Blood Viscosity and Hematocrit in the Estuarine Crocodile, Crocodylus porosus

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1 Comparative Biochemistry and Physiology Part A: Physiology (1991) 99 (3): Blood Viscosity and Hematocrit in the Estuarine Crocodile, Crocodylus porosus R. M. G. Wells, L. A. Beard and G. C. Grigg Abstract 1. Viscosities of whole blood and plasma from Crocodylus porosus were low in comparison with other diving animals when measured over a range of shear rates at 30 C (e.g ± 0.07 mpa.sec and 1.67 ± 0.06 mpa.sec respectively, at a shear rate of 450 sec-1). 2. Hematocrit (19.2 ± 0.5%) and mean cell hemoglobin concentration (262 ± 23 g/l) are high in crocodiles compared with non-diving reptiles. 3. Nucleation of the red blood cell does not seem to have affected viscosity. 4. The potential for oxygen transport was estimated from pooled blood reconstituted to a range of hematocrits and used to predict an optimal hematocrit of 38%, which greatly exceeded measured values. 5. Low blood viscosity is associated with low flow resistance and may assist circulation during the low blood pressure events occurring during diving. Introduction Reptiles make extensive use of anaerobic metabolism during activity (Gatten, 1985), yet the natural dives of alligators (Lewis and Gatten, 1985) and crocodiles (Grigg et al., 1985) appear essentially aerobic. Crocodiles have a number of features that appear adaptive in their aquatic lifestyle and diving behaviour. These include cardiovascular shunts that conserve oxygen during diving (Grigg and Johansen, 1987), low respiratory quotients (Grigg, 1978), and hematocrits near the upper range of oxygen carrying capacity for reptiles (Grigg and Cairncross, 1980). Periods of apnoea have important consequences for blood gas tensions and acid base balance in crocodiles and, following burst exercise, result in an extensive lactacidosis (Seymour et al., 1985). Thus a store of oxygen and distribution to tissues is necessary for maintaining aerobic operations. There is, however, a potential conflict. High hematocrit pro-motes an increased blood oxygen store but it may be counter-productive to oxygen delivery if it also leads to higher viscosity. Blood viscosity and its effects on blood flow have been studied in a range of vertebrates, including mammals (Chien et al., 1971), amphibians (Hillman et al., 1985), and fishes (Fletcher and Haedrich, 1987; Wells and Forster, 1989), and these studies confirm that hematocrit has an exponential effect on blood viscosity. Further, diving mammals have very high blood viscosity, having high hematocrits, prompting Hedrick et al. (1986) to suggest that oxygen transport may become limited by blood viscosity. This possibility arises because blood oxygen transport is dependent on both blood flow and oxygen carrying capacity and, above a defined oxygen capacity, the former declines due to the blood's resistance to flow (Crowell and Smith, 1967). Nevertheless, in diving mammals, hematocrit is commonly elevated beyond the optimum predicted by this model (Hedrick et al., 1986; Wickham et al., 1989).

2 Apparently there are no data on the rheological characteristics of reptiles, despite the fact that all the orders have representatives that are competent diversmarine iguanas, aquatic snakes, turtles, and crocodiles. In this study, we examined the influence of hematocrit on blood flow, as revealed by viscosity measurements in the estuarine crocodile, Crocodylus porosus. Blood viscosity is a complex variable which is influenced by physical and physiological factors such as the deformability of erythrocytes, shear rate, and plasma proteins, and these also have been considered. Materials and Methods Blood sampling Estuarine crocodiles (Crocodylus porosus), 3-5 years old, and approximately 1.5 m in length were obtained during commercial slaughter at the Edward River Crocodile Farm at Pormpuraaw, Cape York Peninsula, Australia (14 54'S, 'E). Resting animals were killed with a rifle shot to the hind brain using low velocity 0.22 ammunition. Blood was taken immediately from a cerebral artery into a heparinised syringe and studied without delay. Hematology Hematocrit (Hct) and hemoglobin concentration ([Hb]) were measured using standard techniques (Dacie and Lewis, 1984), with the added precaution of centrifuging the cyanmethemoglobin solutions (Gruca and Grigg, 1980). Mean cell hemoglobin concentration (MCHC) was calculated from [Hb]/Hct fraction. Total plasma protein was determined spectrophotometrically by the biuret reaction. Blood viscosity Viscosity was measured on 0.5 ml samples of whole blood and separated plasma using a cone-plate viscometer with cone angle of 8 (model LVTD CP/11, Brookfield Engineering Labs, U.S.A.). Viscosity determinations were made over a range of shear rates corresponding with the rotational speed of the cone, and the results reported in units of mpa.sec (= centipoise). The temperature of the sample cup was held constant at C. Cells and plasma were separated by centrifugation at 1200 g from pooled blood, and a range of hematocrits reconstituted for subsequent viscometry. No evidence of lysis or change in MCHC occurred during the procedure. Fig. 1. Viscometric curves for blood and plasma from C. porosus at 30 C, Mean ± SD for seven animals.

