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Department of Arctic Biology and Institute of Medical Biology, University of Tromsø, N-9037 Tromsø, Norway
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Cabanac, Arnaud, Lars P. Folkow, and Arnoldus Schytte Blix.
Volume capacity and contraction control of the seal spleen. J. Appl. Physiol. 82(6):
1989-1994, 1997.
Volume changes in the spleens of hooded seals
(Cystophora cristata) and harp seals
(Phoca groenlandica) were measured
plethysmographically in vitro in response to epinephrine,
norepinephrine, isoprenaline, phentolamine, and acetylcholine. Dilated spleens contracted forcefully
within 1-3 min of 
-adrenoceptor activation with 1.0-5.0
µg epinephrine/kg body mass, whereas stimulation of 
-adrenoceptors
and cholinergic receptors had little effect. The mass of dilated hooded
seal spleens corresponded to 2-4%
(n = 7) of body mass, with volume (V;
ml) relating to body mass (M; kg) as follows: V = 12.0M + 910 (r2 = 0.96, n = 4). Thus the spleen of a 250-kg
hooded seal maximally expels 3.9 liters, or 13%, of its estimated
total blood volume. Average hematocrit in splenic venous outflow from
dilated spleens was 90 ± 3% (n = 3) in hooded seals and 85% (n = 2) in
harp seals. From these data we have estimated that the aerobic diving
limit of a 250-kg hooded seal increases only 105 s, at the most, if complete emptying of the spleen occurs during diving, while the corresponding estimate for a 112-kg harp seal is 80 s.
phocid seals; diving; circulation; catecholamines; hematocrit
INTRODUCTION A RISE IN THE RED BLOOD CELL concentration has been
observed during diving in the Weddell seal
Leptonychotes weddelli (9, 23, 25, 30)
and in the elephant seal Mirounga
angustirostris (8). This rise in red blood
cell concentration is believed to contribute toward extended
submersion. While the source of this hematocrit elevation is
undocumented in seals, several authors have suggested that the spleen
is the place of origin (4, 7, 23, 29, 30). This is based on the fact
that several terrestrial mammals have been shown to have a spleen that
may act as a red blood cell reservoir (for review, see Ref. 31).
Recently, in in vivo experiments on Weddell seals, Hurford et al. (23)
found that changes in splenic size (length and thickness) were
accompanied by changes in arterial hematocrit levels. However, marine
mammals also possess huge venous sinuses (5) in which blood flow may fluctuate substantially and at times even be stagnant (15, 22). It is,
therefore, reasonable to assume that the large veins can also, by
simple sedimentation of blood cells, be an origin of variations in
systemic hematocrit in pinnipeds.
Several attempts have been made to estimate the volume capacity of the
pinniped spleen (3, 19, 26), but most of these studies were based on
postmortem weighing of the organ, which yields little real information
on the size of the organ in vivo. Castellini and Castellini (7)
estimated the mass of the spleen of three species of phocid seals to
represent 4-14% of body mass by back calculations based on the
rise in hematocrit observed during diving. In so doing, they had to
assume, of course, that all the red blood cells originated from the
spleen. Ponganis and co-workers (29) attempted to measure the maximal
splenic volume in anesthetized harbor seals (Phoca
vitulina) and sea lions (Zalophus californianus) by using computerized tomography.
These animals were reported to have a spleen mass that varied between
0.8 and 3.0% of body mass.
The purpose of the present study was to test whether the seal spleen
can contract and expel its contents in a way similar to that previously
described for some terrestrial mammals. By using an in vitro technique,
we have administered various drugs (adrenergic and cholinergic) to the
spleens of hooded seals (Cystophora cristata), which are able to dive for >52 min and
reach depths in excess of 968 m (18). We also recorded maximal splenic
capacity and the hematocrit of the arterial blood and of the splenic
venous outflow of these animals. Some measurements were also made on spleens from the harp seal (Phoca
groenlandica), which is a not-so-capable diver (Ref.
17; Folkow and Blix, unpublished observations).
