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The effect of temperature and season on the respiratory rates of three psammolittoral gastropods
Comp. Biochem. Phrsiol., Vol. 66A. pp. 107 to 111
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© Pergamon Press Ltd 1980. Printed in Great Britain
THE EFFECT OF TEMPERATURE AND SEASON ON THE RESPIRATORY RATES OF THREE PSAMMOLITTORAL GASTROPODS A. H. DYE* a n d L. McGWYNNE Department of Zoology, University of Port Elizabeth, PO Box 1600, Port Elizabeth, South Africa
(Received 21 May 1979) Abstraet--l. The effect of season and of acute temperture changes on the respiratory rates of three sandy beach gastropods (Bullia rhodostoma, Bullia digitalis and Bullia pura) was investigated. 2. Although the animals exhibited a considerable degree of metabolic regulation some rotation and translation of the rate/temperature curves occurred between summer and winter. 3. Qt0 was found to be independent of body size and temperature in B. rhodostoma and B. digitalis, but some temperature dependence was found in B. pura.
INTRODUCTION Scavenging gastropods of the genus Bullia are comm o n on sandy beaches in South Africa (Brown, 1961) a n d account for a significant p r o p o r t i o n of the macrofauna (McLachlan, 1977). The respiratory physiology of the three d o m i n a n t beach gastropods, Bullia rhodostoma Reeve, B. digitalis Meuschen a n d B. pura Melvill was studied as part of a larger project on the ecology of sandy beaches in the vicinity of P o r t Elizabeth (33°55'S, 25°38'E) on the south coast of South Africa. D a t a on the ecophysiology of Bullia sp, in South Africa are available, the most notable works being those of Brown (1961) on B. digitalis a n d B. laevissima (Gmelin) o n the west coast, Brown et al. (1978) on B. melanoides and B. digitalis, Brown & da Silva (1979) a n d Brown (1979) o n the effects of temperature a n d activity o n the respiration of B. digitalis. O t h e r work includes that of M c L a c b l a n et al. (in press) on B. rhodostoma distribution a n d population dynamics in the Eastern Cape.
MATERIALS AND METHODS The respiratory rate of Bullia typical of the local size range (3-55 mm max. shell length) was measured in summer and winter during 1978. The environmental temperatures were around 20°C and 15°C respectively. Oxygen consumption was measured over a temperature range of 10°C from l0 to 20°C in winter and from 15 to 25°C in summer, at intervals of 5°C. The animals were not fed during the experiments which were completed Within 72 hr of collection to minimize starvation effects (Heeg, 1977). The animals were kept for 18 hr at the desired experimental temperatures prior to the respiration determinations. All measurements were done in triplicate, the number of animals used varying between 8 and 27 depending on species. Oxygen consumption was measured by placing an animal (or number of animals, depending on size) in a container of pre-filtered (0.45 gin) and aerated seawater of known volume. A plastic tube (2.5 mm i.d.) was placed in
the container and the water was sealed off from the atmospbere by a 1 cm layer of liquid paraffin oil iTrevallion, 1971). Oxygen consumption runs lasted for 60 min during which time four l ml samples of water were withdrawn through the tube by syringe at intervals of 15 min. The water in the tube itself was discarded each time since it may have equilibrated with the air above it. The partial pressure of oxygen in the samples was measured on a Radiometer unit fitted with a Clark E5046 oxygen electrode. The decrease in PO2 was used to calculate the oxygen consumption of the organisms. At no time was the PO2 allowed to drop below 70% of air saturation. An identical container, without an animal, served as a control. The water volume varied between 50 and 120ml depending on the size and number of the animals. It was found that sustained stirring had no effect either on the respiratory rates of the animals (Brown, 1979), or on the oxygen measurements themselves, and this procedure was therefore omitted. Two sources of variation are associated with the above procedure, although they were easily corrected for under the present experimental conditions. Firstly, the decrease in volume as a result of withdrawing water from the containers introduced a variable ranging from 0.1 to 8% depending on animal size and secondly, the liquid paraffin was found to be slightly permeable to oxygen. A mean leakage of 2.18 + 0 . 1 7 # l O 2 / h r for every 100 ml of water present was found in tests done without the. plastic tube. Both of these factors were taken into account when calculating the respiration rates. In the case of B. rhodostoma dry mass was calculated from the expression Logto W = 2.791ogtol = 1.77 previously calculated for the population being studied IMcLachlan, pers. comm.). Dry mass was obtained for B. digitalis and B. pura by removing the animals from their shells and drying at 60°C for 24 hr. During the experiments the animals had the foot extended and slow movements were observed. This corresponds to a state of activity somewhat below their field "active" state (Brown, 1979).
