon had an in vitro intrinsic HR of <30
beats/min and an in vivo HR of 60 beats/min at 23 ± 1.0°C.
Control HR in the present study (49 ± 1.5 beats/min) was similar
to that reported for quiescent white sturgeon (19°C; Ref. 11) and
Siberian sturgeon (52 ± 2 beats/min, 18°C; Ref. 25).
Resting SV for our normocapnic white sturgeon (0.83 ml · beat1 · kg1) was higher than values
previously reported for teleost fishes but similar to those reported
for elasmobranchs (14, 16). This finding is
interesting because white sturgeon possess a pericardioperitoneal canal
(PPC; C. E. Crocker, J. J. Cech, and J. B. Graham,
unpublished observations) as do sharks (24). Apparently,
the PPC allows for large SVs by permitting the displacement of
pericardial fluid from the pericardial cavity into the peritoneal
cavity (14, 24).
Cardiovascular control has not been studied previously in sturgeon in
vivo. The present study suggests that the systemic circulation is
predominantly under tonic constrictatory -adrenergic stimulation, although -adrenergic-mediated vasodilation and other humoral/neural influences may play a role. In addition, our findings suggest that a
significant component of this vasoconstrictory activity was located in
the splanchnic circulation. For example, the 17% change in
Rsys with PEPH injection was associated with
a threefold increase in Rspl (Figs. 3 and 4). Although
-adrenergic control of the white sturgeon heart appears to be either
minor or absent, our results show that -adrenoceptors play a
significant role in stimulating cardiac function. These findings are
qualitatively similar to those documented for both teleosts and
elasmobranchs (7, 8, 13,
29, 30), and so the white sturgeon does not
appear unusual in this regard.
No measurements of GBF in sturgeon or other chondrosteans exist in the
literature. Our direct measurements of GBF in white sturgeon show that
blood flow in the CMA (8.9 ± 1.1 ml · min1 · kg1) accounted for 20% of Q. Although our value for GBF is comparable to that reported for resting
chinook salmon (12.0-14.2 ml · min1 · kg1; Ref. 41), anesthetized rainbow trout (13 ml · min1 · kg1; Ref. 28), and Atlantic
cod (Gadus morhua, 7.6 ml · min1
· kg1; Ref. 3), the rGBF we measured (20%) was only
half that reported for the cod. The potent -adrenergic regulation of
the splanchnic vasculature, as revealed by the threefold increase in
Rspl with PEPH and the 50% decrease in Rspl
with Phent, is also consistent with these studies on nonchondrostean
fishes. Two pieces of evidence suggest that the pronounced decrease in
GBF after a struggle was primarily mediated by an -adrenergic
constriction of the splanchnic circulation. First, despite the 29%
increase in Q after a struggle, GBF decreased sharply and took several
minutes to recover. Second, although Rspl after a struggle
could not be determined quantitatively because of mechanical artifacts
in our pressure traces, it appeared that changes in Rspl
after a struggle were of a similar magnitude to those measured after
PEPH injection (2.36-fold). Although -adrenoreceptors are probably
the predominant mechanism involved in the control of Rspl
in white sturgeon, it is clear that other factors are involved. For
example, because Prop injection into our hypercapnic sturgeon decreased
GBF by 32%, -adrenoreceptors must also play a role in mediating
Rspl. The increase in Q after struggles most likely
reflected -adrenergic stimulation of chronotropy and inotropy as
well as an enhancement of venous return due to body undulations associated with struggles.
Regional blood flow measured with the use of colored microspheres.
Burggren and Randall (6) reported that white sturgeon
decreased total energy expenditures during hypoxia and suggested that
this hypometabolic response was partially accomplished by reduced
ventilatory and cardiovascular work. Furthermore, they hypothesized
that Q and regional blood distribution during hypoxia changed to meet
the minimal oxygen demand of the "vital" organs and tissues.
However, few studies have actually measured the distribution of blood
flow in fish (2, 3, 7,
10, 23, 41). Our expectation was
that the colored microspheres would reveal useful information on
regional blood flow in white sturgeon under conditions of normocapnia,
hypercapnia, and after -adrenergic blockade and that the indirect
measurements of GBF with colored microspheres could be calibrated
against the direct measurements obtained with the use of the ultrasonic
flow probes. In fact, this is the first time that a direct calibration
of the microsphere method has been attempted in fish. However, our
expectations were not realized, and we were very disappointed with the
quality of the microsphere results. First, we conducted eight more
microsphere experiments than those on the five fish reported here.
