J. exp. mar. Biol. Ecol., 1919, Vol. 40, pp. 167-181
0 Elsevier/North-Holland
Biomedical Press
THE EFFECTS OF FLUCTUATING SALINITY ON THE PHYSIOLOGY
OF MODIOLUS
DEMISSUS
(Dillwpt)
SANDRA E. SHUMWAY’S*
N.E.R.C.
Unit of Marine Invertebrate
Biology, Marine Science Laboratories,
Wales, U.K.
Menai Bridge, Gwynedd,
and
ARTHUR
N.E.R.C.
Institute
YOUNGSON
of Marine Biochemistry,
St FittickS
Road, Aberdeen,
Scotland
Abstract: Specimens of the Atlantic ribbed mussel, Modiolus demissus (Dillwyn), were exposed to both
gradual (sinusoidal) and abrupt (square wave) salinity fluctuations during which changes in haemolymph osmolality, Na+ , K+ , Ca*+ , M?’ , tissue water content, shell valve movements, oxygen uptake,
and adductor muscle free amino acids (FAA) were measured.
Shell valve closure was found to occur when the external sea-water concentration reached R 60% sea
water. The haemolymph osmolality, Na+, K+, Ca*+, M?’
concentrations followed those of the
external medium as long as the animals’ shell valves remained open. There were no changes in haemolymph ionic or osmotic concentrations during periods of shell valve closure. Total tissue water varied
inversely with salinity change reaching a maximum of ~82% in wedged-open animals exposed to an
abrupt salinity change. During exposure to decreasing salinities the adductor muscle FAA pool decreased; after shell valve closure the concentration increased, primarily due to an increase of alanine
and glycine. Oxygen consumption by M. demissus in air saturated sea water was found to vary with
body weight according to the equation:
oxygen consumption = 0.295 dry weight0-670.
Oxygen consumption during declining oxygen tensions was found to be directly dependent on the
environmental oxygen concentration. The rate of oxygen consumption during exposure to fluctuating
salinities remained constant as long as the shell valves remained open.
INTRODUCTION
The ribbed mussel, Modiolus demissus (Dillwyn), is a common inhabitant of the
upper intertidal zone of salt marshes and as such is subjected to wide variation in
environmental conditions including salinity and oxygen availability. The mussel has
an impressive salinity range of at least 70yW (Lent, 1969) and has been shown to
tolerate low oxygen tensions (Booth & Mangum, 1978).
Pierce (1970, 1971a,b), Bartberger & Pierce (1976), Baginski & Pierce (1973,
and Lent (1969) have studied osmotic and volume control in salinity stressed
M. demissus under steady-state conditions; recent evidence has, however, been
’ Present address: Portobello Marine Laboratory, P.O. Box 8, Portobello, New Zealand.
* Address for reprints: 71 Clifford St., Taunton, MA 02780, U.S.A.
167
168
SAND~AE.SHUMWAYANDARTHURY~UN~SON
presented by Shumway et al. (1977) to suggest that species living in constantly fluctuating environments do not continually conform to the conditions of the external
medium but instead maintain their tissue water and free amino-acid levels at some
intermediate level.
Respiration in intact M. demissus has been investigated with regard to oxygen
uptake and transport (Booth & Mangum, 1978) and size and temperature (Read,
1962; Kuenzler, 1961) but not with respect to salinity. Van Winkle (1968), however,
has studied the effects of salinity on oxygen consumption in excised gills on M. demisSUS.
In view of the already existing steady-state data it seemed interesting to examine
certain aspects of the physiology of M. demissus during exposure to fluctuating
salinities and to compare these results with those obtained from steady-state experiments. In this paper we present experiments on the effects of fluctuating salinities on
osmotic control and respiration in M. dem~ssus.
MATERIALSANDMETHODS
Ribbed mussels, M. demissus, were collected from the Tiverton basin of the Sakonnet River (Rhode Island, U.S.A.), placed in insulated containers, and flown to
Great Britain. The mussels were then kept in Menai Strait sea water (S % 33.5%, =
100% sea water) at 15 “C for at least two weeks prior to use. All experiments were
carried out at 15 “C.
The apparatus used to produce fluctuating salinities has been described by Davenport et nE.(1975). The mussels were exposed to both gradual (sinusoidal) and abrupt
(square wave) salinity changes (see Figs 1 and 4). Maximum sea-water concentration
was 100%; minimum sea-water concentration was 30%. Both normal and wedgedopen specimens were used. Samples of haemolymph and adductor muscle were
collected hourly for osmotic, ionic, tissue water, and free amino-acid (FAA) determinations. The methods of analyses have all been described in detail previously
(Shumway, 1977a,b; Shumway et al. 1977).
