Read Is there an optimal haematocrit for rainbow trout, Oncorhynchm mykiss (Walbaum)? An interpretation of recent data based on blood viscosity measurements text version

Journal Of'Fish Biology (199 1) 38,53-65

Is there an optimal haematocrit for rainbow trout, Oncorhynchus mykiss (Walbaum)? An interpretation of recent data based on blood viscosity measurements

R. M. G. WELLS* AND R. E. W E B E R ~

*Department of Zoology, University of Auckland, Auckland, New Zealand and ?Department qf Zoophysiology, University of Anrhus, Aarhus C , DK-8000, Denmark (Received30 March 1990, Accepted 25 July 1990)

The viscosity of blood from rainbow trout was measured following manipulation of haematocrit by bleeding, hypoxia. exercise, and anaesthesia. Blood viscosity when measured at high shear rate (225 s I) was proportional to haematocrit. but the dependence of viscosity on shear rate was far less for swollen erythrocytes from exercised and anaesthetized trout. Erythrocyte swelling was most marked in exercised and anaesthetized trout, and is a confounding factor when considering the effect of haematocrit o n viscosity. The viscosity of blood with variable haematocrit. but constant mean cell H b concentration, indicated that the relative oxygen transport capacity in trout was optimal at a haematocrit of 30%. Data from this, and earlier studies show that haematocrit in trout isvariableand labile, yet none of the haematocrit values following manipulations are less than 85% of optimal. Optimal haematocrit is however. significantly higher than measured values from either cannulated or acutely venesected resting trout.

mykiss; haematocrit: blood viscosity Key words: O~icorlijnrhus

I. INTRODUCTION

A rise in haematocrit is associated with an exponential rise in blood viscosity, and consequently in the work that has to be performed by the heart (Rand et al., 1964). Fish biologists have documented a number of factors triggering haematocrit increase, both quantitatively through a rise in the number of cells per unit blood volume, and qualitatively through erythrocyte swelling (reviewed by Soivio & Nikinmaa, 1981; Weber & Jensen, 1988). There must therefore be a balance between haematocrit and viscosity, with additional regulation of oxygen transport provided by changes in blood-oxygen affinity. Schmidt-Nielsen (1984) described both haematocrit and viscosity as non-scaleable variables which are apparently adjusted to maximize oxygen transport, and minimize the work required for cardiac pumping. This appears ` sensible ' in terms of the optimizing power of Natural Selection and is enunciated in Taylor and Weibel's (1981) principle of ` symmorphosis ', which suggests that respiratory systems have evolved to a level required for maximum performance, with no single link in a system being stronger or weaker than the whole. We have puzzled over the wide range of intraspecific haematocrit values published for fish under apparently standard conditions. Haematocrit values have been studied extensively in humans and other mammals, where standard values are routinely employed as an index of blood oxygen carrying capacity in both diagnosis and research. And yet, as exemplified by rainbow trout, Oncorhynchus

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1991 The Fisheries Society of the British Isles

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R. M. G . WELLS AND R. E. WEBER

mykiss (Walbaum), standard haematocrits in fish seem an elusive quantity. In v i m experiments show that the viscosity of blood from trout increases dramatically at high haematocrit (Fletcher & Haedrich, 1987) supporting the Presbyterian epithet that ' too much of a good thing is bad for you '. We ask whether trout haematocrit is a poorly regulated component of a respiratory system in which oxygen transport is maintained through precise control of other variables such as ventilation, cardiac output, peripheral vascular resistance and blood oxygen affinity? One approach to answering this question is to predict an optimal haematocrit based on the compromise between the oxygen-binding capacity of trout blood and its viscosity. In addition, we present new information on blood viscosity following manipulation of haematocrit in whole fish. Changes in both oxygen-carrying capacity and erythrocyte swelling were observed. In v i m viscosity experiments using blood with adjusted haematocrit enabled us to propose an optimal haematocrit for rainbow trout, and to comment on recently published values that depart from this value.

11. MATERIALS AND METHODS

FISH MAINTENANCE A N D SURGERY Rainbow trout were obtained from a commercial trout farm and kept in large tanks supplied with aerated tapwater (1.5 1 min-' flow, 15f 1" C, PO,> 135 mmHg) for a minimum of 2 weeks before use. The fish were given a 12 : 12 h light : dark regime and appeared to feed well on maintenance rations. Aortic cannulations were carried out under 0.1 g l-' benzocaine anaesthesia as previously described (Tetens & Lykkeboe, 1985) and the fish were permitted to recover for 3-5 days before sampling.