MATERIALS AND METHODS Experimental Animals
Pharmacological Experiments
For the pharmacological experiments, one subadult hooded seal weighing 138 kg and two 7-mo-old hooded seals, weighing 52.4 and 66.8 kg, were used. In <30 min postmortem, the splenic artery was cannulated and the spleen was perfused with 37°C oxygenated saline.The splenic volume was measured plethysmographically. After removal of
the spleen and start of perfusion, the spleen was placed in a bath made
of two transparent Plexiglas cylinders (Fig.
1). The internal smaller cylinder, the
organ bath (diameter: 0.25 m, length: 0.5 m), was filled with saline,
and the larger cylinder surrounding the small one was circulated with
thermostatically controlled water at 37°C. The
composition of the physiological saline was (in mM) 119.0 NaCl, 25.0 NaHCO3, 4.7 KCl, 2.5 CaCl2, 1.18 KH2PO4,
1.17 MgSO4, 5.5 glucose, and 0.027 EDTA. It was kept at 37°C and was oxygenated with a mixture of 95%
O2-5%
CO2.
The organ bath communicated with the outside through a small pipe. The cylinders were tilted to have a weak slope. Any change in the splenic volume was directly reflected in the size of a bubble of air at the top of the organ bath, measured by use of a ruler fixed to the bath. The size of the bubble was finally calibrated against volume (by using an equation correlating the volume withdrawn from the organ bath into a graduated cylinder to the corresponding value read simultaneously from the ruler). Within the bath, the spleen was perfused through its cannulated splenic artery while the perfusate left through the cannulated splenic vein, without being recirculated. On the arterial side, a peristaltic pump was used to maintain the arterial pressure at 96-110 mmHg, as directly read on a water column manometer connected close to the splenic artery. The minute volume of the pump was changed to maintain pressure despite any change in the splenic vascular resistance. On the venous side, the catheter in the splenic vein was raised to maintain a steady venous pressure of 6-8 mmHg. In addition to the reading of changes in splenic volume obtained from the ruler, the venous outflow was collected continuously and measured by use of graduated cylinders, as a control to verify that the system was functioning well. All variables were recorded every minute, starting 3 min before the injection of a drug. The drugs were injected into a three-way stopcock that was connected to the splenic artery. The volume of fluid injected was 1 ml for the agonist but sometimes was larger for the blockers. All drug doses were scaled to the body mass of the animals.
Experiment 1. Epinephrine was administered in doses of 0.005, 0.01, 0.5, 1.0, or 5.0 µg/kg. Sufficient time (10-45 min) was allowed for the spleen to recover to its preinjection size before another dose was given. Experiment 2. In separate series of experiments, epinephrine (1.0 µg/kg) and norepinephrine (1.0 µg/kg) were administered before and 4 and 9 min after injection of the-adrenoceptor-blocker phentolamine (100 µg/kg).
Experiment 3.
In separate series of experiments, acetylcholine was administered in
doses of 0.1, 1.0, and 5.0 µg/kg and the -adrenoceptor-agonist isoprenaline in doses of 0.1 and 1.0 µg/kg.
Experiment 4.
In separate series of experiments, acetylcholine (5.0 µg/kg) and
isoprenaline (1.0 µg/kg) were given 2-3 min after epinephrine (5.0 µg/kg).
Splenic Volumes
The maximal volume capacity of the spleen was measured in four hooded seals (270 kg, adult; 120 kg, adult; 56 kg, subadult; and 52 kg, juvenile) and in two adult harp seals (102 and 121 kg). In these animals, the excised spleens were first dilated by arterial perfusion with saline at a pressure of 96-110 mmHg, with a venous pressure of 12 mmHg, in the plethysmograph, after which they were removed to be weighed before and after injection of a high dose of epinephrine (1.0 or 5.0 µg/kg) into the splenic artery for determination of the maximal volume the spleen can expel.Hematocrit Levels
The hematocrit was determined immediately after death in splenic venous and/or aortic blood samples from six hooded seals. The spleens of three of these seals (120 kg, adult; 148 kg, adult; 104 kg, adult) were found to be dilated, whereas the spleens of the other three (214 kg, adult; 25 kg, 1 wk old; and 25 kg, 1 wk old) were contracted. Data were also collected from one adult harp seal and one 1-wk-old harp seal pup, both with dilated spleens. Hematocrit levels were determined by use of heparinized microhematocrit tubes after centrifigation at 13,000 revolutions/min for 5 min in a microcentrifuge.Statistics
When appropriate, results were meaned for each animal before group means were calculated to avoid nesting effect. Multiple dose responses were compared and tested with nonparametric Kruskal-Wallis one-way analysis of variance. Other data were tested with Student's t-test when parametric and with Kolmogorov-Smirnov one-sample or
2 tests when
nonparametric.