Oxygen consumption under constant salinity conditions was measured using a
Radiometer oxygen electrode as described by Crisp et al. (1978). Results are expressed as ml 0, consumed. h-’ . animal-‘. Experiments were run until the animals
had ceased aerobic respiration and hourly readings were plotted at decreasing tensions created by the respiration of the animals in the sealed containers. It has been
shown (Taylor & Brand, 1975) that oxygen consumption rates recorded using a
closed chamber technique were unaffected by metabolite accumulation in the bivalve
Arctica islundica. Oxygen consumption during fluctuating salinities was again monitored using a Radiometer electrode in the system described previously (Shumway,
1978a,b).
Shell movements were monitored during fluctuating salinities by the use of
SALINITY
strain
gauges.
chamber.
paper
OF MODIOLUS
THE PHYSIOLOGY
DEMZSSUS
One valve of a mussel was glued to the bottom
A paper
gauge. The gauge resistance
were displayed
changes.
on a Smith’s servoscribe
169
of the experimental
clip was glued to the free valve and a string
clip to the strain
movements,
AND
attached
reflecting
from the
shell valve
chart recorder.
RESULTS
CHANGES
IN INORGANIC
IONS AND
FREE
AMINO-ACID
CONCENTRATIONS
Table I shows the Na+, Mg’+, K’ and osmotic concentrations
of Menai Strait
sea water and the haemolymph
of Modiolus demissus. The haemolymph
is ionic but
slightly hyperosmotic
to the ambient sea water under steady-state conditions.
TABLE
Na+,
Ca’+,
I
Mg’+, K+ and osmolality of Modioh dew&us haemolymph
and Menai
values for the sea water taken from Shumway (1977a); figures ~s.D.
Na+
Ca’ +
Mg”+
K+
(mM)
(mM)
(mM)
(mM)
465 + 7
471&3
10.0 * 0.4
10.7 & 0.4
52.1 & 1.0
54.3 f 1.1
9.8 f 0.6
11.1 kO.5
Osmolality
(mOsm/kg H,O)
Sea water, Menai Strait
M. demissus
965 + 5
988 k 8
Strait sea water:
TABLE
II
Times of shell valve opening and closure and approximate
sea-water concentrations
(% sea water)
Modiolus demissus during exposure to 30% sea-water minimum sinusoidal salinity programme.
Opening
Closure
Time of valve movement
Sea-water concentration
(h + min)
(%)
03.15 * 15
60
09.16 & 13
60
Closure
15.38 * 14
65
in
Opening
21.04 f 18
60
Figs 1 and 2 show the changes in haemolymph
osmolality,
ionic concentration,
tissue water content and activity of M. demissus during exposure to 30% sea water
minimum
gradual
and abrupt
salinity
fluctuations,
and Table
II shows
the times
and approximate
sea-water concentrations
of shell valve opening and closure during
exposure to the same salinity fluctuations.
The exact sea-water concentration
at
which shell valve closure occurs in the abrupt profile could not be determined
due
to the rapidity of the salinity decrease (3 min from 100 to 30% sea water). It can be
seen from Figs 1 and 2 that the osmotic and ionic concentration
of the haemolymph
of normal mussels closely followed those of the external medium as long as the shell
valves remained open. After the valves had closed the haemolymph
osmotic and
ionic concentrations
remained constant until the valves were re-opened.
Valve clo-
SANDRA
170
E. SHUMWAY
AND
ARTHUR
YOUNGSON
loot
h
e
;;
%
i
.r ..;.: :.
.,
30”:
:
..,
o
b
:.
:y:;:,
:.
. . ...”
;.;I ;.,
:
:.
jj, :. 1.
o : :,I:?; :I..
:: ‘. ‘.
,.,: .;;’
;,
,;.:
: ..
:
,,. :
0-
OT
6or
2
8
01
0
t 80
i=
’
’
’
’
12
Hours
’
’
’
a
24
24
7oOU
Hours
Fig. 1. Changes in haemolymph
osmolality (mOsm) and Na+, K+, Ca*+ and Mg*+ concentrations
(mM)
in normal (0) and wedged-open (0) M. demissus during exposure to a 30% sea-water minimum sinusoidal
salinity regime with changes in total tissue water and ‘A time open: stippled areas represent changes
in the external medium; each point is a mean of four animals; error bars representing
95% confidence
limits are smaller than the actual points.
SALINITY
AND THE PHYSIOLOGY
OF MODIOLUS
DEMISSUS
500
T
f
2
350
12
3
E
80
701
0
Hours
’
’
’
’
12
’
’
’
‘
24
Hours
Fig. 2. Changes in haemolymph
osmolality
(mOsm) and Nat,
K+, Ca*+ and Mg*+ concentrations
(mM) in normal (0) and wedged-open
(0) M. demissus during exposure to a 30% sea-water minimum
square wave salinity regime with changes in total tissue water and oA time open: stippled areas represent
changes in the external medium; each point is a mean of four animals;
error bars representing
95%
confidence limits are smaller than the actual points.