3 Results Blood from C. porosus decreased in viscosity when shear rate was increased (Fig. 1) as expected from the non-newtonian behaviour of mammalian blood (Rand et al., 1964). Plasma viscosity was relatively less shear-dependent over the range of shear rates measured. Table 1 summarises hematocrit measurements and other hematological data. Hematocrit influenced blood viscosity in reconstituted samples and viscosity rose dramatically at hematocrits above 20%, this value corresponding with the in vivo hematocrit of 19.2% (Fig. 2). Assuming that oxygen transport by the blood is directly proportional to viscosity (see Snyder, 1983), the potential transport capacity may be calculated by the ratio 1.34 [Hb]/η, where η is viscosity at a shear rate of 90 sec 1 (Hedrick et al., 1986). The potential oxygen transport capacity for reconstituted hematocrits is shown in Fig. 3, and indicates an optimal hematocrit of about 38%. Fig. 2. Dependence of viscosity on hematocrit for reconstituted, pooled blood. Discussion High hematocrit and high MCHC combine to produce a high oxygen carrying capacity in C. porosus. Hematocrit values were slightly lower in our captive crocodiles than those in the wild (Grigg and Cairncross, 1980), and lower than in sea turtles (Lutz and Bentley, 1985), yet consistent with their diving habits, they lie in the upper range of oxygen carrying capacity for reptiles (Dawson and Poulson, 1962). Hematocrit comparisons in reptiles are however, complicated by differences in the temperatures at which the reptiles are normally active, such that hematocrit may be limited by the expected rise in blood viscosity as temperature falls (Pough, 1980). Values of MCHC were also high, consistent with the concept that high values of MCHC are typical of diving reptiles, compared with non-divers (Wood and Johansen, 1974; Seymour et al., 1981; Maginniss et al., 1983; Birchard et al., 1984), as is also the case within the Mammalia (Kooyman et al., 1981). In sea turtles also, pulmonary oxygen stores are supplemented by high blood oxygen carrying capacity and appear adequate to sustain predominantly aerobic dives (Lutz and Bentley, 1985). Diving in the estuarine crocodile is also predominantly aerobic (Grigg et al., 1985). Our results

4 therefore support the view that MCHC is a means of increasing oxygen stores in diving reptiles. The reptilian vascular system is characterised by large, widely spaced capillaries (Pough, 1980). Since reptilian hematocrits are only about one-third those of diving mammals, one might expect circulation under low pressure with little peripheral vasodilation to perfuse the predominantly white, skeletal musculature. The viscosity of crocodile blood at a high shear rate is slightly higher than that of diving mammals at an equivalent hematocrit of 20% (cf. Hedrick et a!., 1986; Wickham et al., 1989), but allowing for the 7 C higher temperature of the latter, they are most probably identical. This suggests that MCHC and nucleated erythrocytes in the crocodile do not impact significantly on blood viscosity. Increasing MCHC is an obvious way of increasing oxygen carrying capacity of the blood without increasing the number of circulating erythrocytes and hence viscosity. A marked increase in viscosity was evident above 20% hematocrit (Fig. 2). Fig. 3. Oxygen transport capacity as a function of hematocrit. In the case of C. porosus, the predicted hematocrit is far in excess of measured values. The theoretical optimum hematocrit for the elephant seal was lower than that measured in vivo, and has led to the suggestion that oxygen transport is compromised by storage capacity in diving mammals (Hedrick et al., 1986). Among poikilothermic divers, however, bull-frogs maintain a hematocrit that maximises oxygen transport capability (Weathers, 1976), but during maximal rates of oxygen uptake when

