The effects of salinity on the physiological ecology of Choromytilus chorus (Molina, 1782) (Bivalvia : Mytilidae)

,I. Exp. Mar. Biol. Ecul., 1988, Vol. 122, pp. I9-33 Elsevier

19

JEM 01132

The effects of salinity on the physiological ecology of ~h~~~~yt~lu~ chu~u~ (~olina, 1782) (Bivalvia: ~ytili~ae) Jorge M. Navarro Centro de Investigaciones Marinas, Vniversidad Austral de Chile, Valdivia, Chile

(Received 27 January 1988; revision received 11 May 1988; accepted 24 June 1988) Abstract: C~urffrn~~ti~u~ chorus frequently occurs in the estuaries of southern Chile, an environment that subjects it to changing ambient salinities. The effect of different salinities on the physiological processes of C. chorus was measured at 15, 1824 and 30x, and at 12 “C. Scope for growth and net growth efficiency were used as physiological stress indices Filtration rate was greater and similar at the two higher salinities (24 and 30%,), decreased at 18%, and was considerably reduced at 15x,. Assimilation efficiency was high ( x 80%) and independent ofboth body weight and salinity. Oxygen uptake was also reduced by low salinity. There were no significant differences between weight exponents or between elevations when standard metabolism was compared at the three higher salinities. However, when the lowest salinity was included in the analysis, significant differences were observed. The energy lost due to excretion was very low at ail salinities. The lowest value obtained at I%!,, was associated with the pronounced valve closure shown at this salinity, resulting in a build up of ammonia in the mantle cavity and body tissue and an inhibition in the production of NH,. Scope for growth in C. chorus of given size was similar between 24 and 30x, salinity and always positive in this range. Low feeding activity and a relatively high metabolic rate at the lower salinities resulted in a negative scope for growth for the larger animals at IS%, and for all the size classes at 157;, salinity. The stress imposed on C. chorus by low salinity was also reflected in a decreased net growth efficiency (KZ). The data suggest that the growth rate as well as the degree to which this species can penetrate estuaries is partially determined by the amount of time which the mussels are able to spend in positive scope for growth under the estuarine conditions of reduced and fluctuating salinities.

Key words: C~or~m~tilus chorus; Physiology; Salinity; Scope for growth

INTRODUCTION

is one of the dominant environmental factors controlling species distribution and influencing physiological processes in marine and estuarine organisms (see reviews by Kinne, 1967,197l; Bayne et al., 1976; Davenport, 1979a,b; Davenport et al,, 1975). Typical responses in bivalves include reduced feeding activity and slower growth at low salinity (e.g., Mytilus edulis; Bohle, 1972; Widdows, 1985a) and also valve closure, e.g., Crassostrea virginica (Hand & Stickle, 1977), Mytilus edulis, Chlamys opercularis, Modiolus modiolus (Shumway, 1977), Anadara senilis (Djangmah et al., 1979). Volume regulation is also affected by changes in salinity, and the ability to regulate body volume Salinity

Correspondence address: 3. M. Navarro, Marine Sciences Research Laboratory, Memorial University of Newfoundland, St. John’s, Newfoundland, AlC 5S7, Canada. 0022-0981/88/$03.50 0 1988 Elsevier Science Publishers B.V. (Biomedical Division)

J. M. NAVARRO

20

appears

to be an important

vertebrates.

A sudden

characteristic

of most estuarine

change in salinity can produce

and some marine

in-

a change in volume that reflects

a disruption in the steady state balance in the influx and efflux of water and salts (Kinne, 1967). Pierce (1971) observed valve closure to be the primary method by which body fluid volume regulation occurs in estuarine bivalves exposed to short-term salinity fluctuations. Davenport (1979b), working with “propped open” mussels, found that M. edulis appears to be a physiological osmoconformer which has behavioural control over its mantle fluid during short term exposure to hypoosmotic stress. Bouxin (1931) exposed Mytilus galloprovincialiswhich were adapted to normal seawater to changes in salinity and found that over a range of 20 to 36z0 there was little change in the rate of oxygen consumption, but with further increases or decreases in salinity oxygen consumption was depressed. Widdows (1985a) observed that when M. edulis is exposed to a fluctuating salinity regime between 20 and 30x,, clearance rate, oxygen uptake and scope for growth (energy balance) are maintained at nearly constant levels, whereas they all decrease at salinities <20%,,. C. chorus frequently occurs in the estuaries of southern Chile, an environment that subjects the mussels to changing ambient salinities over short (tidal) and long (seasonal) cycles. Most studies on this species have been concerned with growth rate in ihe field and population dynamics (Lozada et al., 1971; Norambuena & Solis, 1978) not with the effect of the environmental factors on physiological processes. The physiological response of C. chants to different salinities has not been previously studied under controlled laboratory conditions. The objective of this study was to determine the effect of different salinities on the physiological processes of C. chorus, using the scope for growth as a physiological stress index. In view of the commercial importance of this species and its potential for aquaculture, information on its response to low salinity has implications in the selection of suitable