RESULTS Figure 1 shows the effect of acute temperature change on the size dependent metabolic rate of B. rhodostoma in summer and winter. Although the slopes of the winter lines did not differ from each other, significant differences were found between the intercepts (analysis of variance, P < 0.01). In summer b o t h the slopes and the intercepts differ (analysis of
* New address from end of December 1979: c/o Dept. Zoology, University of Transkei, Private bag X5092, Umtata, Rep. of Transkei. i07
108
A.H. DYE and L. McGwYNNE W
I00
,'~'" f . / ,s ° -O,j, ~ .O 0/" • ,.'" . •" 0" --
. ". ~. " ~
,,:;--... 0 o
•
~ . 20 " . o " "
•f
t:<:;
o
~-~ I00
x 0
•
"~.~S' "~ ~ "
so .:~u~r'''20 "," I0
50 ,0o Dry Mass (rag) 25"C ...... .........
5;0
20"C 15"C IO*C
Fig. 1. The effects of acute temperature change on the respiration of Bullia rhodostonu~ in summer (S) and winter (W).
Figures 4-6 show the effect of body mass and season on Qlo in B. rhodostoma, B. digitalis and B. pura respectively. In B. rhodostoma no significant relationship between mass and Qlo was evident either in summer or winter although Qlo appears to be more variable between 10 and 15°C than between 20 and 25':C. A similar situation occurs in B. digitalis with Ql0 virtually identical in summer and winter. There was a slight tendency for Qlo to increase at the lower temperatures. In B. pura, however, significant differences were found between the Q~o values for various size classes (analysis of variance, P < 0.01), such that in winter the smaller animals have a higher Qlo than the larger ones. In summer the Qlo values of all size classes increases at the lower temperatures but there is no clear relationship with size. Figures 7-9 show the acutely measured metabolic rate/temperature curves for three size classes of B. rhodostoma, B. digitalis and B. pura respectively. The curves for the larger size classes do not differ much between summer and winter and a considerable degree of metabolic regulation is evident. The 100mg and 10mg size classes of B. rhodostoma do, however, show some counter-clockwise rotation in winter. This is also evident in the small size classes of B. pura. DISCUSSION
variance, P < 0.01). No significant differences were found between summer and winter in either slopes or intercepts. The effect of temperature on the respiration of B. digitalis is shown in Fig. 2. In this case both the slopes and the intercepts differed significantly from each other in summer (analysis of variance, P < 0.01), but the slopes did not differ from each other in winter. Significant seasonal differences were found in B. digitalis (analysis of variance, P < 0 . 0 0 1 ) . Similarly, significant differences both within and between seasons was found in B. pura (Fig. 3) (analysis of variance, P < 0.01 within; P < 0.001 between). Table 1 gives an analysis of this data.
The value of b in the metabolism/mass expression for B. rhodostoma is close to the expected 0.75 for poikilotherms (Zeuthen, 1953). However, both B. digitalis and B. pura have much lower and more variable b values. They are, however, close to the values obtained by Brown & da Silva (1979) for B. digitalis on the west coast. Large variations in b have been reported for a number of molluscs and the exponent seems to be related to such factors as temperature, season, body size, nutritive state, body composition and reproduction (Zeuthen, 1953). Bayne & Scullard (1978) reported a range of b values of 0.334).86 in Thais lapillus, in this case related to nutrition. Newell (1973) gives a range of 0.314).59 for Littorina littorea, dependent upon activity. The values for Bullia in the present study vary from 0.21 to 0.80 depending on
w. ~ :;,,,,-,. I00 5O ~
30
0
,,S~
.o-''"
w
I00
• ,,-,.'~.....
