\i
FISHERIES AND MARINE SERVICE
Translation Series No.3269
Stimulation of the activity of chloride-secreting cells in fish
by L.S. Krayushkina
Original title: Stimulyatsiya deyatel'nosti khloridsekretiruyushchikh
kletok ryb
From:
Tsitologiya
Translated by the Translation Bureau(DCM)
Multilingual Services Division
Department of the Secretary of State of Canada
Department of the Environment
Fisheries and Marine Service
Halifax Laboratory
Halifax, N.S.
1974
20 pages typescript
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L.S. Krayushkina.
TITLE IN ENGLISH - TITRE ANGLAIS
Stimulation of the activity of chloride-secreting cells in fish.
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Stimulyatsiya deyatel'nosti khloridsekretiruyushchikh kletok ryb.
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Tsitologiya.
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Gytology
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1972
14
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3 1974
Tsitologiya (Cytology), vol. 14, 1972, pp 731-738 (USSR)
UDO 591.14 s 591,423.4
Stimulation of the activity of
chloride-secreting cells in fish.
UNEDUEDTRANS.LATIONI
By L.S. Krayushkina.
For inforrnalion only
TRADUCTION NON REVISEE
Inforrneion souk:I:lent
Laboratory of Cortical-Visceral Physiology,
Physiological Institute of Leningrad University
and Laboratory of Kidney Function Development,
Institute of Evolutionary Physiology and
Biochemistry of the Academy of Sciences
of the USSR, Leningrad.
Resume.
The starting factor of the beginning of the work of
the chloride-secreting cells which participate in the removal
of the excess of sodium and chlorine ions with a salt load
was investigated. Adult specimens of tilapia Tilapia
mossambica Peters and beluga sturgeon juveniles Huso huso (L)
aged 2 months were used in the experiments. We compared the
morphological state of the chloride-secreting cells in fish
Numbers in the right-hand margin indicate the corresponding
page in the original.
SOS-200-10-91
731*
2.
gills with an external salt influence and with intramuscular
731*
injections of solutions of electrolyte-sodium and non-electrolyte mannitol. In the experiments with the beluga sturgeon
/PLei-n-î
juveniles the ce-ri the depression ofublood plasma was
traced.
On the basis of morphophysiological and cyto-chemical
data we can conclude that the increase in the depression of the
blood plasma in the initial period of the salt adaptation is the
stimulator of the excretory activity of the chloride-secreting
cells.
The external salt influence cannot be considered the
main stimulus which stimulates the beginning of the activity
of the chloride-secreting cells.
The stimulation of the
activity of the chloride-secreting cells is connected with the
increase in the osmolity*of the blood plasma and not with an
increase in the blood of a concentration of ions only.
one
are
The chloride-secreting cells of the i11 • epit±Lelium
,
of the effector elements of the osmoregulation syStem
in fish. At present no doubt arises regarding the part of
these cells in the removal of the excess of sodium from the
organism (Copeland, 1947, 1948, 1950; Ginetsinskii and others,
1961; Natochin and Krestinskaya, 1961; Threadgold and
Houston, 1961; Krayushkina, 1967a, 19676 and others) . At the
same time much is still not clear in the mechanism of the work
of the chloride-secreting cells. In particular, it is not known
what is the starting factor of the beginning of the work of
these cells - the stimulus of the cells by an increased
*Revisor's note. "Osmolity" is a direct rendition of the original Russian
osmolyarnost', for which no other suitable English
bc-priaient is available.
731*
concentration of salts in the environment or the indirect stimdation
of the beginning of the excretory function as a result of
.the increased osmolity of the blood plasma,
This work is
devoted to solving this problem.
MATERIAL AND PROCEDURE'
The experiments were conducted with mature specimens of
tilapia Tilapia mossambica Peters of an average length of
81 mm, an average weight of 8 g and 11 months old, and
beluga sturgeon Huso huso (L) juveniles of an average length
of 170 mm, average weight 16,7 g and 2 months old.
In the experiments with freshwater tilapia, but -those distinguished
by
high euryhalinity,
the fish were divided
'
into 3 groups (10 specimens in each): the first - the control was kept in fresh water; the second was kept for 24 hours in
water with 20%0 salinity; the third was kept in fresh water
an
for 3 hours aftWintramuscular injection of a solution of
sodium chloride (0,27 ml of 2,5% solution of sodium chloride
to 10 g of weight).