Total
ARG
TAU
ASP
THR
SER
GLU
PRO
GLY
ALA
VAL
MET
1 LEU
LEU
TYR
PHE
____-
NH3
LYS
HIS
Amino
acid
--.-
Free amino-acid
435.14
12.65
303.42
0.94
1.45
1.37
_
21.74
5.55
0.62
0.38
0.20
0.92
0.32
4.68
2.74
0.11
0.12
0.08
0.12
0.08
0.04
513.76
0.90
1.39
3.28
0.14
13.35
446.13
1.51
2.08
3.77
0.85
18.52
408.45
0.91
1.39
2.62
0.14
3.36
0.98
10.90
13.69
118.85
1.97
11.64
6.56
14.10
12.46
81.97
124.59
1.72
0.34
0.12
4.16
0.12
4.13
0.49
0.24
0.34
0.90
0.44
5.00
1.92
0.08
0.04
0.06
0.06
0.08
_
5.19
1.13
18.87
14.72
118.87
2.64
18.68
7.55
14.33
12.26
95.28
126.42
1.98
_
4.51
0.98
14.59
15.49
135.24
1.56
15.08
9.92
16.15
16.15
156.39
119.67
1.72
_
0.28
0‘10
5.40
0.24
0.12
3.40
0.12
2.77
0.34
0.22
0.25
0.61
0.32
3.26
1.34
0.08
0.04
0.06
0.06
0.08
0.04
2.91
1.02
21.88
8.55
88.03
1.20
6.07
2.65
10.34
5.56
57.09
93.16
1.20
_
0.18
0.07
3.21
0.24
3.11
0.38
0.30
0.22
0.32
0.22
3.06
1.02
0.08
0.06
0.06
0.06
0.08
0.04
5.82
2.81
10.20
18.17
133.33
11.31
26.21
9.35
10.26
14.18
92.81
88.89
1.83
1.11
1.37
2.16
3.66
1.70
Tissue
Haem.
Tissue
Hour
Haem.
6
Tissue
Hour
Haem.
Tissue
Hour 4
h
Haem.
2
03.1.5-09.16
Closed
@M.
20.52
0.58
0.23
5.60
0.12
3.96
0.44
0.68
0.69
1.46
0.76
2.92
2.28
0.15
0.06
0.14
0.20
0.21
0.04
Haem.
8
dry wt tissue-‘)
and haemolymph
sinusoidal salinity profile.
Tissue
Hour
in the adductor
muscle &M.g
30% sea-water minimum
___~
Hour 0
o--03.15 h
Open
concentrations
III
-
-..
and ammonia
TABLE
415.42
0.95
1.03
1.47
4.9 1
0.60
7.16
10.26
122.41
7.59
10.00
4.22
19.22
9.40
84.74
130.17
1.29
-
Tissue
Hour
ml-‘)
10.35
0.24
0.08
2.74
0.06
2.09
0.47
0.17
0.23
0.50
0.32
1.68
1.51
0.04
0.02
0.06
0.06
0.04
0.04
Haem.
10
Hour
436.57
0.98
1.07
2.32
_
3.84
0.62
14.91
10.62
124.11
4.64
10.80
6.07
16.96
9.73
105.35
123.21
1.34
Tissue
09.16 h
Open
12
to a
10.31
0.14
0.08
2.32
0.06
2.44
0.47
0.17
0.18
0.31
0.22
2.50
1.20
0.04
0.02
0.03
0.06
0.04
0.04
Haem.
of M. demissus exposed
SALINITY
AND THE PHYSIOLOGY
OF ~O~IOLU~
DEMISSUS
173
sure and opening occurred at similar salinity values during the second cycle of the
salinity protile and the haemolymph concentrations again remained constant during closure.
Experiments with wedged-open animals showed a time lag in their response to
salinity change. During exposure to the sinusoidal profile the haemolymph osmolality
fell to 548 mOsm during the first cycle and 540 mOsm during the second cycle. The
minimum haemolymph concentrations were similar during exposure to the square
wave salinity profile, reaching a low of 530 mOsm during the first cycle and 525 mOsm
during the second cycle.
In all cases, the haemolymph ion concentrations closely foltowed the total osmotic
concentration of the haemolymph. There was no evidence of regulation of any of
the ionic species studied; the Ca2+ and Mg2+ ions, however, showed a damped
response to reduced salinity. K+ ions showed the least change during exposure to
low salinities, reaching a minimum of 9.1 mM in abrupt regime and 8.4 mM in
gradual regime.
As might be anticipated, normal and wedged-open M. demissus showed changes
in their tissue water content in both the gradual and abrupt salinity profiles. The
TABLE IV
Changes
&Pvl. g dry wt tissue-t)
Shell valves
Hours
Tissue
Total
NH3
FAA
AFAA
Taurine
ATau
Alanine
AAla
Glycine
AGly
Haemolymph
Total
NH,
FAA
AFAA
Taurine
ATau
Alanine
A Ala
GIycine
AGly
in total free amino acids and ammonia
Open
0
435. I
10.2
424.9
133.3
88.9
92.8
12.65
3.21
9.44
3.11
1.02
3.06
concentrations.