.,..-".-'T... OJ'o..,~ . . . ' 0~" . . e"
~20
.... i ....
cO
,oc .50 50
20
~.'~'-'-
sot- , - - - ' ' 5 . " 5~
,~o
50o
Dry Mass (rn~)
.
.
.
.
io
5o
too Dry Mass (rag)
25"C
~
.....
20"C
.....
...... ..........
15"C IO*C
. . . . . . . 15"C .......... IO*C
Fig. 2. The effects of acute temperature change on the respiration of Bullia digitalLs in summer (S) and winter ( W ) .
L 50O
25"C
20"C
Fig, 3. The effects of acute temperature change on the respiration of Bullia pura in summer (S) and winter (W).
109
Respiration in gastropods Table 1. Analysis of the rates of oxygen consumption (Vo2) of B. rhodostoma, B. digitalis and B. pura in summer and winter
Species
Season
B. rhodostoma
n
15 20 25 10 15 20
27 27 27 20 20 20
0.601 0.660 0.701 0.600 0.631 0.653
_+ 0.012 ___0.006 _+ 0.019 + 0.010 __. 0.015 + 0.008
0.701 0.703 0.724 0.623 0.722 0.801
_ 0.063 _+ 0.061 +_ 0.065 + 0.037 _ 0.044 + 0.041
1.00 1.18 1.38 0.69 1.18 1.78
15 20 25 10 15 20
17 17 17 21 21 21
1.010 0.963 1.122 0.700 0.721 0.841
_+ 0.009 + 0.006 + 0.009 + 0.002 + 0.002 + 0.051
0.361 0.436 0.381 0.511 0.554 0.530
_+ 0.005 + 0.008 + 0.006 _+ 0.020 _+ 0.022 + 0.021
0.54 0.66 0.76 0.53 0.66 0.80
15 20 25 10 15 20
18 18 18 8 8 8
0.921 1.072 1.022 0.813 1.121 1.311
_ + + _ + _
0.361 0.324 0.436 0.291 0.230 0.210
+ + + + + _
0.44 0.51 0.87 0.25 0.38 0.54
Summer Winter
B. digitalis
Summer Winter
B. pura
Respiratory rate of a 100 mg animal (plO2mg/hr)
Temperature (' C)
Summer Winter
Regression analysis a + SD b _+ SD
0.088 0.033 0.018 0.049 0.067 0.078
0.005 0.002 0.003 0.011 0.009 0.008
a and b are the constants in the equation logtoVo 2 = a + b IogtoW where W is the dry mass in mg. "n" indicates the number of animals used.
temperature and species, and are well within the published range. The respiration rates for the Bullia species reported here compare well with the metabolic rates of other gastropods. Sandison (1966) reported respiratory rates of 1.0 and 1 . 5 # 1 0 2 m g - t h r -~ at 18°C for Thais lapil/us and Bayne & Scullard (1978) gave values of _+ 1.5/A 0 2 m g - J h r - ~ for the same species. Newell & Pye (1970) measured standard metabolic rates of 0.254).80 #1 O2 m g - t h r - ~ in L. /ittorea and active rates of 1.0-5.0/~1 0 2 rag- ~ h r - ~ in the same species. Studies on Bu/inus africanus by Heeg (1977) yielded a metabolic rate of 1.44 #1 0 2 m g - t h r - t at 25°C, and this seemed to be unaffected by starvation up to 21days. Studies on various littoral snails have yielded metabolic rates of between 1.0 and 2.5 #1 O2 m g - ~ h r - t at 20°C ( M c M a h o n & Russel-
3
Hunter, 1977). Brown et al. (1978) reported respiratory rates of 2.3/A 0 2 rag- t h r - ~ in B. digitalis at 15'~C. A study of the effect of turbulence on the respiratory rate of B. digitalis by Brown (1979) revealed that while a constant level of turbulence (stirring) did not affect the respiratory rate, an increase of approximately 37°o in oxygen c o n s u m p t i o n occurred when the turbulence was continually changing. This level of activity was equated by Brown with conditions in the swash zone of the beach, and appears to approximate the natural active state of the animals. The results of the present study therefore underestimate the active rate by approximately 37%. Both B. rhodostoma and B. digitalis have low and fairly constant Qlo values, independent of season or
w
QIO
[7t L
1"751 ~ ~ " " ",~,
,o
,'~
,~
,;
~'~
~'~
Temperature *C
.......