HYPOXIA ACCLIMATION Oxygen tension in a 300-1 experimental tank was lowered over a period of 2 days and stabilized to 55 2 mmHg PO, using a PO,-stat controlling the supply of N, and air. The fresh water inflow rate was 1.5 1 min-' and nitrite levels, tested daily, were always less than 0.1 mg I ' I . Trout maintained for 2 weeks under these conditions were considered to be acclimated to hypoxia. Five cannulated fish were subjected to acute hypoxia (water PO, = 30 mmHg) for 1 h as described in Tetens & Lykkeboe (1985). ADDITIONAL MANIPULATIONS Five fish were exercised in a large tank over a period of 5-10 min by repeatedly touching the tail with a rod. A 5-min wait preceded sampling by acute caudal venepuncture. A further seven fish were anaesthetized in 1 : 10 000 buffered MS-222 and sampled from the caudal vein at the first signs of deep anaesthesia, when all ventilation had ceased and there was no response to tail stimulation. Samples were also taken from the aortic cannulas of seven normoxic fish which had been exsanguinated at a rate of 2-3 ml blood per day without plasma replacement. These fish had low haematocrits and were deemed anaemic. BLOOD SAMPLING Approximately 1-ml blood from resting, undisturbed fish was drawn from the cannula into a heparinized syringe. Other fish were rapidly despatched by spiking the brain (known to Japanese fishermen as ikejime), and the blood taken from the caudal vein, the procedure usually taking less than 30 s. MEASUREMENT TECHNIQUES Haematocrit values (Hct) were estimated after centrifugation in microhaematocrit tubes for 5 min at 5400 x g . Haemoglobin concentration ([Hb]) was measured by lysing erythrocytes in distilled water, reading the absorbance at 577 and 542 nm, and applying the

HAEMATOCRIT A N D VISCOSITY I N R A I N B O W T R O U T

55

respective millimolar extinction coefficients of 15.37 and 14.37 for oxyhaemoglobin. Mean cell Hb concentration (MCHC), calculated from [Hb]/fractional Hct, was used as the index of erythrocyte swelling. Nucleoside triphosphate (NTP) was assayed in deproteinized extracts using the Sigma enzymatic test kit No. 366-UV. We assumed that all the red cell nucleotides were ATP (cf Weberet al., 1976; Tetens & Lykkeboe, 1985). VISCOSITY MEASUREMENTS Viscosity was measured in 5OO-pl aliquots of fresh, whole blood using a cone-plate viscometer (model LVTD CP/11) with a cone angle of 8", capable of shear rates from 2 . 3 4 5 0 s- ' (Brookfield Engineering Laboratories, MA, U.S.A.). The temperature of the sample cup was regulated to 15-0f0.1" C using a circulating water bath. Calibration of the viscometer was checked regularly using Brookfield viscosity standards, and found to be within specification. Data are presented in units of centipoise (cP) which are equivalent to mPa.s. The viscosity of blood samples with adjusted haematocrit values was also measured. To this end, erythrocytes were separated from plasma in a pooled sample of blood (five fish, e x cannula) by gentle centrifugation at 1200g for 3 min at 17" C , and changing plasma: erythrocyte ratios to give Hcts between 0 and 70%. Measurements of Hct and viscosity, and protein-free extracts for ATP assays were made without delay. Preliminary tests of inequality of treatment variances revealed that sample variances did not differ significantly. Analysis of variance rejected a multisample hypothesis of equal treatment means and established a significant (P< 0.05) variance component. Following ANOVA, Tukey's multiple comparison test was applied a posteriori to analyse treatment effects (Zar, 1984).

111. RESULTS

VISCOSITY

The viscosities of blood were similar in acutely sampled normoxic and chronically hypoxic groups ( P > 0.5), at both high and low shear rates (Table I). The method of blood sampling (acute, or from cannulae) appeared to have a small effect on blood viscosity, although differences in haematocrit and MCHC were significant (P< 0.05). Acute hypoxia significantly increased blood viscosity ( P <0.05) and the erythrocytes swelled (MCHC decreased). Although anaesthesia and exercise resulted in erythrocyte swelling, these conditions greatly decreased the dependence of blood viscosity on shear rate (Table I). The effect of Hct on viscosity at constant shear rate was isolated from accompanying changes in MCHC by reference to the adjusted Hct data in Fig. 1. As Hct was increased, MCHC remained constant, Hb concentration rose linearly, and viscosity rose exponentially. Plasma osmolarity remained within normal physiological limits at approximately 270 mOsmol.