Closed
Open
2
4
6
8
10
12
303.4
21.9
281.5
- 143.4
88.0
-45.3
93.2
+4.3
57.1
-35.7
513.8
14.6
499.2
+211.7
135.2
+ 47.2
119.7
+ 26.5
156.4
+99.3
446.1
18.9
421.2
-72.0
118.9
- 16.3
126.4
+6.7
95.3
-61.1
408.4
10.9
397.5
-29.7
118.8
-0.1
124.6
-1.8
82.0
- 13.3
415.4
7.2
408.2
- 10.7
122.4
+ 3.6
130.2
+5.6
84.7
i-2.7
436.4
14.9
421.7
- 13.5
124. I
+ 1.7
123.2
-7.0
105.4
+ 20.7
21.74
5.40
16.34
+ 6.90
5.55
+ 2.44
2.74
+ 1.72
4.68
+ I.62
13.35
3.40
9.95
-6.39
2.77
-2.78
1.34
- I.40
3.26
- 1.42
18.52
4.16
14.36
+ 4.41
4.13
+ 1.36
1.92
+ 0.58
5.00
+ 1.74
20.52
5.60
14.92
+0.56
3.96
-0.17
2.28
+ 0.33
2.92
-2.08
10.35
2.74
7.61
-7.31
2.09
- 1.87
1.51
-0.77
1.68
- I.24
10.31
2.32
7.99
+ 0.38
2.44
+ 0.35
1.20
-0.31
2.50
+ 0.82
174
SANDRA
E. SHUMWAY
AND ARTHUR
YOUNGSON
hydration levels of wedged-open animals exposed to the abrupt profile showed
greater changes than did the levels in animals exposed to the gradual profile. There
was a significant difference between the tissue water level of normal and wedgedopen animals, wedged-open animals showing the higher degree of swelling.
Table III shows the changes in adductor muscle and haemolymph free aminoacid concentrations and ammonia during the first 12 h of exposure to a 30% seawater minimum sinusoidal salinity regime, and Table IV summarizes these changes.
Quantitatively the most important amino acids in the adductor muscle (in alphabetical order) were alanine, arginine, glycine, taurine, and threonine. In addition,
aspartic acid, glutamic acid, proline, and serine made up a significant portion of
the FAA pool of the adductor muscle. Glycine, alanine, and taurine comprised
x 60% of the FAA pool of the haemolymph.
During the first two hours of exposure to decreasing salinities, while the animals’
tissues were still exposed to the external environment, there was a decrease in the
FAA concentration in the adductor muscle and a slight increase in the FAA concentration of the haemolymph. After closure of the shell valves, there was an initial
increase, followed by a gradual decrease in the FAA pool of the adductor muscle.
FAA concentration in the adductor muscle returned to the control value by Hour
12. FAA levels of the haemolymph increased slightly during the initial decrease in
salinity but after shell valve closure decreased initially and then continued to increase until the shell valves re-opened but did not return to the control value.
OXYGEN
CONSUMPTION
IN RELATION
TO SIZE, P,, AND SALINITY
Fig. 3 shows the relationship between oxygen consumption in air saturated sea
water and dry body weight for M. demissus. The results have been fitted to the
equation :
oxygen consumption = a dry weighth,
oxygen consumption = 0.295 dry weight0.670,
(correlation coefficient = 0.968 for 39 D.F.).
Fig. 4 shows the results of five individual experiments in which oxygen consumption was related to oxygen concentration. It would appear from these curves that the
rate of oxygen consumption was directly dependent on the environmental oxygen
concentration ; however, Tang (1933) and Bayne (197 1) have shown that respiratory
dependence cannot be determined by simple inspection. When the oxygen tension
(Po,) is divided by the weight specific oxygen consumption (Q,,) and this result plotted against P,, the line relating PO, to Qo2 becomes linear, this straight line has an intercept (K,) and a slope (KJ which Bayne (1971) showed could be used to determine
an oxygen independence index, K,IK,. The lower the value KJK,, the greater the
capacity to regulate oxygen consumption. The mean K,/K, value for ten animals
(dry wt 1.01 + 0.08) was 26.38.
Oxygen
consumption
(ml 0, h-’ g dry
w t-’ )
2
.O a
0
9
I
1
,
11,111
Oxygen
0
‘d
uptake
I
1
1111111
(ml h-l)
6
SANDRA
176
E. SHUMWAY
AND ARTHUR
YOUNGSON
It has also been shown (Bayne, 1971; Taylor & Brand, 1975) that other bivalves
show an increase in their degree of oxygen independence with increasing size. Table
V gives the equations for the oxygen dependence indices for M. demissus and those
of live other species of bivalves. The results obtained for M. demissus are very
similar to those for ~~v~~~useduces (Bayne, 1971). All mussels continued to extract
oxygen until the external concentration had reached z 10% saturation at which time
two of the animals ceased to respire aerobically; the other three mussels, however,
continued to extract oxygen until the oxygen supply was completely depleted.