RESULTS
Pharmacological Experiments
In vitro experiments were carried out for up to 7-9 h without apparent deterioration of the organ, as indicated by the capacity of the spleens to respond in a reproducible way to various drug injections.All the spleens contracted within 1-3 min regardless of the doses
of epinephrine. The contraction started at the apex and at the margins
of the spleen and progressed toward the venous hilus. The time taken to
return to the dilated stage was more or less proportional to the
magnitude of the contraction (see Fig. 2),
as shown by use of the Kruskal-Wallis test on the grouped data from two
hooded seals (138 and 52.4 kg; K = 1.84, P < 0.25). The
dose-dependent response of the spleen of the 52.4-kg juvenile hooded
seal to epinephrine is illustrated in Fig. 2.
), 0.01 µg/kg (
), 0.5 µg/kg (
), and 1.0 µg/kg (
).
Epinephrine injections in doses of 0.005 µg/kg caused minor responses. When 0.01 µg/kg epinephrine was injected, the spleen responded weakly and expelled only 750 ml. A dose of 1.0 µg/kg caused a stronger contraction with expulsion of 1,550 ml. Injection of 5.0 µg/kg of epinephrine in pilot experiments proved to cause extremely prolonged contraction periods and was avoided because of the potential risk of disrupting the preparation. Furthermore, this dose was found to increase the expelled volume by only ~20%, and, consequently, a concentration of 1.0 µg/kg was chosen as a submaximal dose for further experiments.
The spleens reacted similarly to epinephrine and norepinephrine, and
the subsequent rates of dilation were also similar (Fig. 3). The mean (±SD) volume of fluid
expelled from the spleens after an epinephrine dose of 1.0 µg/kg was
751 ± 693 ml (n = 3) compared with
579 ± 519 ml (n = 3) for
norepinephrine in the same dose. These differences were not
significantly different according to a paired Student's
t-test
(t = 1.47, P = 0.28). In two hooded seals,
injections of the general -adrenoceptor blocker phentolamine before
epinephrine and norepinephrine largely abolished their effects (the
degree of splenic emptying was reduced by 99.3 and 99.9%,
respectively, for epinephrine, and by 99.1 and 92.7%, respectively, for norepinephrine, compared with the volume expulsion when epinephrine and norepinephrine were injected alone in doses of 1.0 µg/kg).
) and norepinephrine (1.0 µg/kg; ).
The -adrenoceptor-agonist isoprenaline, given to dilated spleens
(n = 3) at doses of 0.1 and 1.0 µg/kg (experiment 3), did not
cause any measurable volume effects. However, it was noticeable during
the experiments that the color of the venous outflow became dark red
after the injection of isoprenaline, an effect that lasted for ~5
min.
Injections of acetylcholine at concentrations of 0.1, 1.0, and 5.0 µg/kg (experiment 3) did not produce any measurable effects on the organ. Furthermore, when acetylcholine or isoprenaline was given in doses of 5.0 and 1.0 µg/kg, respectively, to spleens that were first made to contract by use of standard doses (1.0 µg/kg) of epinephrine (experiment 4), no obvious effect could be seen with regard to either the contraction state or the time taken by the spleen to return to its precontraction volume.
Splenic Volumes
Figure 4 illustrates the relationship between the mass of the maximally dilated spleens and the respective body mass of seven hooded seals. The relationship can be described by a linear function: SM = 17.5M + 1,085 (r2 = 0.92; n = 7), where SM is spleen mass (g) and M is body mass (kg).
) and residual mass after
epinephrine-induced contraction (n = 4; ) in hooded seals of different body masses. Relationships can be
described by the following equations: dilated spleen mass = 17.5 × body mass + 1,085 (r2 = 0.92;
n = 7); contracted spleen mass = 5.3 × body mass + 255 (r2 = 0.83; n = 4).