The response [return] reaction of the chloride secreting cells to
-
the salt influence in fish in
different series of experiments
was judged by the morphological changesin these cells.
For this,
the fish from the first and second groups were killed after 24
hours, the fish from the third group in 3 hours after the
beginning of the experiment; the fixing of the gills was
4.
carried out in the liquid of Shampi, Meves and Karnua with
732*
the following histological treatment of the material and
preparation of sections 5-6 microns thick. The preparat3.ons
of the gill.swhich were fixed according to the method of Shampi
and Meveslwere coloured by ferric haematoxylin according to
Heidenhein for the research on the change in the cell structure.
The sections of gills which were fixed according to Karnua were
coloured with methyl groen-pyronine according to Kurnak for the
development of ribonucleic acid.
In the experiments with the beluga sturgeon juveniles,
the fish were divided into the saine threé groi.tps. However,
because of the lower euryhalinity of the beluga sturgeon
juveniles as compared to the euryhalinity.of the tilapia, the
second group was kept in lower salinity: 12.2-12.5%o. An
injection of a solution of 10% of sodium chloride, calculated
at 0.2 ml to 15 g of weight, was given to the fish of the
third group.
The histoldgi.cal-fixing of the gills by the Shampi
method was carried out parallel with the measurement of the
depression of the blood plasma not only 24 hours after the salt
influence but at shorter intervals as well. In a separate
experiment, an intramusciblar injection of non-electrolyte -
15% solution of mannitol (0.78 ml to 15 g of weight) was given.
5.
RESULTS
732*
The chloride-secreting cells of tilapia and
juvenile beluga sturgeon are located at the base of the
respiratory plates or between them together with the mucous
and so-called reserve cells. Along with the respiratory
cells which cover the respiratory plates, the
above
cells represent the gill epithelium which is located in the
basal membrane. The gill epithelium has under it one layer
of extremely elongated cells which we call underlying.
The state of the chloride-secretinm cells of tilapia
whichwere in fresh water. The chloride-secreting cells are
located mainly in one layer and make contact with the petalled
capillarvand eesanguiferous system of the respiratory plate
with their basal or lateral part through the underlying cells
and basal membranes. In addition, these cells can be located
in the reserve cells and are not directly in contact with the
sanguiferous system.
In both locations the apical pàrt of the
cells are washed by water.
As a rule, chloride-secreting cells
have an almost cylindrical or "flask-shaped" form. However,
cells are also found whose shape is almost cubic.
The borders
of the cells are clearly discernible.
The average height of these cells is 10.6 microns (with
fluctuations from 8 to 12.5 microns), the width is 8.1 microns
(with fluctuations from 6.2 to 8.7 microns). The cells have
6.
large nuclei. of a spheric form: the average diameter
732*
is 4.5 microns (with fluctuations from 3.7 to 6.2 microns).
As a rule, the nucleus contains one large nucleolus. The
nucleus is located in the basal or central part of the cell.
A significant quantity of mitochondri.ae 'l.n :-,the .: form .of ^ sma7.1
granules, uniformly distributed in all the ce:lls, appear in
the cytoplasm (f z g.1, a).
The ahloride-secreting cells are surrounded or come
In contact with an insignificant part of 1,heir surface 'with
cells called reserve, by analogy with similar cells in
sturgeon (whether there are such cells in tilapia is not
clear at present). The reserve cells are located in several
They are characterised by a polygonal form and by the
the
small amount of/cytoplasm, whose total mass is concentrated
layers.
around the nucleus.' The edges of the cell form protuberances
which adjoin one another. The borders of the cells are not
'clearly expressed.
The nuclei of the reserve aellti; do no t
have as definite a form as the nuclei of.the chloride-secreting
cells and can be both round and oblong or pblygonal. The
diameter of the nucleus is mainly 2.5-3 microns; in addition,
there are cells with nuclei whose diameter is from 3.7-5 microns.
The average diameter of the nuclei is 3.1 microns.
The colouring of the histological preparations of the
gills of telapia from fresh water with methyl-green pyronine
7
.
does not reveal an increased production of ribonucleic
acid in the chloride-secreting cells.