The oxygen consumption of ~odio~~s demissus exposed to gradual and abrupt
salinity changes is shown in Fig. 5. As long as the shell valves remained open the
TABLE V
The regression
Species
equations
for the oxygen-dependence
index, K,/Kz, against
consumption,
Qo..
Number of
determinations
Regression
equation
K,/K2 =
the weight
3.ggQ,,;:;:;
KIIK, =
6.46Q020~93,j
4lK2
=
62.7lQ0~~,~,~
K,lKz = 75.50(20,,~~~~
K,/K2 = 500.00Q02
10
7
10
10
10
specific
oxygen
Source
Bayne (1973)
Bayne (1973)
Present study
Bayne (1971)’
Bayne (1971)’
’ This value is reported as 15.5Q020~s’8; this is a misprint (Bayne, pets. comm.) the true value being
75.5Q0z0s?
’ This value is reported as 19.0Qoz ‘.“‘; inspection of Fig. 6 (Bayne, 1971) reveals that the value of the
coefficient is not 19.0 but nearer 500.
Hours
Fig. 5. Oxygen consumption
by M. demiscus during exposure to 3O’:a sea-water minimum sinusoidal
salinity regime (upper), and 307; sea-water
minimunl
square wave salinity regime (lower): stippled
areas represent changes in the external medium; each point is a mean of six animals; error bars represent
95% confidence limits; arrows indicate points of shell valve opening and closure.
SALINITYAND THE PHYSIOLOGYOF MODIOLUS
DEkfISSUS
177
rate of oxygen consumption was constant but, not surprisingly, ceased entirely during
periods of shell valve closure. There was no significant ‘overshoot’ upon re-opening
in higher sea-water concentrations to indicate any appreciable oxygen debt.
DISCUSSION
OSMOTICAND IONIC COMPOSITION
The results reported here are almost identical to those previously reported for
M. modiolus, Mytilus edulis, and Crassostrea gigas (Shumway, 1977a), in that as
long as the shell valves remain open the osmotic concentrations of the haemolymph
follow the same pattern of change as that of the external medium. There was no
evidence of ionic regulation for any of the ions studied; even in wedged-open
animals, however, K+ concentrations showed only small fluctuations compared
with the magnitude of change of the external medium. When placed in dilute sea
water, Myths edulis and Glycmeris glycmeris are known to regulate K+ ions to
maintain the concentrations at the value it has in the haemolymph of normal seawater animals (Gilles, 1972). Hand & Stickle (1977) found that haemolymph K+ did
not follow the K’ concentration of ambient sea water as closely as did other ions in
Crassostrea virginica during salinity fluctuations. In addition, they found that K+
is hyper-ionic to ambient sea water at 10, 15, and 2Oy&,5’. It is still not known what
role, if any, this regulation plays in the osmoregulation process (Gilles, 1972).
TISSUEWATER
Again, the results reported
here are similar to those reported previously for
1977b). Wedged-open animals
showed significantly higher hydration levels in dilute water than normal animals in
both the sinusoidal and square-wave regimes. In neither regime was there evidence
for overshoot of the original tissue water content to indicate volume regulation by
solute extrusion. In an extensive study on volume regulation in marine bivalves
exposed to constantly lowered salinity, Pierce (1971a, b) found that Modiolus demissus regulates its cellular volume in dilute sea water by solute extrusion but also
points out that volume regulation appears as a “desperation response” when after
a period of shell valve closure the animal is forced to interact with the external
environment. Like many other marine and estuarine bivalves M. demissus relies
primarily on shell valve closure for temporary protection from dilute external media.
Mytilus edulis and Crassostrea gigas (Shumway,
FREE AMINO-ACIDPOOL
The changes in the FAA pool of M. demissus adductor muscle, during the first
12 h of exposure to fluctuating salinities, are shown in Table III and summarized
in Table IV. It is generally accepted that marine invertebrates utilize free amino
SANDRA
178
acids as one source
E. SHUMWAY
of solute
AND ARTHUR
for cell volume
term salinity stress (for reviews see Florkin
1975; Schoffeniels,
YOUNGSON
regulation
& Schoffeniels,
1976). It has been shown,
however,
during
exposure
1969; Lange,
to long-
1972 ; Gilles,
that free amino
acids are
probably not used for the same purposes in animals exposed to cyclic salinity changes
(Shumway et al., 1977). Livingstone
et al. (1979) have shown that long-term changes
in ninhydrin-positive
substances
(NPS) in Myths edulis represent
an adaptive
response to fluctuating
salinity. The animals used by Livingstone
et al. (1979) were
open throughout
the salinity cycle, whereas in the study of Shumway et al. (1977)
there was shell valve closure as a result of decreased salinity. This combination
of
decreased salinity and shell valve closure makes interpretation
of FAA levels solely
in terms of salinity adaptation
difficult. It was found in this study that the nonessential amino acids - alanine, glycine, and taurine accounted
for the greatest
changes in the total FAA pool during salinity fluctuations.