HAEMATOLOGY

Haematocrit values in the trout were increased following exercise, anaesthesia, and acute hypoxia (P<0.05 v. all other groups), and were lower in cannulated than in acutely sampled normoxic fish (Table I). As is apparent from the MCHC values, the erythrocytes of exercised and anaesthetized fish were significantly swollen compared to all other groups (P<O.O5), and MCHC lower in erythrocytes from acutely sampled fish than in those from cannulated normoxic fish (P< 0.05). These data demonstrate that Hct increase is not invariably related to Hb increase, and a corresponding improvement in oxygen carrying capacity cannot be assumed from

TABLE Factors affecting the haematology and blood viscosity of trout. Data are means f S.D. I.

Chronic hypoxia acute sample Anaesthesia Acute hypoxia cannulated Normoxia cannulated

Normoxia acute sample

n=7

n=9 19.2 3.8 f 0.70 f0.14 3.62 0.24 k 26.3f6.7 3.94f 0.80 21.0+11.4

11.5f4.2

Exercise acute sample n=5

n=7 38.0 6.4 f 1 0 f0.12 .5 2.78 0.26 1 . f5.3 84 6.25 2.42 8.9 4.6 f

n=4 32.8f 1 7 . 10 &01 .3 .3 3.16k0.54 24.9 6.7 f 6.01 f0.71 36.7f 12.6

n=6 19.4f8.8 0.84 0.39 f 4.30 0.36 f 32.6 9.3

4.03 f0.23

25.1 k6.1 0.89 0.24 & 3.60 0.88 f 32.0+ 8.3 7.00 1.9 k 1

41.8 9.0 1.18k0.32 2 8 k0.35 .1 27.9 3.6

4.77 0.76 f

Haematocrit (%) Haemoglobin (mM) MCHC (mM) ATP (pmol g - ' Hb) High shear viscosity 2 5 S C ' (cP) 2 Low shear viscosity 1 1.3s - (CP)

'

23.9f21.7

1 . f 10.2 76

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0

1 0

20

30

40

50

60

Haematocrit (%)

FIG. 1. Effect of adjusted haematocrit on viscosity. (n=four replicates from a pooled sample, 15'C.) Corresponding [Hb] and MCHC are also given. Shear rate 90 s-'.

elevated Hct values. The Hct values from exercised and anaesthetized fish, when M corrected for swelling (to MCHC = 3.6 m tetramer) become 29.9 and 27.4% respectively, and are closer to the control value of 25.1 O h . Erythrocyte ATP concentrations were lower during chronic and acute hypoxia, and after exercise and anaesthesia, than in normoxic controls ( P < 0*05),but similar in cannulated and acutely sampled normoxic trout ( P > 0 . 5 ) . These observations are consistent with ATP-modulation of oxygen affinity as a mechanism regulating the transport of Hb-bound oxygen (reviewed by Weber & Wells, 1989). Changes in ATP do not appear to influence either Hct or viscosity.

EXPERIMENTAL ANAEMIA

Exsanguinated fish had Hct values ranging from 3.9 to 13.5%, with corresponding reductions in [Hb] but constant MCHC (Table 11). The viscosity at low shear rate (1 1.3 s-I) was extremely low in the most anaemic fish, but rose steeply from 6-970 Hct. The role of plasma factors in the viscosity of anaemic fishes was not examined, but plasma osmolarity remained constant. IV. DISCUSSION

HAEMATOCRIT VARIABILITY

Hct in resting, cannulated trout is lower than that obtained from acutely venesected fish. Table I11 summarizes additional Hct data from rainbow trout, and

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TABLE Haematology and blood viscosity of anaemic trout. Data are for individual cannulated fish, 11. and are compared with cannulated controls (n = 6) Controls Haematocrit (YO) Haemoglobin (mM) MCHC (mM) Osmolality (mosmol) High shear viscosity 225 S K(cP) I Low shear viscosity 11.3 S - ' (cP)

3.9

-

300 2.12 4.31

4.8 0.20 4.23 265 1.75 2.87

5.6 0.25 4.45 260 1.74 3.47

5.9 0.26 4.46 270 2.40 3.69

9.0 0.40 4.46 250 3.71 21.7

12.9 0.50 3.90

-

13.5 19.4f8.8 0.62 0.84f0.39 4.60 4.30f0.36 275 282f11.3 4.08 4.03f0.23 20.0 17.6f10.2