The cytoplasm
of these cells is uniformly coloured pale rose.
nucleus has a green colour.
732*
The
The nucleolus, with rare
exceptions, is a dark green colour. Now and then in theSe cells
nuclei are found whose nucleoli have combined colour - the
733*
central part of the nucleolus is a pale raspberry colour
which is scarcely seen in the general green colour.
As a
rule, in the reserve cells i the perinuclear zone of the cytoplasm is coloured deep raspberry, the peripheral part of the
cytoplasm is deep rose.
The nucleus is green. The nucleolus
is dark green and along with this colour it has a raspberry
centre.
The cells with an intensely coloured perinuclear
zone contain nucleoli with raspberry centres.
Uniformly
rose coloured cells have a green nucleolus.
The state of the chloride-secreting cells of tilapia
with a salt load.
The chloride-secreting cells of tilapia,
which were in water with 20%0 salinity l and of tilapia which
received an intramuscular injection of a sodium chloride
solution i proved to be in a different state than the same cells
in the control fish. On the other hand, no differences
between the state of the chloride-secreting , cells of fish in
these two variants of tests were
discovered, therefore a
description is given of the state of the chloride-secreting
cells which is characteristic of fish placed in salt water
as well as of fish which were in fresh water after the injection
8
.
733*
of the sodium chloride solution.
The chloride-secreting cells have peculiarities
The nuclei of
characteristic of their excretory state.
these cells are basally located and do not now have such
a definite spherical form and become weakly polymorphous
and often have bay-shaped depressions. Small vacuoles are
discovered in the cytoplasm; a large vacuole is formed in the
apical part of the cell which can
open
outwards.
v
Mito-
chondriae have for the most part the appearance of large
granules, uniformly distributed in the cytoplasm.
They fill 734*
the cytoplasm of the chloride-secreting cells densely, and
an impression is given that their concentration has increased
significantly compared with the concentration in these cells
of the fish which were in fresh water.
Because of this, the
chloride-secreting cells turn out to be dark coloured (fig.1, 6).
The sizes of the cells remain almost the same; in the
tilapia from the salt water the average height of the cells
is 11.4 microns (with variatiolis from 8.7 to 12.5 microns),
the average width is 7.4 microns (with variations from 6.2 to
8.7 microns); in those of the tilapia which received the
injection of the sodium chloride solution,the average height
of the cells is 11.3 microns and the average width is 7.5 microns,
with the same variations in the height and width of the cells
as in the tilapia from the salt water.
The average sizes of the
diameter of the nucleus of the cells remains the same - 4.5
microns.
The state of the reserve cells remained the same as
9
.
it was in the fish in the fresh water. One can note
734 *
only that the nuclei acquired a predominantly spherical
form.
When colouring the histological preparations of
the gills with methyl green-pyronine in the chloridesecreting cells, the perinuclear zone turns to an intense
raspberry colour, the nucleus remains green and the nucleoli
acquire an intense raspberry colour.
This indicates the
increased production of ribonucleic acid in the chloridesecreting cells with salt loads and the participation of the
nucleolus in this process.
The reaction of the reserve cells
to the colouring with methyl green-pyronine remains the same
as it was in the tilapia from the fresh water.
The blood plasma depression in beluga sturgeon
juveniles. With an intramuscular injection of a sodium chloride
solution, some increase in the blood plasma depreSsion is
observed in the first3 hours (up to -0.65 against -0.61 in
fresh water).
Subsequently, an adaptive decrease in the blood
plasma depression occurs and, 24 hours after the salt
influence, restoration of the previous level of depression
is observed (see table; fig. 2).
In the beluga sturgeon juveniles which were in water
whose salinity was 12,2-12.5 %f l an increase in the blood plasma
depression to a significant level (-0.71) is observed for 12
hours. After 24 hours of the salt influence of the environment,
1 0.
the blood plasma depression remains almost as before
(-0.70).
734*
The introduction of 15% of a mannitol solution,
in the first hours after the injection, is accompanied by
an increase in the blood plasma depression (-0.68 after 3
hours), and after this a decrease in the level of the
depreSsion occurs, considerably lower than the original.
After 24 hours the freezing point of the blood plasma
decreases to -0.54.
The state of the chloride-secreting cells in the
beluga sturgeon juveniles which were in fresh water.