sites for cultivation. MATERIALS

AND

METHODS

C. chorus (Molina, 1782) were collected by scuba diving in the Queule estuary (39”24’S : 73’ 13’W), where this species occurs in natural beds on a shingle and mud bank. Water temperature on the bottom varied in 1984 between 9.5 “C (July) and 20.8 “C (January) (monthly averages), with an annual mean of 13.9 and 14.3 “C at high tide and low tide, respectively. The salinity varied considerably with tide and season, ranging from 20.0%, (June) to 31.0%, (April) (monthly averages) during high tide with a mean annual value of 25.6%,. During low tide, salinity decreased to between 1.6x,, (July) and 22. lx0 (May) (monthly averages), with a mean annual value of 9.6%,, (unpubl. data, Instituto de Zoologia, Universidad Austral de Chile). The experimental animals were collected during the winter (June-August), the period in which the largest variations in salinity occur due to the rainfall. Six size classes of mussels were selected, ranging in shell length from 19 to 140 mm. Individuals from each

PHYSIOLOGICAL

ECOLOGY

OF C~U~O~Y~~~U~

CHORUS

21

size class were divided into four groups and held at 15, 18, 24 and 30% salinity, respectively. Water temperature was 12 ‘C throughout. Dilutions were made by adding distilled water to seawater. The mussels were maintained under these laboratory conditions for 15 days before the determination of physiological rates. During this acclimation period, seawater was changed every 2 days and the mussels were fed five times a day with ~~n~lieZlQrna~~~ (20 x lo6 cells * 1- ‘). Filtration rate was determined by an indirect method in which the decrease in algal cell density in the experimental aquarium was monitored in relation to time (Winter, 1973). A homogeneous mixture of the experimental medium was maintained by the use of a circulation pump. The experiments were carried out over 24 h in aquaria of 16 1 containing several mussels of similar size from which a single value of filtration rate was calculated for an individu~ mussel. All the experiments were done at 12 “C and at 1.5, 18,24 and 30X salinity. The experiments food concentration was 20 x lo6 D. marina cells .l- ‘, corresponding to 1.07 mg dry wt * 1- *. The average calorific content of D. marina is 19.3 kJ *g- r dry wt and 20.8 kJ *g- ’ AFDW (Buhr, 1976). The effect of salinity on assimilation efficiency was determined by the method of Conover (1966). Feces were collected with micropipets, washed with isotonic ammonium formate, dried to constant weight, ashed and weighed again. Oxygen uptake was measured in experimental chambers by a pol~o~aphic anatyzer. The water in the chamber was mixed by means of an internal circulation pump to provide a steady reading on an oxygen meter (Yellow Springs Instruments). The volume of the respiration chambers varied from 2500 to 4500 ml as appropriate for the size of the group of mussels. Oxygen uptake was determined at three different physiological states; standard (3 days starved), routine (continuous feeding) and postfeeding (immediately after feeding) in relation to body size and at four experimental salinities. Values for oxygen consumption were expressed in ml 0, * h- ’ and transformed to Joules using the conversion factor: 1 ml O2 = 19.9 J. Excretion rate was determined at four experimental salinities. The mussels were placed in 1 to 4 1 of filtered seawater, and one additional beaker containing filtered seawater, but with no animals, served as a control. Following an incubation period of 5 h, samples from the water containing the mussels and from the control were analyzed for ammonia using the method of Solorzano (1969). Values for excretion rate were expressed in pg NH,-N - h- I and transformed to Joules using the conversion factor: 1 mg NH,-N = 24.8 J. Scope for growth (P) was calculated by subtraction of the energy lost in respiration (R) and excretion (U) from the energy absorbed from the food (A), after converting all values to Joules: P = A - (R f U} .