5 hematocrit is artificially elevated, the rise in viscosity cannot be compensated (Hillman et al., 1985). We propose that the lower than "optimal" hematocrit could be interpreted in terms of cardiovascular adjustments correlated with diving and other breathholds. Crocodiles are periodic breathers, and the pulmonary oxygen store is tapped during breathholds (Glass and Johansen, 1979); during longer dives blood may be shunted away from the lungs, perhaps in order to extend the aerobic range (Grigg and Johansen, 1987). Extended use of the pulmonary oxygen store is facilitated not only by the high blood oxygen carrying capacity, but by a significant increase in affinity of blood when carbon dioxide is given off from blood to lungs (Jelkmann and Bauer, 1980). The bicarbonate-mediated decrease in affinity ensures that oxygen released from the blood occurs at relatively high oxygen pressures. The oxygen binding properties of crocodile blood have been interpreted as being consistent with short burst activity (Grigg and Gruca, 1979), rather than for sustained aerobic activities such as diving. The oxygen affinity is relatively high, and there is a large effect of carbon dioxide (Glass and Johansen, 1979). The apparent conflict between the oxygen stores required for diving and the transport requirement for activity may be resolved in crocodiles by elevated reptilian MCHC and hematocrit that nevertheless do not compromise blood flow through high viscosity. The peculiar anatomy of the cardiovascular system in C. porosus allows for a pulmonary by-pass shunt during diving, and blood pressure decreases (Grigg, 1989). This arrangement also allows for extended aerobic metabolism by diverting blood to the systemic system. A low blood viscosity may assist circulation over a range of reduced blood pressures associated with diving. Acknowledgements We thank the staff of the Edward River Crocodile Farm and, in particular, Don Morris and Vic Onions for facilitating our research. The authors are grateful to the Australian Research Council for providing the funds which enabled this work to be carried out. R.M.G.W. was further supported by a grant from the Auckland University Research. References Birchard G. F., Black C. P., Schuett G. W. and Black V. (1984) Foetal-maternal blood respiratory properties of an ovoviviparous snake the cottonmouth, Agkistrodon piscivorous. J. Exp. Biol. 108, Chien S., Usami S., Dellenmack D. J. and Bryant C. A. (1971) Comparative hemorheologyhematological implications of species differences in blood viscosity. Biorheology 8, Crowell J. W. and Smith E. E. (1967) Determinant of the optimal hematocrit. J. Appl. Physiol. 22, Dacie J. V. and Lewis S. N. (1984) Practical Haematology 5th edition, 453 pp. Churchill Livingstone, Edinburgh. Dawson W. R. and Poulson T. L. (1962) Oxygen capacity of lizard bloods. Am. Midl. Nat. 68, Fletcher G. L. and Haedrich R. T. (1987) Rheological properties of rainbow trout blood. Can. J. Zoo/. 65, Gatten R. E. (1985) The uses of anaerobiosis by amphibians and reptiles. Amer. Zoo/. 25, Glass M. L. and Johansen K. (1979) Periodic breathing in the crocodile, Crocodylus niloticus: consequences for the gas exchange ratio and control of breathing. J. Exp. Zool. 208,