735*
The
chloride-secreting cells of beluga sturgeon juveniles, by
their position in the gill epithelium, in form and in the
change in chondriome with the salt influence on fish, are
consistent with the chloride-secreting cells of the sturgeon
juveniles described earlier (Krayushkina, 1965, 1967a, 19676).
The chloride-secreting cells of the beluga sturgeon juveniles
from fresh water are distinguished by a greater range of the
nucleus position as compared to similar cells in juveniles
which are undergoing the salt influence. In fish which are
in freshwater conditions, the nucleus in the chloridesecreting cells has a spherical form-and has a mainly central,
eccentric and basal position as well.
The mitochondriae in
the cell are few and are located throughout all the cytoplasm
or concentrated in the basal part of the cell (fig. 18.1e).
11.
The vacuoles between the mitochondriae (with
735*
the rare exception) are absent. The height of the
chloride-secreting cells on the average is 14.1 microns
(with variations from 11.1 to 18.5 microns), the width
of the cells at the base on the average is 7.0 microns
(with variations from 5 to 8.5 microns).
The diameter of
the nucleus is 6.2-6.8 microns. The reserve cells are
distinguished by polymorphism, a large nucleus in relation
to the cell sizes and an insignificant cytoplasm zone free from
mitochondriae.
The greatest diameter of the cell on the
average is 8.7 microns (with variations from 7.7 to 11.2
microns). The diameter of the nucleus is 6.2 microns. When
colouring the gill epithelium with methyl green-pyronine,
the cytoplasm of the chloride-secreting cells turns a rose
colour uniformly, the nucleus at bright green and the
nucleolus a dark green.
The state of the chloride-secreting cells in the
beluga sturgeon juveniles which were in salt water. In the
chloride-secreting cells of the beluga sturgeon juveniles
which were in 12.2-12.5%0 salinity for 6 hours, a sharp
shifting of the mitochondriae into the apical part of the
cell is observed.
In this case, the mitochondriae acquire
a
spherical form. The nucleus has both an acentric and basal
position.
After 12 hours of the salt influence only part of
the cells transfers to the excretory state, while at the same
time after 24 hours all the chloride-secreting cells are in
LI
12.
a state of excretion: a large quantity of mitochondriae
7351,
is revealed which has a thread-like and granule-like
form; small vacuoles are located among the mitochondriae;
the nucleus is in a basal position (fig. 19-1.).
An increased production of ribonucleic acid in the
chloride-secreting cells is revealed after 6 and 12 hours
of the salt influence, that is, precisely in that period
when the reorganization of these cells into the excretory
state takes place.
The state of the chloride-secreting cells in the
beluga sturgeon juveniles with an injection of sodium
chloride.
The chloride-secreting cells, 24 hours after an
injection of a 10% solution of sodium chloride, show signs
of the excretory state which appears with a large quantity 736*
of mitochondriae of thread-like and granule-like form,
uniformly distributed throughout all the cytoplasm, with the
^basal position of the nucleus. and with mainly small vacuoles
among the mitochondriae.
The large_àpical vacuoler.qharactèristic
of the excretory state of the chloride-secreting cells in
osseous fish, is rarely found. The nucleus can have bay-shaped
depressions, adjacent to which is the vacuole located close to
the nucleus (fig. 1, 8).
The height of the cells on the average is 14.3 microns
(with variations from 11.2 to 18.7 microns), the average width
of the cells is 7.2 microns (with variations from 5.0 to 8.7
microns).
Their number in the histological section with a
13.
thickness of 5 microns between the two respiratory plates
736*
is from two to seven. The number of reserve cells can be
up to ten. Their height on the average is 9.4 microns (with
variations from 7.5 to 12.5 microns), the average width is
8.0 microns (with variations from 6.2 to 11.2 microns).
When analysing the state of the chloride-secreting
cells 1 and 3 hours after an injection of sodium chloride,
attention is drawn to.the fact that the mitochondriae have
a spherical shape and have increased in size just as in the
initial period of the ;external salt influence. Howevert the
mitochondriae are distributed uniformly throughout all the
cytoplasm and are not concentrated in the apical part of the
cell, as is observed with the external salt influence.
Apparently, the spherical shape of the mitochondriae is
connected with their swelling and can be seen as the initial
reaction to the stress influence, i.ri this case, the salt
influence (Sjostrand, 1955).