4.31 27.4

TABLE Examples of haematocrit measured in rainbow trout 111. under normoxic controlled states. MCHC has been converted to m from g%, or calculated from 0, capacity data assuming 1.34 ml M oxygen bound per g Hb Haematocrit (YO) MCHC (mM) Acutely sampled fish 44.2 f3.8 S.D. 41.8 38.8 f3.6 S.D. 36.7f 1.1 S.E. 33.2 k 1 .O S.E. 32.3 k 2.8 S.E. Cannulated fish 30.4 f 1.7 S.E. 30 29.4 k 1.4 S.E. 28.2 f4.1 S.D. 27.9 f6.6 S.D. 27.8 f 1.94 S.E. 26.5 26.3 24.6 k 2.9 S.D. 24.3 k 1.7 S.E. 22.5 & 1.4 S.E. 21.7-t 1.1 S.D. 20.8 4.4 S.D. 19.5 f 1.8 S.E. 17.25 f2.63 17.1 k 2 . 6 Reference

2.94 2.98 3.88 3.80 3.75 4.90

-

Davie et al. (1986) Lane (1979) Lowe-Jinde & Niimi (1983) Fletcher & Haedrich (1987) Houston & Smeda (1979) Lane et al. (198 1) Barron et al. (1987) Milligan & Wood (1987) Railo et al. (1 985) Tetens & Lykkeboe (1981) Tetens & Lykkeboe (1985) Thomas et al. (1986) Soivio et al. (1980) Bushnell et al. (1 984) Soivio et al. (1972) Wood et al. (1982) Boutilier et al. (1988) Turner et al. (1983) Vorger & Ristori (1985) Primmett et al. (1986) Nikinmaa (1982) Kikuchi et al. (1985)

4.46 5.00 3.55 4.82

-

4.60 4.00 3.8 1

-

5.23 3.79 4.85 4.60

-

indubitably supports the importance of sampling technique. Recent studies have shown the implications of adrenoceptor activity at the membrane surface as a trigger for erythrocyte water and ion fluxes (Nikinmaa, 1982; Heming et al., 1987;

HAEMATOCRIT AND VISCOSITY IN RAINBOW TROUT

5.5

59

5.0

0

0

0

I

4- 5

E

U

I

4.0

0 0

.

3.5

3.0

20

25

30

35

40

3

Haematocrit

('A)

FIG.2. Scattergram of mean values of haematocrit and MCHC from Table 111 for cannulated (0)and acutely sampled ( 0 ) trout.

Tetens & Christensen, 1987). Erythrocyte swelling is accompanied by a rise in cell pH, decreased erythrocyte Hb and NTP concentrations, and decreased Hb-bound ATP, all of which serve to increase the oxygen affinity of Hb (Weber et al., 1976; Soivio et al., 1980; Soivio & Nikinmaa, 1981; Tetens & Lykkeboe, 1985; Primmett et al., 1986). If cannulated fish are unstressed and MCHC is a useful indicator of stress, then the results of Fig. 2 are unexpected. MCHC is not constant in cannulated groups, and the correlation between mean values of Hct and MCHC is weak (r = - 0.65). In addition to cell volume, MCHC may vary according to erythrocyte age, with newly recruited cells having lower MCHC (Wells & Weber, 1990). Two features emerge from the distribution of Hct data in Table 111. Firstly, the range of mean values is very large (1 7-30°/0 Hct) and implies a range in oxygencarrying capacity. Secondly, the means are highly dispersed, and offer no statistical grounds for rejecting extreme values. Variation between studies is markedly greater than within-study variation. Can the distribution be explained? Acclimation temperature is one factor affecting trout Hct (Houston & Smeda, 1979; Houston & Mearow, 1981), however, the values in Table I11 are from fish held close to 15" C. Recent work has shown the importance of circadian rhythms (Peterson & Gilmore, 1988) and sex (Miguel et al., 1988) on the Hct value of trout; but the magnitude of these changes is too small to account for the observed dispersion of mean Hct values. Size may have a minor influence, though Schmidt-Nielsen (1984, p. 141) believes this is unimportant. A third possibility is the technical

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problem of the time between surgery and sampling. Post-operative Hct continues to decrease for up to 3 weeks (Houston et al., 1971; Soivio et al., 1972; our unpublished results) and cannot be fully accounted for by serial blood sampling. We do not know whether other workers have noted this decrease, or whether the cause is simply due to internal bleeding or leakage from the site of catheterization. Acute sampling techniques may also generate misleading data as discussed by Heisler (1986). On the basis of evidence available to us, we cannot therefore assume that cannulated trout under sensory deprivation have a ' normal ' Hct. There is simply no way of knowing in the absence of an appropriate control sampling procedure. Frequency distributions for haematocrits occurring in wild caught starry flounder also show a wide range, from 3-36% (Wood eta/., 1979), yet normal levels of oxygen uptake are maintained in the face of severe experimental anaemia (Wood et d., 1982). These findings reflect the capacity of animals to compensate for decreased oxygen-carrying capacity through adjustments of the respiratory system as, for example, in systemic blood flow (Lenfant et al., 1970).