The concentration
of
the FAA pool of the adductor muscle decreased by 30% during the first two hours
of the salinity cycle but by one hour after shell valve closure the concentration
had increased to 514pM g. dry wt-‘. Excluding taurine, z 60% of this increase may
be accounted
for by the increase in glycine. This is in agreement with a previous
study on the effects of fluctuating
salinities on the concentration
of FAA in bivalves
in which glycine was found to accumulate
during salinity-induced
shell valve closure
in M. edulis, Crassostrea gigas, Mercenaria mercenaria and Modiolus modiolus
(Shumway et al., 1977) and the issue is discussed in detail in that paper.
It has been shown by Pierce & Greenberg
(1972) that in bivalves exposed to low
salinities, free amino acids are extruded across the cell membranes,
and Bartberger
& Pierce (1976) showed that during low salinity acclimation
in M. demissus free
amino acids are released intact from the cells into the haemolymph
and subsequently degraded elsewhere. In the present study a slight initial increase in haemolymph FAA was found and Hand & Stickle (1977) found pericardial
fluid NPS to
increase from 3 mM to 4.8 mM during
the increase noted in the present study
the decrease in tissue FAA, e.g. whereas
435 FM. g dry wt-’ to 303 PM. g dry
lymph
a 20-l&20%,
S diurnal cycle. At first glance
does not appear large enough to account for
the tissue FAA concentration
decreased from
wt-’ (132 FM), the total increase in haemo-
FAA was a mere 9 ~1M ; one must, however,
to ambient
sea water
haemolymph.
in order
to evaluate
know the rate of efflux of FAA
the significance
of this increase
in
RESPIRATION
Oxygen consumption
in M. demissus was found to vary with the 0.67 power of
body weight. This would appear to signify that oxygen consumption
is proportional
to surface area in M. demissus; however, the biological significance of ‘b’ the (weight
exponent) is not at all clear and has recently come under speculation
(Zeuthen, 1947,
1953; Hemmingsen,
1950, 1960; von Bertalanffy,
1957; Widdows, 1978). Newell &
SALINITY
AND
THE PHYSIOLOGY
OF MODIOLUS
179
DEMZSSUS
Roy (1973) suggested that temperature and season may influence the value of b,
and Bayne et al. (1973) recorded different values of b during summer and winter in
Myths edulis. Widdows (1978) has shown that high food levels and high temperatures also alter the weight exponent. Table VI shows the relationships between the
TABLE VI
Some relationships
between the rate of oxygen consumption
and body weight in Modiolus demissus:
a and h are fitted parameters
in the equation
Y = aXh; b’ = b-l; Y = ml 0,. h-’ ; X= g dry flesh wt.
Range of dry
flesh wt
Temperature
Salinity
Number of
observations
(g)
(“C)
(%a)
(n)
a
b
b’
Reference
0.23-I .30
0.25-2.60
0.16-1.00
0.23-3.50
0.30-l .oo
0.40-0.95
0.40-1.30
0.40-1.30
0.40-1.30
0.01-3.00
16
22
28.2
35.2
8
13.5
14.0
20.6
26.5
15
29.7
29.7
29.7
29.7
11
12
12
13
3
3
4
4
4
40
0.466
0.629
1.059
1.225
0.130
0.230
0.260
0.370
0.530
0.295
0.757
0.798
0.787
0.645
0.310
0.620
0.690
0.380
0.410
0.670
- 0.243
-0.202
-0.213
-0.355
- 0.690
-0.380
-0.310
- 0.620
-0.590
-0.330
Read (1962)
Read (1962)
Read ( 1962)
Read (1962)
Kuenzler (1961)
Kuenzler (1961)
Kuenzler (1961)
Kuenzler (1961)
Kuenzler (1961)
Present study
33.5
rate of oxygen consumption and body weight in Modiolus demissus obtained by
three authors. The values for both a and b obtained in .this study are in close
agreement with the values recorded at 14 “C by Kuenzler (1961). Read (1962) reported values for both a and b at 16 “C that are significantly higher than those of
Kuenzler and the present authors. The b values reported by Read at 16, 22, and
28.2 “C are not significantly different from one another, and since similar b values
have been recorded at varying temperatures it seems unlikely that temperature alone
is responsible for the varying a and b values, and it is possible that some other environmental factors such as season or salinity are affecting these values in M. demissus.
The effect of declining oxygen tension on the rate of respiration in M. demissus
is shown in Fig. 4 and Table VI. The animals were found to be partially oxygen
independent, that is the rate of oxygen consumption is independent of the oxygen
concentration of the external medium above a certain critical tension. Having studied
four species of bivalve from different environments Bayne (1973) concluded that
the capacity to regulate oxygen consumption may be correlated with the degree of
hypoxia experienced in the natural environment. Taylor & Brand (1975) supported
this conclusion with a study of Arctica islundicu in which they found that results for
this sublittoral species were similar to those obtained for the sublittoral Luevicurdium.