However, because sphere recovery values in many fish were very variable
(range 14-94%), only data from tissue microsphere recovery values
>35% are reported here. Second, individual microsphere flow
measurements had high variability, unlike the direct measurements of
GBF. Third, when GBF was measured with the use of flow probes
(directly) and microspheres (indirectly) in the same fish, the results
of the two methods were substantially different. GBF measured with the
use of microspheres during the control period was 2.8 ml · min1 · kg1 (nearly 1/3 of the
control values measured with the ultrasonic flow probes). In addition,
GBF measurements during hypercapnia and after Phent treatment were 38 and 72% greater, respectively, than those directly recorded with the
use of flow probes.
Hypercapnic status. In the present study, plasma norepinephrine concentrations during normocapnia (96.5 ± 12.0 nM) and hypercapnia (91.5 ± 8.5 nM) were higher than plasma epinephrine concentrations (41.5 ± 5.5 and 59.8 ± 11.6 mM, respectively), and only plasma epinephrine was significantly elevated during hypercapnia. In contrast, previous measurements of circulating catecholamines in white sturgeon (11) indicated that the predominant hormone released during rapid-onset hypercapnia was norepinephrine (transient spike followed by a return to control levels within 72 h), and this pattern of catecholamine release has been demonstrated in trout exposed to hypercapnia (39) and in dogfish (Scyliorhinus canicula) exposed to hypoxia (9, 29). Differences in the concentrations of plasma epinephrine and norepinephrine during hypercapnic stress may be species specific and related to the severity of hypercapnia, to catecholamine storage levels within the chromaffin tissue, or to different rates of reuptake, metabolism, and tissue binding (36). Alternatively, because our sampling interval (4 h) was longer compared with our previous study (1 h; Ref. 11), it is possible that we missed the transient norepinephrine spike.
Our results showing that hypercapnia caused considerable changes in blood-gas, acid-base, and ventilatory status in the white sturgeon are consistent with the results of our previous study (11). The significant increase in plasma concentration of cortisol observed during hypercapnia suggests that environmental hypercapnia initiated a stress response in white sturgeon. In fish, increases in plasma concentration of cortisol mobilize energy reserves (12) and will typically result in an elevation in plasma concentration of glucose. Interestingly, however, we recorded a 22% decrease in plasma concentration of glucose in our sturgeon when exposed to hypercapnia. In autoperfused hearts of the dogfish Squalus acanthias, hypercapnia (seawater equilibrated with 5% CO2) caused a vagally mediated bradycardia and a decrease in Q but no change in SV (22). However, our findings were the opposite and similar to those of Randall and Shelton (37), who reported tachycardia in hypercapnic tench Tinca tinca L. In hypercapnic white sturgeon, we report positive chronotropic and inotropic effects and a decrease in Rsys. This could have come about through sympathetic (-adrenergic) activation of the heart
and inactivation of -adrenergic mechanisms controlling vasomotor
tone in the peripheral vasculature. This is substantiated, in part, by
the observation that Iso had limited cardiovascular actions under
hypercapnia but stimulated the heart and systemic vasculature under
normocapnia. The adrenergic stimulation of the heart may be part of a
ventilation-perfusion matching related to the hypercapnic stimulation
of the respiratory center and Vf. In addition, adrenergic
stimulation could protect the myocardium from the negative inotropic
effects of hypercapnic acidosis that are well documented for teleost
hearts (13, 20).
Rspl and GBF were unchanged with hypercapnia. In addition,
measurements of rGBF with the use of microspheres and flow probes indicated that hypercapnia did not redistribute blood flow away from
the splanchnic organs. Therefore, the change in Rsys
associated with hypercapnia must reside elsewhere in the systemic
circulation. The effectiveness of -adrenergic splanchnic
vasoconstriction was retained under hypercapnia, whereas Iso reduced
Rspl and increased GBF under hypercapnic but not
normocapnic conditions. This latter result cannot be explained at this
time and will require further investigation.