VISCOSITY AND HCT OPTIMIZATION

The viscosity measurements, the first to be reported from cannulated rainbow trout, suggest that blood viscosity in undisturbed fish is lower than that in acutely sampled stressed trout which have elevated Hct (Fletcher & Haedrich, 1987). Blood from anaemic fish had a still lower viscosity which was far less dependent on shear rate than that from cannulated normoxic fish (Table 11). Thus resistance to flow is predicted to be much less in the high resistance vessels of anaemic fish, and may partly compensate for reduced oxygen transport capacity. In the extreme case of Antarctic channichthyiid fishes which lack erythrocytes, blood viscosity is remarkably low and cardiac output exceptionally high (Wells et al., 1990). Both anaesthesia and strenuous exercise have marked effects on the sheardependence of blood viscosity (Table I). That is, viscosity does not increase to the high levels expected at low shear rates and the blood approaches the Newtonian ideal where viscosity is independent of flow (Chien et al., 1971; Chien, 1975). The importance of this lies in the fact that low viscosity confers a significant flow advantage to blood in capillaries and in venous circulation in which shear rates are probably very low. Thus the lowering of viscosity at low shear rate may, in physically disturbed fish, make a significant contribution to the lowering of vascular resistance, and thereby cardiac work required. We are not aware of any estimates for low shear rates in the capillaries and venous return of fishes. The observations may be explained either by changes in membrane fluidity, or in the cytoskeletal-membrane protein interactions associated with adrenergic cell swelling. Since it is a reasonable proposition that oxygen transport is proportional to blood oxygen carrying capacity, and inversely proportional to flow resistance (Snyder, 1983), the ratio of 0,-carrying capacity to viscosity provides a relative index of the oxygen transport potential of blood (see justification by Crowell & Smith, 1967; Hedrick et al., 1986; Wells & Forster, 1989). We calculated an index by assuming that 1 g Hb binds a maximum of 1.3 ml oxygen, thus oxygen transport capacity ( O X ) = 1.3 [Hb]/r, where v = viscosity). Figure 3 depicts OTC at different Hct values, and the optimum Hct is 30%. None of the observed values in

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Haernatocrit !%)

FIG.3. The optimum haematocrit defined by oxygen transport capacity of adjusted Hct (n=4 replicates from a pooled sample, 15" C). Arrows indicate the position of mean Hct from Table I with the following treatments: normoxia (NOR), chronic hypoxia (CH), exercise (EX), anaesthesia (AN), acute hypoxia (AH) and cannulated normoxic fish (CAN).

Table I are less than 85% of the optimal Hct, and the highest published values of Hct for cannulated, resting fish (cf. Railo et al., 1985; Milligan & Wood, 1987) approximate the optimum Hct. Only our anaesthetized and strenuously exercised trout showed higher Hct values confirming earlier observations (Soivio et al., 1972; Lowe-Jinde & Niimi, 1983; Primmett et al., 1986; Milligan & Wood, 1987; Korcock et al., 1988), but since the optimum Hct model is based on oxygen carrying capacity ([Hb]), cell swelling is not accounted for. When corrected to control values of MCHC, the two groups present Hcts of 27.4 and 29.8% respectively, and thus approach the predicted optimum. In light of these observations, we interpret variability in trout Hct as follows. Firstly, the extreme cell swelling (low MCHC) and Hct changes that occur under the exceptional circumstances of anaesthesia, strenuous exercise or handling stress, need not be considered as aspects of the normal physiology of trout. Secondly, the Hct optimum determined from viscosity measurements is not maintained under all physiological circumstances, as it tends to be among mammals (Crowell & Smith, 1967). Cameron & Davis (1970) suggested that blood-oxygen capacity in the trout is maintained at a level that allows cardiac output to vary over an optimal range of its efficiency curve. Splenic contraction does not however, appear to be a carefully regulated system in the trout (Yamamoto, 1988; Wells & Weber, 1990). Nevertheless, cardiac output, regional blood flow (Jones, 1971; Barron et al., 1987), and ventilation (Smith & Jones, 1982) are regulated features of the trout respiratory system which are influenced by Hct. Reducing the oxygen transport capacity by decreasing Hct below 30% does not appear to confer any energetic advantage through decreased shearing stress.