The mass of the spleens of four hooded seals was reduced to 18, 22, 27, and 38%, respectively, of the mass of the dilated organs, after
contraction by injection of a high dose (1.0 µg/kg) of epinephrine
(Fig. 4). The size of the seals did not seem to influence this response
(Kruskal-Wallis test; K = 3.0, P > 0.05). In two harp
seals, splenic mass was reduced to 16 and 14% of the mass of the
dilated organs (1,514 and 1,888 g, respectively) after a similar
treatment. The reductions in splenic mass of the two species were not
significantly different (Kolmogorov-Smirnov test; K = 1.0, P = 0.12). Figure 4 also illustrates
the mass of the contracted spleens (n = 4) plotted against body mass, which followed this relationship: SM = 5.3M + 255 (r2 = 0.83; n = 4). The maximal
volume that could be expelled (V; ml) was estimated from the difference
between the masses of dilated and contracted spleens and related to
body mass according to the equation V= 12.0M + 910 (r2 = 0.96 ;
n = 4). Thus a hooded seal of 112 kg
should be able to expel 2,200 ml of blood by splenic contraction. In
comparison, the maximum expelled volumes of two harp seals were 1,270 and 1,622 ml for the 102- and 121-kg animals, respectively. The average maximum expelled volume of these seals, which had a mean body mass of
112 kg, was 1,446 ml, which is significantly lower than the predicted
value for a similar-sized hooded seal
(2 test;
2 = 8.69, P < 0.05).
Hematocrit Levels
The hematocrit values obtained from the splenic veins of dilated spleens from adult hooded seals were 88, 90, and 93%, respectively, while the values for aortic blood from the first two were 51.5 and 57.5%, respectively, the sample from the last being lost. A hooded seal pup, moreover, had a hematocrit of 88% in the splenic venous blood and 59.5% in the aorta. In contrast, an adult hooded seal with a contracted spleen had a hematocrit of 57.5% in the splenic vein and 62% in the aorta. Two harp seals, one adult and one pup, had hematocrits of 83 and 88%, respectively, in the splenic venous blood.DISCUSSION
The present study has shown that the spleens of pinnipeds contract very
strongly when stimulated with catecholamines. The spleen of the hooded
seal responds to arterial epinephrine injections with a dose-dependent
decrease in its volume. Because the effects of epinephrine and
norepinephrine were abolished when the -adrenergic receptors were
first blocked with phentolamine, there is reason to assume that the
contraction is mediated mainly through activation of -adrenoceptors.
This result is in accordance with recent observations by Hurford et al.
(23) in Weddell seals in which epinephrine injections caused the spleen
to contract. It also corresponds well with those obtained in various
terrestrial mammals, e.g., guinea pigs (13) and dogs (27).
The possible role of -adrenoceptors in the seal spleen contraction
is at present obscure. Isoprenaline did not affect the quantity of
fluid expelled from the spleens, suggesting that activation of
-adrenoceptors is not involved. Yet, the fact that the color of the
venous effluent became darker red after isoprenaline injections suggests that -adrenoceptors do exist and somehow may be involved in
the process of releasing red blood cells from the spleen. In this
context it is interesting to note that injection of small doses of
isoproterenol (i.e., isoprenaline) in cats inhibited the red blood
cell-concentrating mechanism (20), which implies that retention of red
blood cells in the spleen is counteracted by -adrenoceptor agonists
also in this species.
Cholinergic-like transmitters have histochemically been identified in the spleens of Weddell seals (L. weddelli), crabeater seals (Lobodon carcinophagus), and fur seals (Arctocephalus gazella) (32). Still, injections of acetylcholine in doses of 0.1, 1.0, or 5.0 µg/kg into the spleens of our hooded seals did not affect their volume capacity. This result is in accordance with observations in cats, mice, and humans, where splenic cholinergic innervation is not present (31). In dogs, however, Daly and Scott (12) found that low doses of acetylcholine may dilate the spleen, whereas higher doses caused contraction.
The high hematocrit values that we have recorded in splenic venous blood of hooded seals (88-93%) and harp seals (82-88%) with dilated spleens suggest that seals have the same ability to concentrate red blood cells as do terrestrial mammals (1, 20). Similarly, the ability of seals to expel ~80% of the splenic volume is also in accordance with data for some terrestrial mammals, such as sheep (33) and dogs (6).