5OOmg I00 mg IO mg
Fig. 4. The effect of temperature on Qto in Bullia rhodos-
torrut in summer (S) and winter (W).
25J I0
13
S
16
19
22
25
Temperoture °C ....... .......
200mg IOOmg IO rng
Fig. 5. The effect of temperature on Qto in Bullia digitalis in summer (S) and winter (W).
110
A, H. DYE and L. McGwVNNE
S,s ,I,s .f'° ~, f f'W
~°
~.
W
Q~ c_o x O
...... I0
13
IL6
119
22
0
I 0 0 mg
.50 mg
.......
IO rng
-w-
25
Temperature °C .......
-__-'- . . . . . . . .
IO
1'5
20
25
Temperature *C 200rr~
Fig. 6. The effect of temperature on Q~0 in Bulliu pura in summer (S) and winter (W).
tO0 mg IO mg
Fig. 8. Acutely measured rate/temperature curves for three size classes of Bulliu di.qitalis in summer (S) and winter (W).
W J
f.S"
/ "I
./ /
3
!
•/"
~-
./
,! .,~"f
o, iO
"
~
/
S
15 20 Temperature *C
~5 0J ~0
......
500 mg I00 mg I0 mg
Fig. 7. Acutely measured rate/temperature curves for three size classes of Bullia rhodostoma in summer (S) and winter (Wt
mass. B. p , r a has a higher and more variable Qlo, particularly at the lower temperatures, suggesting a lesser degree of metabolic regulation over the measured temperature range t h a n in the other species. This is borne out by the considerable degree of counter-clockwise rotation of the rate/metabolism curve for the small size classes in winter, a characteristic shared to a much smaller extent by B. rhodostoma and not at all by B. digitalis. These findings in the case of B. digitalis correspond with those of Brown (1979) for the west coast populations. The conclusion made by
b
-
-
~
15 20 Temperature *C
......
25
IOOmg 50rng I0 mg
Fig. 9. Acutely measured rate/temperature curves for three size classes of Bullia pura in summer IS1 and winter (Wl.
Brown (1979) that B. digitalis is not acclimatory adaptive ,to temperature is supported in the data for the Indian Ocean population as well as for B. rhodostoma. Bullia pura on the other hand does appear to show a degree of winter and summer acclimation to temperature.
Acknowledgements--The University of Port Elizabeth and the Department of Planning and the Environment are thanked for their financial assistance. Professor T, Erasmis and Dr. A. McLachlan are thanked for their constructive comments and for reading the manuscript.
Respiration in gastropods REFERENCES
BAYNE B. L. & SCULLARD C. (1978) Rates of oxygen consumption by Thais (Nucella) lapillus (L.). J. exp. mar. Biol. Ecol. 32, 97-111. BROWN A. C. (1961) Physiological ecological studies on two sandy beach gastropoda from South Africa; Bullia digitalis Meuschen and Bullia laevissima (Gmelin). Z. Morph. Okol. Tiere. 49, 629-657. BROWN A. C., ANSELL A, D. & TREVALLION A. (1978) Oxygen consumption by Bullia (Dorsanum) melanoides (Deshayes) and Bullia digitalis Meuschen (Gastropoda, Nassaridae~-an example of non-acclimation. Comp. Biochem. Physiol. 61A, 123-125. BROWN A. C. & DA SILVA F. M. (1979) The effect of temperature on oxygen consumption in Bullia digitalis Meuschen (Gastropoda, Nassaridae). Comp. Biochem. Physiol. 62A, 573-576. BROWN A. C. (1979) Oxygen consumption of the sandybeach whelk Bullia digitalis Meuschen at different levels of activity. Comp. Biochem. Physiol. 62A, 673-675. HEEG J. (1977) Oxygen consumption and the use of metabolic reserves during starvation and aestivation in Bulinus (Physopsis) africanus, (Pulmonata : Planorbidae). Malacologia 16~ 549-560.