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Fine control of the oxygen transport system is permitted through regulation of Hb-oxygen affinity, although actual data supporting this as the site of fine control of the entire system is lacking. Trout erythrocytes contain multiple Hbs with different affinities for oxygen (Binotti et al., 1971; Weber et al., 1976; Eddy et al., 1977). The affinity of these haemoglobins for oxygen is increased both by a reduction in erythrocyte ATP (Soivio et al., 1980; Tetens & Lykkeboe, 1985), and by erythrocyte swelling. In contrast to homeothermic animals which tend to preserve maximal oxygen transport capacity through optimal Hct, the rainbow trout presents a picture of Hct lability that is nonetheless close to optimal. This idea parallels the generally well-defined basal metabolic rates in homeotherms, and the wide range of endogenous and exogenous factors known to affect standard metabolism in poikilotherms.

We thank Sonja Kornerup for expert technical assistance, Ole Nielsen for cannulating trout, and Gunnar Lykkeboe for adrenergic discussions. The project was funded by the Danish Science Research Council, grant no. 11-7764.

References

Barron, M. G., Tarr, B. D. & Hayton, W. L. (1987). Temperature-dependence of cardiac output and regional blood flow in rainbow trout, Salmo gairdneri (Richardson). Journal ofFish Biology 31,735-744. Binotti, I., Giovenco, S., Giardina, B., Antonini, E. M., Brunori, M. & Wyman, J. (1971). Studies on the functional properties of fish hemoglobins-11. The oxygen equilibrium of isolated hemoglobin components from trout blood. Archives OfBiochemistry and Biophysics 142,274-280. Boutilier, R. G., Dobson, G., Hoeger, U. & Randall, D. J. (1988). Acuteexposure to graded levels of hypoxia in rainbow trout (Salmo gairdneri): metabolic and respiratory adaptations. Respirotion Physiology 71,69-82. Bushnell, P. G., Steffensen, J. F. & Johansen, K. (1984). Oxygen consumption and swimming performance in hypoxia-acclimated rainbow trout Salmo gairdneri. Journal of Experimental Biology 113,225-235. Cameron, J. N. &Davis, J. C. (1970). Gas exchange in rainbow trout (Salmogairdntvi) with varying blood oxygen capacity. Journal o the Fisheries Research Board of Canada f 27,1069-1085. Chien, S . (1975). Biophysical behaviour of red cells in suspensions. In The Red Blood Cell, Vol. 2 (Surgenor, D. McN., ed.), pp. 1032-1 131. New York: Academic Press. Chien, S., Usami, S., Dellenmack, D. J. & Bryant, C. A. (1971). Comparative hemorheology-hematological implications of species differences in blood viscosity. Biorheology 8,35-37. Crowell, J. W. & Smith, E. E. (1967). Determinant of the optimal hematocrit. Journal of Applied Physiology 22, 50 1-504. Davie, P. S., Wells, R. M. G. & Tetens, V. (1986). Effects of sustained swimming on rainbow trout muscle structure, blood oxygen transport, and lactate dehydrogenase isozymes: evidence for increased aerobic capacity of white muscle. Jortrnal qf Experimental Zoology 237,159-171. Eddy, F. B., Lomholt, J. P., Weber, R. E. & Johansen, K. (1977). Blood respiratory properties of rainbow trout (Salmo gairdneri) kept in water of high CO, tension. Journal o Experimental Biology 67,37747. f Fletcher, G . L. & Haedrich, R.T. (1987). Rheological properties of rainbow trout blood. Canadian Journal of Zoology 65,879-883.