Modiolus demissus, an intertidal mussel found in similar regions to Myths, shows
almost exactly the same degree of respiratory independence as Myths thus lending
180
SANDRA E. SHUMWAY AND ARTHUR YOUNGSON
further support to Bayne’s conclusion. Booth & Mangum (1978) found Modiolus
they also found, however, that oxygen consumption by M. demissus ceased suddenly at P,, values between 15 and 45 torr (z l&30%
saturation). In the present study two of the experimental animals ceased respiring
at z 7% saturation (z 10 torr) but three other animals continued to extract oxygen
from the external medium until the oxygen supply was completely depleted.
Respiration in M. demissus during exposure to salinity fluctuations is shown in
Fig. 5. In normal animals, as long as the animals’ shell valves remain open, the
respiration rate is constant regardless of salinity but ceases immediately upon shell
valve closure. It is interesting to note that both normal and wedged-open animals
ceased respiring at the same point in the salinity profile. There is no marked increase
in respiration rate upon return to higher sea-water concentration in either normal
or wedged-open mussels to indicate any oxygen debt. This same response to decreased
salinities has been found for both normal and wedged-open Myths edulis exposed
to the same salinity regimes used in this study (Miss J. Bettison, pers. comm.).
demissus to be oxygen dependent;
ACKNOWLEDGEMENTS
The authors wish to thank Professor D. J. Crisp and Dr B. L. Bayne for helpful
discussions, Dr W. B. Stickle for critically reading an earlier version of the manuscript, and Mr B. H. Shumway for collecting the mussels. One of us (S.E.S.) was
under tenure of a fellowship for the Marshall Aid Commemoration Commission.
REFERENCES
BAGINSKI,R. M. & S. K. PIERCE, 1975. Anaerobiosis: a possible source of osmotic solute for high
salinity acclimation in marine molluscs. J. exp. Biol., Vol. 62, pp. 589-598.
BARTBERGER,C. A. & S. K. PIERCE, 1976. Relationship between ammonia excretion rates and hemolymph nitrogenous compounds of a euryhaline bivalve mollusc during low salinity acclimation. Biol.
BUN. mar. biol. Lab., Woo& Hole, Vol. 150, pp. l-14.
BAYNE,B. L., 1971. Oxygen consumption by three species of lamellibranch mollusc in declining ambient oxygen tension. Camp. Biochem. Physiol., Vol. 40A, pp. 955-970.
BAYNE,B. L., 1973. The responses of three species of bivalve mollusc to declining oxygen tension at
reduced salinity. Comp. Biochem. Physiol., Vol. 45A, pp. 793-806.
BAYNE,B. L.. R. J. THOMPSON& J. WIDDOWS,1973. Some effects of temperature and food on the rate
of oxygen consumption by Mytilus edails L. In, Effkrs of’remperarure on ectothermic organisms. edited
by W. Wieser, Springer-Verlag, Berlin, pp. 181-193.
BOOTH,C. E.&C. P. MANGUM,1978. Oxygen uptake and transport in the lamellibranch mollusc Modiolus
demissus. Physiol. Zoiil., Vol. 51, pp. 17-32.
CRISP, M., J. DAVENPORT& S. E. SHUMWAY,1978. Effects of feeding and of chemical stimulation on
the oxygen uptake of Nassarius reticulatus (Gastropoda: Prosobranchia). .I. mar. biol. Ass. U.K.,
Vol. 58, pp. 387-399.
DAVENPORT,
J., Ll. D. GRUFFYDD&A. R. BEAUMONT,1975. An apparatus to supply water of fluctuating
salinity and its use in a study of the salinity tolerances of larvae of the scallop Pecten maximas L.
J. mar. biol. Ass. U.K., Vol. 55, pp. 391409.
FLORKIN,M. & E. SCHOFFENIELS,
1969. Molecular approaches to ecology. Academic Press, New York,
203 pp., (see pp. 89-163).
SALINITY
AND THE PHYSIOLOGY
OF MODIOLUS
DEMISSUS
181
GILLES, R., 1972. Osmoregulation
in three molluscs: Acunthochitonu discrepans (Brown), Glycymeris
glycmeris (L.) and Mytilus edulis (L.). Biol. Bull. mar. hiol. Lab., Woods Hole, Vol. 142, pp. 25-35.
GILLES, R., 1975. Mechanisms
of ion and osmoregulation.
In, Marine ecology, edited by 0. Kinne.
John Wiley & Sons, New York, pp. 259-347.
HAND, S. C. & W. B. STICKLE, 1977. Effects of tidal fluctuations
of salinity on pericardial
fluid composition of the American oyster Crassostrea virginica. Mar. Biol., Vol. 42, pp. 259-271,
HEMMINGSEN,A.. 1950. The relation of standard
(basal) energy metabolism
to total fresh weight of
living organisms. Rep. Steno. meml Hosp.. Vol. 4, pp. 7-58.