111
MCLACHLAN A. (1977) Composition, distribution, abundance and biomass of the macrofauna of four sandy beaches. Zool. afr. 12, 279-306. MCLAcHLAN A., COOPER C. t~ VAN DER HORST G. (1979) Growth and production of Bullia rhodostoma Reeve (Mollusca, Gastropoda) on an open sandy beach in Algoa Bay. S. Aft. J. Zool. In press. MCMAHON R. F. & RUSSEL-HUNTER W. D. (1977) Temperature relation of aerial and aquatic respiration in six littoral snails in relation to their vertical zonation. Biol. Bull. 152, 182-198. NEWELL R. C. (1973) Factors affecting the respiration of intertidal invertebrates. Am. Zool, 13, 513 528. NEWELL R. C. & PVE V. 1. (1970) Seasonal changes in the effect of temperature on the oxygen consumption of the winkel Littorina littorea (L.) and the mussel Mytilus edulis L. Comp. Biochem. Physiol. 34A, 367 383. SANDISON R. L. (1966) The oxygen consumption of some intertidal gastropods in relation to zonation. J. Zool. (London) 149, 163-173. TREVALL1ON A. (1971) Studies on Tellina tenuis Da Costa IlL Aspects of general biology and energy flow. J. exp. rrutr. Biol. Ecol. 7, 95-122. ZEUTHEN E. (1953) Oxgen uptake as related to body size in organisms. Q. Rer. Biol. 28, 1-12.
0300-9629/80/0501-0107$02.00/0
© Pergamon Press Ltd 1980. Printed in Great Britain
THE EFFECT OF TEMPERATURE AND SEASON ON THE RESPIRATORY RATES OF THREE PSAMMOLITTORAL GASTROPODS A. H. DYE* a n d L. McGWYNNE Department of Zoology, University of Port Elizabeth, PO Box 1600, Port Elizabeth, South Africa
(Received 21 May 1979) Abstraet--l. The effect of season and of acute temperture changes on the respiratory rates of three sandy beach gastropods (Bullia rhodostoma, Bullia digitalis and Bullia pura) was investigated. 2. Although the animals exhibited a considerable degree of metabolic regulation some rotation and translation of the rate/temperature curves occurred between summer and winter. 3. Qt0 was found to be independent of body size and temperature in B. rhodostoma and B. digitalis, but some temperature dependence was found in B. pura.
INTRODUCTION Scavenging gastropods of the genus Bullia are comm o n on sandy beaches in South Africa (Brown, 1961) a n d account for a significant p r o p o r t i o n of the macrofauna (McLachlan, 1977). The respiratory physiology of the three d o m i n a n t beach gastropods, Bullia rhodostoma Reeve, B. digitalis Meuschen a n d B. pura Melvill was studied as part of a larger project on the ecology of sandy beaches in the vicinity of P o r t Elizabeth (33°55'S, 25°38'E) on the south coast of South Africa. D a t a on the ecophysiology of Bullia sp, in South Africa are available, the most notable works being those of Brown (1961) on B. digitalis a n d B. laevissima (Gmelin) o n the west coast, Brown et al. (1978) on B. melanoides and B. digitalis, Brown & da Silva (1979) a n d Brown (1979) o n the effects of temperature a n d activity o n the respiration of B. digitalis. O t h e r work includes that of M c L a c b l a n et al. (in press) on B. rhodostoma distribution a n d population dynamics in the Eastern Cape.