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63

Hedrick, M. S., Duffield, D. A. & Cornell, L. H. (1986). Blood viscosity and optimal hematocrit in a deep-diving mammal, the northern elephant seal (Mirounga angustirostris). Canadian Journal of Zoology 64,208 1-2085. Heisler, N. (1986). Comparative aspects ofacid-base regulation. In Acid-base Regulation in Animals (Heisler, N., ed.), pp. 397-450. Elsevier: Amsterdam. Heming, T. A., Randall, D. J. & Mazeaud, M. M. (1987). Effects of adrenaline on ionic equilibria in red blood cells of rainbow trout (Salmo gairdneri). Fish Physiology and Biochemistr-v 3, 83-90. Houston, A. H. & Mearow, K. M. (1981). Thermoacclimatory modification of red cell ion composition in rainbow trout, Salmo gairdneri: possible relationship with (Na+/ K+)- and (HCO, -)-stimulated ATPase activity. Comparative Biochemistry and P h ~ * ~ i o l o g ~3 15-3 19. 70A, ~ Houston, A. H. & Smeda, J. S. (1979). Thermoacclimatory changes in the ionic microenvironment of haemoglobin in the stenothermal rainbow trout (Salmo gairdneri) and f eurythermal carp (Cyprinus carpio). Journal o Experimental Biology 80,3 17-340. Houston, A. H., Madden, J. A,, Woods, R. J. & Miles, H. M. (1971). Variations in the blood and tissue chemistry of brook trout, Salvelinus fontinalis, subsequent to f handling, anaesthesia, and surgery. Journal o the Fisheries Research Board of Canada 28,635-642. Jones, D. R. (1971). Theoretical analysis of factors which may limit the maximum oxygen uptake of fish: the oxygen cost of the cardiac and branchial pumps. Journal o f Theoretical Biology 32,341-349. Kikuchi, Y . ,Hughes, G. M. & Duthie, G. G . (1985). The effects of moderate and severe exercise in rainbow trout on some properties of arterial blood, including red blood cell deformability. Japanese Journal of Ichthyology 31,422-426. Korcock, D. E., Houston, A. H. & Gray, J. D. (1988). Effects of sampling conditions on selected blood variables of rainbow trout, Salmo gairdneri Richardson. Journal of Fish Biology 33, 319-330. Lane, H. C. (1979). Some haematological responses of normal and splenectomized rainbow trout Salmo gairdneri to a 12% blood loss. Journal of Fish Biology 14, 1 59- 164. Lane. H. C., Rolfe, A. E. & Nelson, J. R. (1981). Changes in the nucleotide triphosphate/ haemoglobin and nucleotide triphosphate/red cell ratios of rainbow trout, Salmo gairdneri Richardson, subjected to prolonged starvation and bleeding. Journal of Fish Biology 18,661-668. Lenfant, C., Johansen, K . & Hanson, D. (1970). Bimodal gas exchange and ventilationperfusion relationship in lower vertebrates. Federation Proceedings 29, 1 1 2 4 1 129. Lowe-Jinde, L. & Niimi, A. J. (1983). Influence of sampling on the interpretation of haematological measurements of rainbow trout, Salmogairdneri. Canadian Joirvnal of Zoology 61,396402. Miguel, J. L., Agapito, M. T. & Recio, J. M. (1988). Sex differences of hematological and biochemical parameters in healthy rainbow trout (Salmo gairdneri, R.). Revista Espanola de Fisiologia 44,2 15-220. Milligan, C. L. & Wood, C. M. (1987). Regulation of blood oxygen transport and red cell pH, after exhaustive activity in rainbow trout (Salmo gairdneri) and starry flounder (Platichthysstellatus). Journal o Experimental Biology 133,263-282. f Nikinmaa, M. (1982). Effects of adrenaline on red cell volume and concentration gradient of protons across the red cell membrane in the rainbow trout, Salmo gairdneri. Molecular Physiology 2,287-297. Peterson, M. S. & Gilmore, R. G . (1988). Hematocrit, osmolality, and ion concentration in f fishes: consideration of circadian patterns in the experimental design. Journal o Experimental Marine Biology and Ecology 121,73-78. Primmett, D. N. R., Randall, D. J., Mazeaud, M. & Boutilier, R. G. (1986). The role of catecholamines in erythrocyte pH regulation and oxygen transport in the rainbow trout (Salmo gairdneri) during exercise. Journal of Experimental Biology 122, 139- 148.