Net growth efliciency (K2), a physiological index representing the efficiency with which food is converted into body tissue, was calculated as follows:

=A-0-U)

K

2

A

’

J. M.NAVARRO

22

where A is the energy absorbed from the food and R + U the energy lost in respiration and excretion, respectively. The relationship between length (L) and dry tissue weight (TW) was determined after the physiological measurements were completed. The regression equation obtained was: TW = 0.0049 L3.15 (TW, g; L, cm; Y= 0.99; n = 106). Length measurements of mussels used in the physiological experiments were converted to dry-tissue weight by interpolation from the length versus dry-tissue weight regression. Calorilic content of the soft parts of mussels was dete~in~ with a Parr bomb calorimeter for the size range of mussels used in the experiments. The mean calorific content was 20.8 kJ ag- ’ dry wt and 23.7 kJ 1g- ’ AFDW. Physiological rates were related to dry meat weight by linear regression analysis, after log-transformation of all variates. Regression equations for filtration rate and oxygen uptake were compared by ANCOVA. ANOVA was carried out to compare oxygen uptake under two different metabolic conditions (routine and postfeeding) and for assimilation efficiency, which did not show significant regressions with body size. In all statistical tests differences are considered significant when P I 0.05 and highly signilicant when P I 0.01.

RESULTS FILTRATION RATE

Highly signiIicant regressions were found between filtration rate and dry tissue weight at all the expe~mental salinities (Table I). Salinity had a clear effect on ~ltration rate in all size classes investigated (Figs. l-2). Thus filtration rate was greater and similar at the two higher salinities (24 and 30%,), but decreased at 18x0 and was considerably reduced at 15%,. For example, a mussel of 1 g dry tissue wt (5.4 cm shell length) filtered

TABLE I C. chorus: regressions

of filtration rate (I’ h- ‘) and assimilation efficiency (%) against dry weight (g), for mussels at different salinities. Regression equations are of the form Y = aWb, where Y = filtration rate or assimilation effkiency and W = dry weight. P is the significance of the difference between the weight exponent 6 and zero. NS, not significant. physiological process Filtration rate

Assimilation efficiency

Salinity

n

b

15 18 24 30 15 18 24 30

12 12 15 11 6 12 17 11

0.36 0.47 0.56 0.57 - 0.010 - 0.019 - 0.012 0.011

a 0.06 0.60

1.42 1.56 88.43 77.81 80.56 80.78

r 0.71 0.97 0.99 0.99 - 0.43 -0.41 -0.31 0.19

P

to.01
PHYSIOLOGICAL

ECOLOGY

OF CHOROMYTILUS

e-4

FR = 0.06

W”‘36

(r=0.77;

n=12;

15%.

6)

*

FR = 0.60

W”‘47

(r=0.97;

n=lZ;

16%.

S)

.----a

FR =

1.42

W”‘56

(v0.99;

n=15;

24%.S)

)-.-

FR =

1.56

W”‘57

(r=0.99;

n=ll;

30X.6)

0.01 0.02

0.05

10.0 5.

CHORUS

23

,;&

2.

2 ;

0.5

3 5 .-

0.2

g 0.1 rlL 0.05

-;

0.02 1.0 1 0.1 0.2

0.5

1.0

2.0

Dry-tissue weight (g) Fig. 1. C. chorus: filtration

rate in relation

to body size at different

10.000-j

salinities.

n

A

_c -

0

O-0

A-A

m-m 12

18

24

1.0

5.0 15.0

30

Salinity(%o) Fig. 2. C. chorus: effect of salinity on filtration

rate at three body sizes (1, 5, 15 g dry tissue wt).

1.56 1. h- 1 at 30x,, 0.60 1. h- ’ at 18%,, and only 0.06 1. h- ’ at 15%, salinity. Similar trends were observed when filtration rates of animals of 5 and 15 g dry tissue wt were compared at different salinities (Fig. 2). ANCOVA showed that the slopes of the filtration rate vs. dry weight regressions were significantly different (P I 0.05) when the four experimental salinities were compared (Table III). However, when pairs of salini-

J. M. NAVARRO

24

ties were compared

no significantly

and higher salinity combinations

different slopes (P 2 0.05) were found at the lower

(15-18 and 24-30x,),

although

in slope were found for all other pairwise comparisons, ences between INGESTION

Ingestion

precluding

significant

differences

any tests for differ-

elevations.