6 Glass M. L. and Wood S. C. (1983) Gas exchange and control of breathing in reptiles. Physiol. Rev. 63, Grigg G. C. (1978) Metabolic rate, Qio and respiratory quotient (RQ) in Crocodylus porosus, and some generalizations about low RQ in reptiles. Physiol. Zool. 51, Grigg G. (1989) The heart and patterns of cardiac outflow in Crocodilia. Proc. Aust. Physiol. Pharmacol. Soc. 20, Grigg G. C. and Cairncross M. (1980) Respiratory proper-ties of the blood of Crocodylus porosus. Respir. Physiol. 41, Grigg G. C. and Gruca M. (1979) Possible adaptive significance of low red cell organic phosphates in crocodiles. J. Exp. Zool. 209, Grigg G. C. and Johansen K. (1987) Cardiovascular dynamics in Crocodylus porosus breathing air and during voluntary aerobic dives. J. Comp. Physiol. B 157, Grigg G. C., Farwell W. D., Kinney J. L., Harlow P., Taplin, L. E., Johansen, Kjell and Johansen, Kjetil (1985) Diving and amphibious behaviour in a free-living Crocodylus porosus. Aust. Zoo/. 21, Gruca M. and Grigg G. C. (1980) Methemoglobin reduction in crocodile blood: are high levels of met Hb typical of healthy reptiles? J. Exp. Zool. 213, Hedrick M. S., Duffield D. A. and Cornell L. H. (1986) Blood viscosity and optimal hematocrit in a deep-diving mammal, the northern elephant seal (Mirounga angustirostris). Can. J. Zoo/. 64, Hillman S. S., Withers P. C., Hedrick M. S. and Kimmel P. B. (1985) The effects of erythrocythemia on blood viscosity, maximal systemic oxygen transport capacity and maximal rates of oxygen consumption in an amphibian. J. Comp. Physiol, B 155, Jelkmann W. and Bauer C. (1980) Oxygen binding proper-ties of caiman blood in the presence and absence of carbon dioxide. Comp. Biochem. Physiol. 65A, Kooyman G. L., Castellini M. A. and Davis R. W. (1981) Physiology of diving in marine mammals. Ann. Rev. Physiol. 43, Lewis, L. Y. and Gatten R. E. (1985) Aerobic metabolism of American alligators. Alligator mississippiensis, under standard conditions and showing voluntary activity. Comp. Biochem. Physiol. 80A, Lutz P. L. and Bentley T. B. (1985) Respiratory physiology of diving in the sea turtle. Copeia 1985, Maginniss L. A., Tapper S. S. and Miller L. S. (1983) Effect of chronic cold and submergence on blood oxygen trans-port in the turtle, Chrysemys picta. Respir. Physiol. 53, Pough H. (1980) Blood oxygen transport and delivery in reptiles. Amer. Zoo/. 20, Rand P. W., Lacombe E., Hunt H. E. and Austin W. H. (1964) Viscosity of normal human blood under normothermic and hypothermic conditions. J. Appl. Physiol. 19, Seymour R. S., Bennett A. F. and Bradford D. F. (1985) Blood gas tension and acid-base regulation in the salt-water crocodile, Crocodylus porosus, at rest and after exhaustive exercise. J. Exp. Biol. 118, Seymour R. S., Dobson G. P. and Baldwin J. (1981) Respiratory and cardiovascular physiology of the aquatic snake, Acrochordus arafurae. J. Comp. Physiol. 144, Snyder G. K. (1983) Respiratory adaptations in diving mammals. Resp. Physiol. 54, Weathers W. W. (1976) Influence of temperature on the optimal hematocrit of the bullfrog (Rana catesbeiana). J. Comp. Physiol. 105, Wells R. M. G. and Forster M. E. (1989) Dependence of blood viscosity on haematocrit and shear rate in a primitive vertebrate. J. Exp. Biol. 145, Wickham L. L., Elsner R., White F. C. and Cornell L. H. (1989) Blood viscosity in phocid seals: possible adaptations to diving. J. Comp. Physiol. B 159, Wood S. C. and Johansen K. (1974) Respiratory adaptations to diving in the Nile monitor lizard, Varanus niloticus. J. Comp. Physiol. 89,

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