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Railo, E., Nikinmaa, M. & Soivio, A. (1985). Effects of sampling on blood parameters in the rainbow trout, Salmogairdneri Richardson. Journalof Fish Biology 26,725-732. Rand, P. W., Lacombe, E., Hunt, H . E. & Austin, W. H. (1964). Viscosity of normal human blood under normothermic and hypothermic conditions. Journal of'Applied Physiology 19, 117-122. Schmidt-Nielsen, K. (1984). Scaling: W h y is Animal Size So Important.? Cambridge: Cambridge University Press. Smith, F. M. & Jones, D. R. (1982). The effect of changes in blood-oxygen carrying capacity on ventilation volume in the rainbow trout (Salmo gairdneri). Journal of' Experimental Biology 97,325-334. Snyder, G. K. (1983). Respiratory adaptations in diving animals. Respirution PhysiologJi 54.269-294. Soivio, A. & Nikinmaa, M. (1981). The swelling of erythrocytes in relation to the oxygen affinity of the blood of the rainbow trout, Salmo gairdneri Richardson. In Stress in Fish (Pickering, A. D., ed.), pp. 103-1 19. London: Academic Press. Soivio, A., Nikinmaa, M. & Westman, K. (1980). The blood oxygen binding properties of hypoxic Salmo gairdneri. Journal of Comparative Physiology 136,83-87. Soivio, A., Westman, K. & Nyholm, K. (1972). Improved method of dorsal aorta catheterization: haematological effects followed for three weeks in rainbow trout (Salmo gairdneri). Finnish Fish Research 1, 11-21. Taylor, C. R. & Weibel, E. R. (1981). Design of the mammalian respiratory system I . Problem and strategy. Respiration Physiology 44, 1-1 0. Tetens, V. & Christensen, N. J. (1987). Beta-adrenergic control of blood oxygen affinity in acutely hypoxia exposed rainbow trout. Journal of Comparative Ph~s&logyB 157, 667-675. Tetens, V. & Lykkeboe, G. (1981). Blood respiratory properties of rainbow trout, Salmo gairdneri: responses to hypoxia acclimation and anoxic incubation of blood in vitro. Journal of Comparative Physiology 145, I 1 7-125. Tetens, V. & Lykkeboe, G. (1985). Acute exposure of rainbow trout to mild and deep hypoxia: 0, affinity and 0, capacitance of arterial blood. Respirurion Phpsiolog~, 61, 22 1-23 5. Thomas, S., Fievet, B. & Motais, R. (1986). Effect of deep hypoxia and acid-base balance in trout: role of ion transfer processes. American Journal ojPhj9siology 25, R3 19-327. Turner, J. D., Wood, C. M . & Clark, D. (1983). Lactate and proton dynamics in the rainbow trout (Salmo gairdneri). Journal qf Experimental Biology 104,247--268. Vorger, P. & Ristori, M.-T. (1985). Effects of experimental anaemia on the ATP content and the oxygen affinity of the blood in the rainbow trout (Salmo gairdneri). comparative Biochemistry and Physiology 82A, 22 1-224. Weber, R. E. & Jensen, F. B. (1988). Functional adaptations in hemoglobins from ectothermic vertebrates. Annual Review of Physiology 50, 161-179. Weber, R. E. & Wells, R. M . G. (1989). Hemoglobin structure and function. In Compururive Pulmonary Physiology: Current Concepts (Wood, S. C., ed.), pp. 279-3 10. New York: Marcel Dekker. Weber, R. E., Wood, S. C. & Lomholt, J. P. (1976). Temperature acclimation and oxygenbinding properties of blood and multiple haemoglobins of rainbow trout. Journal qf Experimental Biology 65,333-345. Wells, R. M. G. & Forster, M. E. (1989). Dependence of blood viscosity on haematocrit and shear rate in a primitive vertebrate. Journal of Experimental Biology 145, 48 3-48 7. Wells, R. M. G. & Weber, R. E. (1990). The spleen in hypoxic and exercised rainbow trout. Journal of Experimental Biology 150,461-466. Wells, R. M. G., Macdonald, J. A. & de Prisco, G . (1990). Thin-blooded Antarctic fishes: a rheological comparison of the haemoglobin-free icefishes, Chionodraca kathleenue and Cryodraco antarcticus, with a red-blooded nototheniid, Pagothenia bernacchii. Journal of Fish Biology 36, 595-609. Wood, C. M., McDonald, D. G. & McMahon, B. R. (1982). The influence of experimental anaemia on blood acid-base regulation in vivo and in vitro in the starry

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flounder (Platichthys stellatus) and the rainbow trout (Salmo gairdneri). Journal of E.yperimenta1 Biology 96,22 1-231. Wood, C . M., McMahon, B. R. & McDonald, D. G . (1979). Respiratory, ventilatory, and cardiovascular responses to experimental anaemia in the starry flounder, Platichthys stellatus. Journal of Experimental Biology 82, 139-162. Yamamoto, K.-I. (1988). Contraction of spleen in exercised freshwater teleost. Comparative Biochemistry and Physiology 89A, 65-66. Zar, J. H. (1984). Biostatistical Analysis, 2nd ed. New Jersey: Prentice-Hall.

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Is there an optimal haematocrit for rainbow trout, Oncorhynchm mykiss (Walbaum)? An interpretation of recent data based on blood viscosity measurements

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Is there an optimal haematocrit for rainbow trout, Oncorhynchm mykiss (Walbaum)? An interpretation of recent data based on blood viscosity measurements