RATE

rate, calculated

as the product

of filtration

rate and the dry weight of

D. marina per unit volume of water, was higher at 24 and 30x,, than at the lower salinities (Fig. 3). Thus at 24-30x, a small mussel of 50 mg dry tissue wt ingested z 14% of its dry tissue wt * day- ‘, and a large mussel of 12 g dry tissue wt ingested M 1.4% of its wt.dayy’. At 18x0 salinity the daily ingested ration was greatly reduced, reaching values of 7.5 and 0.4%, respectively, in the same smaller and larger animals, and at the lowest salinity (15x,) the reduction was more pronounced, a small mussel ingesting 1.1% of its dry tissue wt . day - ’ and a large mussel only 0.03% of its wt +day- ‘.

207 ‘;6

107

0 r 0, 2 .Y

* t 2 -0 0 \:

=.

21:

.

0.5-

2 C .0

0.2-

z

0.1 :

B 5 :

0.05o--* U .---.

0.02 -

).+ 0.01

!

0.01

IR% = IR% = IR% = IR% =

0.16 1.53 3.66 4.01

I - ‘I”“, 0.02 0.05

W-o’64 W-o’53 W-o’44 W-o’43

0.1 Dry-

Fig. 3. C. chorus: ingested

ration

expressed

(r--0.91; (r=-0.96; (r=-0.96; (r=-0.99;

n-12; 15%. S) n=12; 16%. S) n=l5; 24%. S) n=ll; 3O%.S)

1 ’ ‘I”“, 0.2 0.5 tissue

1.0

weight

:\

0

1 1 ’ I”“, 2.0 5.0

‘\\

I f lo.0 20.0

(g)

as a % of dry tissue wt.dayrelation to body size.

’ at different salinities and in

PHYSIOLOGICAL ASSIMILATION

ECOLOGY OF CHOROMYTILUS

25

CHORUS

EFFICIENCY

C. chorus assimilated D. burnt with high efficiency (w 80%) (Table I, Fig. 4). Assimilation efficiency was independent of both body weight (P2 0.05) and salinity (ANOVA: F = 2.46, df 3,41, P 2 0.05).

*-* h--& .----0

AE = 88.43 AE = 77.80 AE = 80.55

I

’

’ I’“‘1

W-o’o1 WI;;: W o;o,

,

Dry-tissue Fig. 4.

C. chorus:

(r=-0.43: (r=-0.41; {:-;Jl;

1

n= 6: 15%. S) 18X0 S) “,I;;; y4 ;{ n=l 1;

II”“1

0.5

1.0

weight

I

2.0

’

’ I”“1

5.0

10.0

I

20.0

’

(g 1

assimilation effkiency in relation to body size at different salinities.

OXYGEN UPTAKE

Highly significant regressions were found between oxygen consumption and drytissue weight for all the metabolic conditions and at all four experimental salinities (Table II). TABLE II C. chorus: regressions of oxygen uptake fml0,. h - ‘) against dry weight (g) for mussels at different salinities and at three metabolic conditions. Regression equations are of the form Y = aW*, where Y = oxygen uptake and W = dry weight. P is the significance of the difference between the weight exponent b and zero.

Metabolic condition Standard

Postfeeding

Routine

Salinity

n

b

a

r

P

15 18 24 30 18 24 30 18 24 30

12 12 12 12 12 12 11 14 12 14

0.60 0.82 0.76 0.76 0.64 0.72 0.63 0.69 0.72 0.67

0.146 0.192 0.215 0.204 0.293 0.272 0.303 0.327 0.284 0.306

0.98 0.99 0.99 0.99 0.98 0.99 0.99 0.99 0.99 0.99

co.01
26

J. M. NAVARRO

The ANCOVA for standard metabolism showed that there were no significant differences between slopes or between elevations when the three higher salinities (18, 24 and 3079 were compared (Table III), but when the lowest experimental salinity (15x,) was included in the analysis, significant differences in the slopes were found, precluding any test for differences between elevations. In a mussel of 1 g dry wt, the standard 0, uptake was lower at 15x,, than at higher salinities (Fig. 5).