The maximal splenic expulsion during in vitro contraction in hooded and harp seals may be compared with the estimated total blood volume in the two species. If we assume this volume to be 12% of body mass (14), an adult 250-kg hooded seal would be able to expel ~13% of its blood volume (Fig. 4) while the corresponding value for an adult 112-kg harp seal is ~11%. Despite the fact that the hooded seal equals the Weddell seal in diving ability (18), this is dwarfed by the estimated splenic volume value of 30-40% for the latter (23, 30), which indicates that large species differences may exist among various phocid species. However, the Weddell seal estimates were mainly based on the assumption that the observed increase in the hematocrit during a dive was caused by splenic contraction alone, a notion that deserves to be reexamined.
The mass of the maximally dilated hooded seal spleen represents 2-4% of body mass (Fig. 4) and that of the adult harp seal 1.5% of body mass. These values are substantially lower than the 13.9% for the Weddell seal, 7.3-10.5% for the northern elephant seal, and 4.3% for the harbor seal, as estimated by Castellini and Castellini (7). But, again, their indirect estimates were based on the assumption that the spleen is the only origin of red blood cells. Ponganis and co-workers (29) have up to this time provided the only in vivo determination of seal splenic volume by use of computed tomography in harbor seals. Their study indicates a splenic mass of 0.8-3.0% of body mass, which is comparable with our data. Thus the low value of the spleen-to-body mass ratio in the only two studies where the volume of the spleen was measured reinforces the assumption that some red blood cell sequestration may also occur elsewhere in the body, possibly in the inferior vena cava and the hepatic sinuses. Such venous sequestration of red blood cells has previously been shown to take place, e.g., in dogs (6).
Our data on maximal splenic volume expulsion and hematocrit values in
hooded and harp seals may be used to estimate how much splenic
contraction may theoretically contribute to their aerobic diving limits
[ADLs (25)]. According to our data, a 250-kg hooded seal
will be able to expel 3.9 liters of blood with a hematocrit of 90%.
Hooded seal blood with a hematocrit of 63% has a hemoglobin (Hb)
concentration of 264 g/l (11). Blood with a hematocrit value of 90%
will then have a Hb concentration of 1.43 × 264 g/l, and the
O2-binding capacity of Hb is 1.34 ml O2/g Hb (24). Finally, if one
assumes that the diving metabolic rate of the hooded seal is similar to
that of the Weddell seal, i.e., 4.5 ml
O2 · kg
1 · min1
(10, 28) and that splenic blood is 100% saturated with
O2, it follows that the estimated
ADL of our 250-kg hooded seal will only increase at most by ~105 s on
splenic contraction, while the value for a 112-kg harp seal is only
~80 s. This minor increase in ADL for two expert divers like the harp
seal, and, in particular, the hooded seal, suggests that splenic
contraction is not primarily a means to extend submersion time, as
proposed by Hochachka (21) and Zapol (34) but more likely is a means to
increase the O2-carrying capacity
of blood and, hence, reduce surface time during repeated diving, as
suggested by Castellini and co-workers (9) and Ponganis and colleagues
(29). Another way of looking at it is that splenic red blood cell
concentration takes place to reduce blood viscosity while the animal is
at rest, as suggested by Elsner and Meiselman (16).
In conclusion, this study has shown that the spleen of some arctic
phocids is capable of storing substantial blood volumes, which are
released by rapid and forceful contraction of the spleen on
-adrenoceptor activation, whereas -adrenoceptors and cholinergic receptors have little effect. The hematocrit of harp and hooded seal
splenic venous blood may reach levels of 90% or more, and maximal
splenic contraction causes expulsion of a volume (ml) that relates to
body mass (kg) according to the relationship V = 12.0M + 910 in hooded
seals. This increase in the circulating blood volume does
not seem to cause any substantial increase of the ADL of hooded seals
but will, of course, increase the
O2-carrying capacity of the blood,
and, conversely, the blood viscosity will be reduced on splenic
dilation.
ACKNOWLEDGEMENTS
We thank the crew of the research vessel Jan Mayen for cooperation in the field.
FOOTNOTES
Address for correspondence: A. Cabanac, 1855 Commerciale, St. Jean Chrysostome, PQ, Canada G6Z 2L2.
Received 30 July 1996; accepted in final form 29 January 1997.
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