Cardiovascular responses and their control during hypercapnia were
recently studied in rainbow trout (32) with the use of a
shorter (20 min), lower (PwCO2 = 9 Torr)
and colder (12-14°C) hypercapnic exposure compared with the
present study. A comparison of the two studies, however, reveals
important similarities and differences in the responses of these two
species. Under normoxia, it appears that a qualitatively similar
adrenergic control exists. Perry et al. (32) found that
epinephrine injection significantly increased Rsys, VA
pressure, DA pressure, venous pressure, and Q, presumably through a
mixture of - and -adrenergic effects. With PEPH, we found that
the -adrenergic effects were reflected in increased
Rsys, Rspl, and DA pressure (Figs. 3 and 4).
With Iso, we found that the -adrenergic effects were reflected in increased HR, SV, and Q with a decrease in Rsys (Figs. 2
and 4). Thus even though background plasma levels of epinephrine and
norepinephrine were higher in white sturgeon than in rainbow trout, the
sturgeon circulatory system was still responsive to adrenergic
stimulation. In rainbow trout, hypercapnia resulted in increased
Rsys, increased VA and DA pressures, bradycardia, and
decreased Q but no change in branchial resistance or venous BP. For
sturgeon, the responses were quite different. Rsys was
initially unchanged but subsequently decreased, and Q, SV, and HR all
increased significantly (Figs. 2 and 4). Thus the significant increase
in DA BP was due solely to the increase in Q. Although we currently
have no explanation for these differences, a number of possibilities
exist. First, the differences could be inherent to the species and
reflective of long, separated evolutionary histories. Second, there was
a significant difference in temperature between the two studies (12-14 vs. 19°C), and cardiovascular responses are known to vary with temperature in fish. Third, the hypercapnic exposure period was
longer in the sturgeon (120 vs. 20 min). However, it is difficult to
resolve whether the duration of hypercapnic exposure had any influence
on the difference in cardiovascular response in these two fishes. When
exposed to incremental levels of hypercapnia (up to 9 Torr
PCO2) that lasted for a total of 60 min, the
cardiovascular response of rainbow trout was the same as seen with the
single 20-min increment to 9 Torr (32). Fourth, the
rainbow trout were not stressed during hypercapnia, as indicated by
unchanged plasma catecholamine levels (32), perhaps
reflecting a longer (inbred) culture history than that of white
sturgeon. We do not think that the elevated Q in sturgeon was solely
due to an increase in plasma catecholamine levels during hypercapnia,
because neither epinephrine nor norepinephrine showed significant
changes (DA + VA and DA + GBF + VA groups) with
hypercapnic exposure. Instead, the differences could be related to the
2.5-fold increase in the number of struggling episodes. Because
struggling increased Q and HR, it is possible that Q during hypercapnia
did not recover fully. Therefore, even though we selected periods
between struggles that we assumed were a routine state, this may not
have been the case. The decrease in Rsys in sturgeon is
less easy to resolve with the increase in Rsys in rainbow
trout. Foremost, Rsys was initially unchanged with
hypercapnia even though struggling frequency had already increased.
Second, stress would be expected to increase rather than decrease
Rsys. Therefore, other than a real or
temperature-related response to hypercapnia that differs with that of
rainbow trout, the decrease could be similar to that seen in
postexercise, hypotensive rainbow trout (40).
Our original hypothesis was that poor GBF limits the digestive process
in white sturgeon during hypercapnia. Our observation that
environmental hypercapnia did not cause preferential redistribution of
blood away from the gastrointestinal tract and to other organs and
tissues (e.g., heart, brain, and kidney) under routine conditions clearly does not support this hypothesis. However, this narrow analysis
of cardiovascular status clearly ignores the cumulative effects of
struggles during hypercapnia and therefore biases the assessment of
overall GBF. During hypercapnia, white sturgeon were more hyperactive,
as evidenced by struggles that were twice as frequent compared with
normocapnic fish. In addition, each struggle during hypercapnia
resulted in a much longer negative effect on GBF. Whether this longer
duration reflected a harder struggle or some unknown
hypercapnia-induced effect on splanchnic blood flow regulation is
unclear at this time. The important point is that overall GBF was
reduced as a result, and this may be related to the poor growth of
white sturgeon maintained under intense, hypercapnic culture
situations. Further studies, however, are needed to ascertain whether
this hyperactive state persists in long-term hypercapnic situations.