TABLE

C. chorus: comparison

Physiological Filtration

Oxygen

between

regressions

(standard)

at different

P (slope)

combination

All 15-18 15-24 15-30 18-24 18-30 24-30 All 18-24-30 15-18 15-24 15-30 18-24 18-30 24-30

rate

uptake

of filtration rate and oxygen uptake not significant.

Salinity

process

III salinities.

NS,

P (elevation)

< 0.05 10.01

NS < 0.05

< 0.05 < 0.05 < 0.05 NS

NS

<0.05 NS

NS -co.01


NS

NS

NS

NS

NS

0.1004 12

18

24 Salinity

30

(%o)

Fig. 5. C. chorus: oxygen uptake by a mussel of 1 g dry tissue wt at three metabolic conditions: (0) postfeeding (A), and routine (m), at three different salinities.

standard

PHYSIOLOGICAL

ECOLOGY

OF CHOROMYTILUS

21

CHORUS

The increase in the oxygen consumption in mussels during “postfeeding” was probably due to the physiolo~~al cost of digestion, and the further small increase under “routine metabolism” represented the mechanical cost of filtration (Fig. 5). The rates of oxygen uptake associated with “routine metabolism” and “postfeeding” were compared by ANOVA and no significant differences were found between them (ANOVA: F = 0.02, df $69, P 2 0.05) at the three highest salinities. EXCRETION

RATE

The energy lost due to excretion was very low at all salinities, having a small effect on the scope for growth. The NH,-N excretion for a mussel of 1 g dry wt increased from 8.78 to 16.22 pg. h- ’ when salinity was lowered from 30 to 18%,, but a decrease to 3.49 pg * h - 1 was found at the lowest salinity (15%,). The value for the weight exponent (b) ranged from 0.68 at 30& to 0.38 at 15x,, suggesting that larger indi~du~s are more sensitive to reduced salinities and/or that excretory losses are enhanced in smaller mussels owing to a larger surface area to volume ratio (Fig. 6). SCOPE

FUR GROWTH

Scope for growth in C. chorus was greater at the higher salinities, although relatively constant between 30 and 24x,. (Fig. 7, Table IV). The negative effect of low salinity on

loo

O---o H l ---+ )_.q

ER ER ER ER

= 3.49 W”= (m0.94; n=lO; 15%,$) = 16.22 W”‘53 (r=O.98; n=10; 18%o 5) = Il.28 k&f; (r=O.Qa: n=15; 24%-S) = 8.78W ’ (m0.98; n-14; JO%0 S)

; .c 2

:,

20-

0.1-1, 0.01 0.02

0.05

0.1

0.2

0.5

Dry- tissue Fig. 6. C. chorus: excretion

rate in relation

1.0

weight

2.0

5.0

10.0

20.0

(g1

to body size at different

salinities.

IS.000

12.000 15.000 18.000

10.000

6.44 23.38 34.47 63.78 84.90 102.51 125.17 138.62 157.08 173.96

20.9 43.4 54.1 76.7 90.2 100.4 112.4 119.1 127.9 135.5

6.85 25.46 37.80 70.71 94.61 114.61 140.45 155.83 176.97 196.35

3.53 10.41 14.42 24.17 30.73 36.00 42.57 46.37 51.50 56.11

20.9 43.4 54.1 76.7 90.2 100.4 112.4 119.1 127.9 135.5

Ash-free (mg,day-‘)

0.50 1.15 1.48 2.20 2.64 2.98 3.39 3.62 3.92 4.19

20.9 43.4 54.1 76.7 90.2 100.4 112.4 119.1 127.9 135.5

in relation

142.5 529.4 786.0 1470.4 1967.5 2383.4 2920.7 3240.6 3680.2 4083.2

133.9 486.2 716.8 1326.3 1765.5 2131.8 2603.0 2882.7 3266.5 3617.6

73.4 216.5 300.0 502.6 639.0 748.6 885.2 964.2 1070.1 1166.8

10.4 23.9 30.8 45.8 54.9 62.0 70.5 75.3 81.5 87.2

Energy (J.day-‘)