MATERIALS AND METHODS The respiratory rate of Bullia typical of the local size range (3-55 mm max. shell length) was measured in summer and winter during 1978. The environmental temperatures were around 20°C and 15°C respectively. Oxygen consumption was measured over a temperature range of 10°C from l0 to 20°C in winter and from 15 to 25°C in summer, at intervals of 5°C. The animals were not fed during the experiments which were completed Within 72 hr of collection to minimize starvation effects (Heeg, 1977). The animals were kept for 18 hr at the desired experimental temperatures prior to the respiration determinations. All measurements were done in triplicate, the number of animals used varying between 8 and 27 depending on species. Oxygen consumption was measured by placing an animal (or number of animals, depending on size) in a container of pre-filtered (0.45 gin) and aerated seawater of known volume. A plastic tube (2.5 mm i.d.) was placed in
the container and the water was sealed off from the atmospbere by a 1 cm layer of liquid paraffin oil iTrevallion, 1971). Oxygen consumption runs lasted for 60 min during which time four l ml samples of water were withdrawn through the tube by syringe at intervals of 15 min. The water in the tube itself was discarded each time since it may have equilibrated with the air above it. The partial pressure of oxygen in the samples was measured on a Radiometer unit fitted with a Clark E5046 oxygen electrode. The decrease in PO2 was used to calculate the oxygen consumption of the organisms. At no time was the PO2 allowed to drop below 70% of air saturation. An identical container, without an animal, served as a control. The water volume varied between 50 and 120ml depending on the size and number of the animals. It was found that sustained stirring had no effect either on the respiratory rates of the animals (Brown, 1979), or on the oxygen measurements themselves, and this procedure was therefore omitted. Two sources of variation are associated with the above procedure, although they were easily corrected for under the present experimental conditions. Firstly, the decrease in volume as a result of withdrawing water from the containers introduced a variable ranging from 0.1 to 8% depending on animal size and secondly, the liquid paraffin was found to be slightly permeable to oxygen. A mean leakage of 2.18 + 0 . 1 7 # l O 2 / h r for every 100 ml of water present was found in tests done without the. plastic tube. Both of these factors were taken into account when calculating the respiration rates. In the case of B. rhodostoma dry mass was calculated from the expression Logto W = 2.791ogtol = 1.77 previously calculated for the population being studied IMcLachlan, pers. comm.). Dry mass was obtained for B. digitalis and B. pura by removing the animals from their shells and drying at 60°C for 24 hr. During the experiments the animals had the foot extended and slow movements were observed. This corresponds to a state of activity somewhat below their field "active" state (Brown, 1979).
RESULTS Figure 1 shows the effect of acute temperature change on the size dependent metabolic rate of B. rhodostoma in summer and winter. Although the slopes of the winter lines did not differ from each other, significant differences were found between the intercepts (analysis of variance, P < 0.01). In summer b o t h the slopes and the intercepts differ (analysis of
* New address from end of December 1979: c/o Dept. Zoology, University of Transkei, Private bag X5092, Umtata, Rep. of Transkei. i07
108
A.H. DYE and L. McGwYNNE W
I00
,'~'" f . / ,s ° -O,j, ~ .O 0/" • ,.'" . •" 0" --
. ". ~. " ~
,,:;--... 0 o
•
~ . 20 " . o " "
•f
t:<:;
o
~-~ I00
x 0
•
"~.~S' "~ ~ "
so .:~u~r'''20 "," I0
50 ,0o Dry Mass (rag) 25"C ...... .........
5;0
20"C 15"C IO*C
Fig. 1. The effects of acute temperature change on the respiration of Bullia rhodostonu~ in summer (S) and winter (W).