In summary, we report the first comprehensive set of cardiovascular
measurements in white sturgeon. The cardiovascular controls that we
identified were qualitatively similar to those previously described for
teleosts and elasmobranchs. The impact of hypercapnia on cardiovascular
status and its control appeared to be rather small, with the exception
of hyperactivity and its negative consequences on GBF.
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ACKNOWLEDGEMENTS |
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For technical and logistical assistance, we thank E. B. Kim, M. A. Kirkman-Iversen, M. R. Lee, J. T. Michaels, C. A. Myrick, D. M. Nunes, L. E. Sharp, and D. F. Stiffler.
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FOOTNOTES |
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This project was funded by a University of California Patricia Roberts Harris Fellowship (to C. E. Crocker), a University of California Agricultural Experiment Station Grant (3455-H) (to J. J. Cech), a Natural Sciences and Engineering Research Council of Canada (National Sciences and Engineering Research Council) Grant (to A. P. Farrell), and a NSERC Post doctoral Fellowship (to A. K. Gamperl).
Present address of C. E. Crocker: Dept. of Biology, San Francisco State University, 1600 Holloway Ave., San Francisco, CA 94132.
Present address of A. K. Gamperl: Dept. of Organismal Biology, Portland State Univ., P.O. Box 751, Portland, OR 97207-0751.
Address for reprint requests and other correspondence: J. J. Cech, Jr., Dept. of Wildlife, Fish, and Conservation Biology, Univ. of California, Davis, CA 95616-8751 (E-mail: jjcech{at}ucdavis.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Received 14 September 1999; accepted in final form 16 March 2000.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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 L. M. Hanson, D. W. Baker, L. J. Kuchel, A. P. Farrell, A. L. Val, and C. J. Brauner Intrinsic mechanical properties of the perfused armoured catfish heart with special reference to the effects of hypercapnic acidosis on maximum cardiac performance J. Exp. Biol., May 1, 2009; 212(9): 1270 - 1276. [Abstract] [Full Text] [PDF]
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G. Ivanis, M. Braun, and S. F. Perry Renal expression and localization of SLC9A3 sodium/hydrogen exchanger and its possible role in acid-base regulation in freshwater rainbow trout (Oncorhynchus mykiss) Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2008; 295(3): R971 - R978. [Abstract] [Full Text] [PDF]
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B. Vulesevic, B. McNeill, and S. F. Perry Chemoreceptor plasticity and respiratory acclimation in the zebrafish Danio rerio J. Exp. Biol., April 1, 2006; 209(7): 1261 - 1273. [Abstract] [Full Text] [PDF]
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A. P. Farrell and S. M. Clutterham On-line venous oxygen tensions in rainbow trout during graded exercise at two acclimation temperatures J. Exp. Biol., February 1, 2003; 206(3): 487 - 496. [Abstract] [Full Text] [PDF]
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S. F. Perry and S. G. Reid Cardiorespiratory adjustments during hypercarbia in rainbow trout Oncorhynchus mykiss are initiated by external CO2 receptors on the first gill arch J. Exp. Biol., November 1, 2002; 205(21): 3357 - 3365. [Abstract] [Full Text] [PDF]
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R. L. Ingermann, M. Holcomb, M. L. Robinson, and J. G. Cloud Carbon dioxide and pH affect sperm motility of white sturgeon (Acipenser transmontanus) J. Exp. Biol., September 15, 2002; 205(18): 2885 - 2890. [Abstract] [Full Text] [PDF]
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M. Axelsson, J. Altimiras, and G. Claireaux Post-prandial blood flow to the gastrointestinal tract is not compromised during hypoxia in the sea bass Dicentrarchus labrax J. Exp. Biol., September 15, 2002; 205(18): 2891 - 2896. [Abstract] [Full Text] [PDF]
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S. F. Perry and J. E. McKendry The relative roles of external and internal CO2versus H+ in eliciting the cardiorespiratory responses of Salmo salar and Squalus acanthias to hypercarbia J. Exp. Biol., March 13, 2002; 204(22): 3963 - 3971. [Abstract] [Full Text] [PDF]
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