Energy ingested

of scope for growth

20.9 43.4 54.1 16 7 ._.. 90.2 100.4 112.4 119.1 127.9 135.5

Shell length (mm)

(d) Salinity: 3Wm 0.050 0.500 1.000 3.000 5.000 7.000

(a)

Salinity: 15% 0.050 0.500 1.000 3.000 5.000 7.000 10.000 12.000 15.000 18.000 lb) Salinity: 18% 0.050 0.500 1.000 3.000 5.000 7.000 10.000 12.000 15.000 18.000 (c) Salinity: 24% 0.050 0.500 1.000 3.000 5.000 7.000 10.000 12.000 15.000

Dry-tissue (g)

Body size

C. chorus: calculation

TABLE

IV

111.3 424.3 634.7 1201.8 1617.1 1966.2 2419.0 2689.3 3061.6 3403.7

111.8 394.9 577.4 1054.4 1394.9 1677.5 2040.0 2253.8 2547.1 2814.6

60.4 170.7 233.3 383.0 482.2 561.3 659.2 715.6 791.4 859.3

9.5 21.3 27.2 40.0 47.8 53.8 60.9 65.0 70.1 74.9

(J.day-‘)

Energy assimilated

31.1 105.2 151.3 268.6 350.4 417.2 501.8 551.3 618.6 679.5

22.1 91.3 139.4 272.0 370.6 454.2 563.4 629.9 719.5 802.9

13.0 45.8 66.6 119.7 156.8 187.3 226.0 248.7 279.6 307.5

0.9 2.6 3.6 5.7 7.1 8.2 9.6 10.3 11.4 12.3

(J,day-‘)

19.9 92.8 147.7 308.4 434.3 544.1 690.9 780.7 906.6 1024.4

15.4 81.0 133.4 294.3 425.1 541.6 700.2 798.5 937.6 1069.2

19.9 97.5 157.3 335.6 477.4 602.2 770.2 873.5 1018.8 1155.4

11.5 49.9 69.6 134.5 182.7 223.6 277.0 308.9 353.3 394.1

(J day- ‘)

0.7 3.3 5.2 11.0 15.6 19.6 25.0 28.3 33.0 37.3

1.0 4.3 6.7 13.7 19.1 23.8 30.0 33.8 39.1 44.0

90.8 328.2 481.8 882.4 1167.2 1402.5 1703.0 1880.2 2122.0 2342.0

95.4 309.7 437.3 746.4 950.7 1112.0 1309.3 1421.5 1570.4 1701.5

-

38.6 66.5 66.4 30.1 17.9 68.0 143.7 194.0 264.9 340.8 2.0 6.7 9.7 17.3 22.7 27.1 32.8 36.1 40.6 44.7

-

-

4.4 15.8 23.1 42.3 56.0 67.3 81.7 90.3 101.9 112.4

4.6 14.8 20.9 35.8 45.6 53.4 62.8 68.2 75.4 81.7

1.9 3.2 3.2 1.4 0.9 3.3 6.9 9.3 12.7 16.3

0.1 1.3 2.1 4.7 6.7 8.4 10.6 11.9 13.9 15.6

Mussel dry-tissue (mg.day-‘)

2.7 - 26.2 - 44.4 - 97.6 - 138.8 - 174.2 221.0 - 249.4 - 259.7 - 325.5

Energy (J.day-‘)

Scope for growth

12 “C.

0.7 1.6 2.1 3.2 3.8 4.3 5.0 5.4 5.8 6.2

(J.day-‘)

Energy lost in excretion

20 x lo6 cells D. marina. l- ‘; temperature:

Energy used m respiration

Food ration:

Energy lost in feces

to body size and salinity. b;;

PHYSIOLOGICAL

ECOLOGY OF CHOROMYTILUS

18

12

24

Salinity

CHORUS

29

JO

(%o)

Fig. 7. C. chorus: scope for growth at different salinities for three body sizes (A, 1 g; B, 5 g; C, 15 g dry tissue

wt).

the scope for growth was more marked in the larger animals. For example, scope for growth for a mussel of 1 g dry tissue wt became negative at 16%,, whereas for a mussel of 15 g dry tissue wt scope for growth became negative at 19&, salinity. NET GROWTH EFFICIENCY

(Kz)

Net growth efficiency (K2) was reduced at low salinities (Fig. 8). Thus at 15%, the net growth efficiency was negative over a large range of body sizes (between 1 and 15 g 0.8-1 t my

C-T Y

0.4

1

-

6 5 ‘U F 5 5 :

-0.4:;

b

-1.0.