It is possible to see individual vacuoles among the
mitochondriae.
basally.
The nucleus of spherical form is located
6 hours after a salt injection the spherical shape
of the mitochondriae is retained for the most part. In addition,
excretory vacuoles are found in such cells. 24 hours after an
injection of sodium chloride the cells with spherical mitochondriae become individuals.
Essentially all'-the chloride-
secreting cells have transferred to the excretory state.
14.
The state of the chloride-secreting cells with
736*
an injection of a 15% solution of mannitol. 3 and 24
hours after the introduction of a solution of mannitol,
traits characteristic of the excretory state were revealed
in the chloride-secreting cells.
A large quantity of mito-
chondriae was formed in these cells which gave a dark colour
to the cell on the photograph.
The mitochondriae were
uniformly distributed in the cytoplasm, often with the
exception of the apical part of the cell which has a small
depression.
Vacuoles are revealed among the mitochondriae4
The nucleus with the spherical form is located basally and
can have a bay-shaped depression (fig. 1, e).
DISCUSSION
An injection of a . sodium chloride solution causes the
same kind of changes in the state of the chloride-secreting
cells of tilapia and beluga sturgeon juveniles as the external
salt influence. In both cases the cells transfer to the
excretory state which is characterised by general traits:
the formation in the cytoplasm of a large number of mitochondriae,
the appearance of vacuoles, the basal position of the nucleus
and the formation of bay-shaped depressions in the nucleus.
In the eXporiments with tilapia with a tsa.ltload
created both by the external salt influence (after 24 hours)
and by
the intramuscular injection of sodium chloride (after
15.
• 3
hours) an increased production of ribonucleic acid in
736*
the chloride-secreting cells was observed. In the beluga
sturgeon juveniles which were in salt water o this increased
production of ribonucleic acid was observed precisely in
of
'the period/the reorganization of the chondriome of the chloridesecreting cells and their transfer to the excretory state
(6 and 12 hours aftei" the beginning of the salt influence), in
the period of the increase in the number of mitochondriae
which determine
the increase in the functional activity of 737*
these cells with a salt load.
A significant change in the sizes of the chloridesecreting cells with a salt load was not obsrved either in
the tests with beluga sturgeon juveniles or in the tests with
tilapia (in all probability, because of the short duration of
the test - 24 hours);
In the long adaptation of the tilapia
juveniles to the high concentrationsof saltsa significant
increase in the sizes of the chloride-secreting cells was
recorded ealier(Krayushkina, 19676).
The transfer of the chloride-secreting cells with an
injection of sodium chloride to the excretory state indicates
the fact that the external salt influence cannot be considered
as the main stimulus,which stimulates the beginning of the
activity of these cells. Precisely the increase in the blood
plasma depression in the beluga sturgeon juveniles, caused by
the introduction of sodium chloride with an injection or its
16.
entrance into the blood with the external salt load,
737*
stimulates the excretory activity of the se cells.
The test with the introduction of non-electrolytemannitol shows that in this case the increase in the osmolity
of the'blood plasma plays a role, and not the increase in
the ion concentration in the blood. Since the chloridesecreting cells are adapted for the active removal of sodium
ions (and the passive removal of chlorine), then the increase
in the osmolity of the blood, because of the non-electrolyte,
was the stimulator of the activity of the chloride-secreting
cells in our experiments. As a result, the removal of the
sodium ions.was begun which led to the decrease in the blood
plasma depression lower than the initial level, since the
process of the non-electrolyte discharge occurred simultaneously
with the urine. Actually, in a mannitol medium, poor in sodium,
in isotonic sea water, according to the data of Natochin (1965),
a decrease occurs in the content of sodium ions and chlorine in
the blood in sea mackerel, which leads to the desalinization of
the animal. In this respect our facts agree with the data quoted
above and confirm the specificity of the activity of the
chloride-secreting cells.
17.
Fig.
1.
733*
Chloride-secreting cells of a tilapia and
a beluga sturgeon juvenile.
i
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e
PI1C. 1. X.tiopri10ettpeTupy1Otque R.-tertett ntrinatta n t0.30,q11 60.13,111.