HEMMINGSEN, A., 1960. Energy metabolism
as related to body size and respiratory
surfaces and its
evolution. Rep. Steno. meml Hosp., Vol. 9, pp. l-110.
KUENZLER, E. J., 1961. Structure
and energy flow of a mussel population
in a Georgia salt marsh.
Limnol. Oceanogr., Vol. 6, pp. 400-415.
LANGE, R., 1972. Some recent work on osmotic, ionic and volume regulation
in marine animals.
Oceanogr. Mar. Biol. Ann. Rev., Vol. 10, pp. 97-136.
LENT, C. M., 1969. Adaptations
of the ribbed mussel, Modiolus demissus (Dillwyn), to the intertidal
habitat. Am. Zool., Vol. 9, pp. 283-292.
LIVINGSTONE, D. R., J. WIDDOWS & P. FIETH, 1979. Aspects of nitrogen metabolism
of the common
mussel Mytilus edulis: adaptation
to abrupt and fluctuating changes in salinity. Mar. Biol., (in press).
NEWELL, R.C. & A. ROY, 1973. A statistical
model relating the oxygen consumption
of a mollusc
(Littorina lifrorea) to activity, body size and environmental
conditions.
PhJlsiol. Zoiil., Vol. 46, pp.
253-275.
PIERCE, S. K., 1970. The water balance of Modiolus (Mollusca : Bivalvia : Mytilidae):
osmotic concentrations in changing salinities. Comp. Biochem. Physiol., Vol. 36, pp. 521-533.
PIERCE, S.K.? 1971a. A source of solute for volume regulation
in marine mussels. Camp. Biochem.
Physiol., Vol. 38A, pp. 619-635.
PIERCE, S. K., 1971b. Volume regulation
and valve movements
by marine mussels. Comp. Biochem.
Physiol., Vol. 39A, pp. 103-l 17.
PIERCE, S. K. & M. GREENBERG, 1972. The nature of cellular volume regulation
in marine bivalves.
J. exp. Biol., Vol. 57, pp. 681-692.
READ, K. R. H., 1962. Respiration
of the bivalve molluscs Myrilus edulis L. and Branchidonfes demissus
plicatulus Lamarck as a function of size and temperature.
Comp. Biochem. Physiol., Vol. 7, pp. 89-101.
SCHOFFENIELS, E., 1976. Adaptations
with respect to salinity. Biochem. Sot. Symp., Vol. 41, pp. 179-204.
SHUMWAY. S. E., 1977a. The effects of salinity fluctuation
on the osmotic pressure and Na+, Ca*+ and
Mg’+ ion concentration
in the hemolymph
of bivalve molluscs. Mar. Biol., Vol. 41, pp. 153-178.
SHUMWAY, S. E., 1977b. The effects of fluctuating
salinity on the tissue water content of eight species
of bivalve molluscs. J. camp. Physiol., Vol. 116, pp. 269-285.
SHUMWAY, S. E., 1978a. Respiration,
pumping activity and heartrate
in Ciona intestinalis L. exposed
to fluctuating
salinities. Mar. Biol., Vol. 48, pp. 235-242.
SHUMWAY, S. E., 1978b. Activity and respiration
in the anemone,
Merridium senile (L.) exposed to
salinity fluctuations.
J. exp. mar. Biol. Ecol., Vol. 33, pp. 85-92.
SHUMWAY, S. E., P. A. GABBO~T & A. YOUNGSON, 1977. The effect of fluctuating
salinity on the concentrations
of free amino acids and ninhydrin-positive
substances
in the adductor
muscles of eight
species of bivalve molluscs. J. exp. mar. Biol. Ecol., Vol. 29, pp. 131-150.
TANG, P. S., 1933. On the rate of oxygen consumption
by tissues and lower organisms as a function of
oxygen tension. Q. Rev. Biol., Vol. 8, pp. 26&274.
TAYLOR, A. C. & A. R. BRAND, 1975. Effects of hypoxia and body size on the oxygen consumption
of
the bivalve Arctica islundica (L.). J. exp. mar. Biol. Ecol.. Vol. 19, pp. 187-196.
WIDDOWS, J., 1978. Combined effects of body size, food concentration
and season on the physiology of
Mytilus edulis. J. mar. biol. Ass. U.K., Vol. 58, pp. 109-124.
VAN WINKLE, W., 1968. The effects of season, temperature
and salinity on the oxygen consumption
of bivalve gill tissue. Comp. Biochem. Physiol., Vol. 26, pp. 69-80.
VON BERTALANFFY.L., 1957. Quantitative
laws in metabolism
and growth. Q. Rev. Biol., Vol. 32, pp.
217-231.
ZEUTHEN, E., 1947. Body size and metabolic
rate in the animal kingdom,
with special regard to the
marine microfauna.
C.r. True. Lab. Car&berg, SCr. Chim., Vol. 26, pp. 17-161.
ZEUTHEN,E., 1953. Oxygen uptake as related to body size in organisms.
Q. Rev. Biol., Vol. 28, pp. l-12.