0.0-

z! 8

-5.0, 12

18

24 Salinity (%0)

30

Fig. 8. C. chorus: net growth efficiency for three body sizes at different salinities (0, 1 g; A, 5 g; II, 15 g dry tissue wt).

J.M. NAVARRO

30

dry tissue between

wt), but at 18x, K, became

positive

in small animals

5 and 15 g dry tissue wt still showed negative

although

growth efficiencies.

mussels At 24 and

30x,,, net growth efficiencies were high, ranging from 0.62 in very large (15 g) mussels to 0.76 in small ones (1 g). At all salinities, K2 decreased with increasing body weight.

DISCUSSION

The responses

and tolerances

of several bivalve species to changes

in salinity have

been investigated by numerous authors (Bohle, 1972; Kinne, 1967, 1971; Costa & Pritchard, 1978; Davenport, 1979a,b; Davenport et al., 1975; Shumway, 1977; and others), but there is little information on the effect of salinity on the physiological energetics of bivalves, although Widdows (1985a) has described physiological responses and scope for growth of M. edulis exposed to fluctuating salinities. The results of the present study relating feeding activity of C. chants to salinity are broadly consistent with those found by other authors for various species of bivalves. Thus, C. chants keeps its filtration rate constant between 24 and 30x,, salinity, and has the capacity to close its valves when the salinity decreases. Direct observations reveal that mussels of this species close their valves partially or totally at 18 and 15x,, salinity. This behaviour would help to isolate the tissue from environments of low salinity, and has been described in other species. Thus Djangmah et al. (1979) recorded that A. se&is closes its valves when the salinity falls to 15.4&,, and Widdows (1985a) observed that M. edulis exposed to a fluctuating salinity regime exhibits a relatively constant rate of feeding between 20 and 30x,, whereas mussels exposed to salinities < 19x0 show valve closure. These physiological responses to low salinity are reflected in slower growth (Bohle, 1972). Davenport & Fletcher (1978) working on gill preparations of M. edulis, concluded that the shell closure response to low salinity levels occurs <20%,, this being a very important mechanism for protection of the frontal cilia against osmotic damage. However, Davenport (1979a,b) later concluded that the exhalant siphon is closed < 20x0 and only a partial valve closure occurs, resulting in a cessation

of feeding activity

and a reduction in oxygen uptake. Similar results were found in the present work, where shell closure occurs at salinities < IS%,. Thus, the oxygen uptake of C. chants (standard metabolism) is similar between 30 and 18x,, whereas at 15%, there is a decrease of z 30%) which is attributable to the reduction in oxygen diffusion and water exchange and to the decreased costs of feeding associated with valve closure. The decrease in oxygen uptake by C. chorus at salinities <20x, is consistent with observations by Shumway & Youngson (1979) on A4. demissus and by Stickle & Sabourin (1979) and Widdows (1985a) on A4. edulis. The decrease in oxygen uptake can be explained by the decline in, or cessation of, the feeding activity and by the reduction of the valve gape. C. chants shows a constant