C — xanpueceDperupyroutan itaerDa (xa) mamma. an xan-nracelcn D npecncil noie. •
punie WU:TIM; 6 — miDpispacDpenipylottnet n.lema TUDDITM1 n DlIcspeToimicpx cocronana nepea 3 qaca nocac Du -benturt NaCI,
— an tuc a DeAta
131
noas;* — xaornutcer.peruppautart ItDD-rna Ito:matt 6enTra, u1aXcuumeflçuu D apec.
non BOIC; e -- TO me noene IICIXOHCDCIDIVI ru regenne ‘iae. D aQ,ze. conenocrhyD
TO MO •ePC3 24 yea DOWD mrtemant NaCl; e — TO me ,:rDpea
2; naca uocne uuiruenurcut MallnItTa. Otsiteauttrt no Illanant, oupacita nceaeautlx
remaroncutuutox rio re0D.earaility. 00. 90x, cat. 10 X.
a chloride-secreting cell 00( ) of a tilapia
which was in fresh water, pK - reserve cells;
2,
6 - a chloride-secreting cell of a tilapia in the
excretory state 3 hours after an injection
of NaC1, at- - apical vacuole;
a chloride-secreting cell of a beluga sturgeon
ir
3.
juvenile which was in fresh water;
4.
- the same after being in water with 12,2-12,5%
salinity for 24 hours;
5.
- the same 24 hours after an injection of NaCl;
6,
e - the sanie 24 hours after an injection of mannitol.
The fixing was by the Shampi method, coloured by ferric
haematoxylin according to Heidenhein•objective 90.x,
eye.piece 10X.
0.
-
-
The changes in the blood plasma depresn ion
in beluga sturgeon juveniles under
different influences.
0.70
0.50
0.50
1
J
6
12
Zed
Pnc, 2. Itamenermn Aenpeccrin tria3mm
EpoBn moao,Iti 6eayrn
npit paaaugaux nouericrDnnx.
no «u a6cnuee
upema coneanro nonnenernsin (13 nac.); no ou op&u , ■ cni —
Ecawutua T041:1( namounaunn nanam.m RpC.UI (Cirpnttarelblialt Temnepanpa
• C)..1 — aneiniwe ci).1elme n0.3eititTnne (cOaelIC-rib auaw. 12.2 - 1 -2
11111sCI:Ulin 10
- ro phcTnupa Nn CI; 3 —14.1:11ild 15
-1'() p3CiDirp4
On the X-axis - the time of the sait influerum. (in h ,
On the Y-axis - the freezing points of the blood plaumn
(negative temperature in ° C);
1 -
external salt influence (salinity of the water
12.2-12.5%D);
2 -
an injection of 10% NaC1 solutions
3 - an injection of
15%
mannitol solution.
19.
The change in the blood plasma depression
of beluga sturgeon juveniles
735^
under different influences.
113N;euciwa Aenpeccuu naa:,au.t xponn >1a7o311 Geayni Dpu paa1u'iuwx 1103peücru11az
^^n:pcecua n.ia^^iw ^;poou le '^/ npu paxu:vnuu npeueun nw^eneruun
(u yaa.)
(
Dapnaur
1
3 colop;Kauue B ycao111ws coicnncrn
(1°_.3-1°_.5'.'00)
41)nLCKI(11n 1U"o-ro pacTuopa MC1
3
I
G
-0.71 (3)
-0.65(4)
5,11 ubeuumi W",^-ro pacroopa Mauuura
-0.70 (8)
-0.61 (5)
-0.54 (5)
II p u a1 e a a a u c. D r.onrpo^e (o npanwil soae) nenpeccun pauua -o.r,i0 (cpeauoe xa 10 onpeL^
^eaelmn). D ra6anue npnueacu^ ci-canne ne:urwu^: n cuu6nai yuaaeaw tmcno o^^l,eac,e^wn.
1. Variant.
2. Blood plasma depression (in °C) at different
times of influence (in hours).
3. Content in salinity conditions (12-2-12-5%,))4. An injection of 10% NaCl solution.
5. An injection of 15% mannitol solution.
In the control (in fresh water) the
6. ''Nôtè-.
depression equals -0.61° (the average of 10
Quoted in the table are the average
tests).
values; the nurr(ber of -tests is shown in brackets.
V
20.
737*
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Sent for publication
28.XII.197 0