assimilation

efficiency at salinities from 15 to 30x0 which

PHYSIOLOGICAL

ECOLOGY

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31

is independent of body size. The values obtained in the present study are in good agreement with those obtained for two other species of bivalves, Mytilus chilensis (Navarro &Winter, 1982) and Ostrea chilensis (Winter et al., 1984), which are sympatric with C. chorus. The excretion rate represents only a small proportion of the energy assimilated by C. chorus at the four experimental salinities. The higher value in the NH,-N excretion at 18%0(16.2 pg. h- ’ for a mussel of 1 g dry wt) suggests that this species may mobilize protein as a major metabolic substrate during the periods of reduced food intake which occur at this salinity. Alternatively, this high excretion rate may be a result of the breakdown of amino acids as intracellular isosmotic regulators following the reduction of salinity to 18%,. Thus, Livingstone et al. (1979) found higher rates of amino acid and ammonia excretion in M. edulis during fluctuating salinity cycles than under the steadystate conditions of 30%,, S. The reduced excretion rate observed at 15%, (3.49 pg NH,-N . h- ’ for a mussel of 1 g dry wt) is associated with the pronounced valve closure shown by C. chorus at low salinity. The closing of the shell valves results in a build up of ammonia in the mantle cavity and body tissue, which can inhibit the production of NH, (Widdows, 1985~). Under these conditions the mussel would be unable to mobilize protein reserves during periods of starvation caused by low salinities (15%0). The overall effect of salinity on the mussel is reflected in the scope for growth and the net growth efficiency (K2), which may be considered as two useful stress indices because they represent the response of the whole organism to the environmental conditions (Bayne & Newell, 1983). Scope for growth in C. chorus of given size is similar between 24 and 30%0 salinity and is always positive in this range. However, the low feeding activity and relatively high metabolic rate at the lowest salinities results in a negative scope for growth for the larger animals at 18%0and for all the size classes at 15%, (Fig. 7). These results agree with those of Widdows (1985a) for M. edulis, which indicate that scope for growth is negative ~20%~ salinity. The stress imposed on C. chorus by low salinity is also reflected in a decreased net growth efficiency (K2). Fig. 8 shows that K, decreases with an increase in body size, which was also found in the sympatric species M. chilensis at 30%0 salinity (Navarro & Winter, 1982). The data suggest that the growth rate of C. chorus and the degree to which this species can penetrate estuaries may be partially determined by the amount of time which the mussels are able to spend in positive scope for growth in estuarine environments which subject them to reduced and fluctuating salinities. Furthermore, these findings will also facilitate the construction of aquaculture systems, such as hatcheries, and the selection of suitable places within an estuarine environment to culture this species. ACKNOWLEDGEMENTS

I am very grateful to Dr. R. J. Thompson for valuable discussions and critical reading of the manuscript, and to Dr. J. E. Winter for discussions during the early stages of this

32

J. M. NAVARRO

work. My thanks are also due to Mrs. Ana Salamanca for help in the laboratory. Temperature and salinity data from Queule estuary were provided by the Instituto de Zoologia, Universidad Austral de Chile. This research was supported by Grants C-80-1 and RS-81-09 from the D.I.D. Universidad Austral de Chile and by the Fondo National de Desarrollo Cientifico y Tecnologico - Chile.

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SHUMWAY, S. E., 1977. The effect of fluctuating salinity on the tissue water content of eight species of bivalve molluscs. J. Comp. Physiol., Vol. 116, pp. 269-285. SHUMWAY, S.E. & A. YOUNGSON, 1979. The effects of fluctuating salinity on the physiology of Modiolus demi.ssus (Dillwyn). J. Exp. Mar. Biol. Ecol., Vol. 40, pp. 167-181. SOLORZANO, L., 1969. Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol. Oceanogr., Vol. 14, pp. 799-801. STICKLE, W. B. & T. D. SABOURIN, 1979. Effects of salinity on the respiration and heart rate of the common mussel, Mytilus edulis L., and the black chiton, Kathertna tunicata (Wood). J. Exp. Mar. Biol. Ecol., Vol. 41, pp. 257-268. WIDDOWS, J., 1985a. The effects of fluctuating and abrupt changes in salinity on the performance ofMytilus edulis. In, Marine biology ofpolar regions and effects of stress on marine organisms, edited by J. S. Gray & M. E. Christiansen, Wiley-Interscience, pp. 555-566. W~DDOWS, J., 1985b. Physiological procedures. In, The effects ofstress andpollution on marine animals, edited by B.L. Bayne, Praeger Publishers, New York, pp. 161-178. W~DDOWS, J., 1985~. Physiological measurements. In, The effects of stress andpollution on marine animals, edited by B. L. Bayne, Praeger Publishers, New York, pp. 3-45. WINTER, J.E., 1973. The filtration rate of Mytilus edulis and its dependence on algal concentrations, measured by a continuous automatic recording apparatus. Mar. Biol., Vol. 22, pp. 3 17-328. WINTER, J.E., M.A. ACEVEDO & J.M. NAVARRO, 1984. Quempilltn estuary, an experimental oyster cultivation station in southern Chile. Energy balance in Ostrea chilensis. Mar. Ecol. Prog. Ser., Vol. 20, pp. 151-164.