Figures 4-6 show the effect of body mass and season on Qlo in B. rhodostoma, B. digitalis and B. pura respectively. In B. rhodostoma no significant relationship between mass and Qlo was evident either in summer or winter although Qlo appears to be more variable between 10 and 15°C than between 20 and 25':C. A similar situation occurs in B. digitalis with Ql0 virtually identical in summer and winter. There was a slight tendency for Qlo to increase at the lower temperatures. In B. pura, however, significant differences were found between the Q~o values for various size classes (analysis of variance, P < 0.01), such that in winter the smaller animals have a higher Qlo than the larger ones. In summer the Qlo values of all size classes increases at the lower temperatures but there is no clear relationship with size. Figures 7-9 show the acutely measured metabolic rate/temperature curves for three size classes of B. rhodostoma, B. digitalis and B. pura respectively. The curves for the larger size classes do not differ much between summer and winter and a considerable degree of metabolic regulation is evident. The 100mg and 10mg size classes of B. rhodostoma do, however, show some counter-clockwise rotation in winter. This is also evident in the small size classes of B. pura. DISCUSSION
variance, P < 0.01). No significant differences were found between summer and winter in either slopes or intercepts. The effect of temperature on the respiration of B. digitalis is shown in Fig. 2. In this case both the slopes and the intercepts differed significantly from each other in summer (analysis of variance, P < 0.01), but the slopes did not differ from each other in winter. Significant seasonal differences were found in B. digitalis (analysis of variance, P < 0 . 0 0 1 ) . Similarly, significant differences both within and between seasons was found in B. pura (Fig. 3) (analysis of variance, P < 0.01 within; P < 0.001 between). Table 1 gives an analysis of this data.
The value of b in the metabolism/mass expression for B. rhodostoma is close to the expected 0.75 for poikilotherms (Zeuthen, 1953). However, both B. digitalis and B. pura have much lower and more variable b values. They are, however, close to the values obtained by Brown & da Silva (1979) for B. digitalis on the west coast. Large variations in b have been reported for a number of molluscs and the exponent seems to be related to such factors as temperature, season, body size, nutritive state, body composition and reproduction (Zeuthen, 1953). Bayne & Scullard (1978) reported a range of b values of 0.334).86 in Thais lapillus, in this case related to nutrition. Newell (1973) gives a range of 0.314).59 for Littorina littorea, dependent upon activity. The values for Bullia in the present study vary from 0.21 to 0.80 depending on
w. ~ :;,,,,-,. I00 5O ~
30
0
,,S~
.o-''"
w
I00
• ,,-,.'~.....
.,..-".-'T... OJ'o..,~ . . . ' 0~" . . e"
~20
.... i ....
cO
,oc .50 50
20
~.'~'-'-
sot- , - - - ' ' 5 . " 5~
,~o
50o
Dry Mass (rn~)
.
.
.
.
io
5o
too Dry Mass (rag)
25"C
~
.....
20"C
.....
...... ..........
15"C IO*C
. . . . . . . 15"C .......... IO*C
Fig. 2. The effects of acute temperature change on the respiration of Bullia digitalLs in summer (S) and winter ( W ) .
L 50O
25"C
20"C
Fig, 3. The effects of acute temperature change on the respiration of Bullia pura in summer (S) and winter (W).
109
Respiration in gastropods Table 1. Analysis of the rates of oxygen consumption (Vo2) of B. rhodostoma, B. digitalis and B. pura in summer and winter
Species
Season
B. rhodostoma
n
15 20 25 10 15 20
27 27 27 20 20 20
0.601 0.660 0.701 0.600 0.631 0.653
_+ 0.012 ___0.006 _+ 0.019 + 0.010 __. 0.015 + 0.008
0.701 0.703 0.724 0.623 0.722 0.801
_ 0.063 _+ 0.061 +_ 0.065 + 0.037 _ 0.044 + 0.041
1.00 1.18 1.38 0.69 1.18 1.78
15 20 25 10 15 20
17 17 17 21 21 21
1.010 0.963 1.122 0.700 0.721 0.841
_+ 0.009 + 0.006 + 0.009 + 0.002 + 0.002 + 0.051
0.361 0.436 0.381 0.511 0.554 0.530
_+ 0.005 + 0.008 + 0.006 _+ 0.020 _+ 0.022 + 0.021
0.54 0.66 0.76 0.53 0.66 0.80
15 20 25 10 15 20
18 18 18 8 8 8
0.921 1.072 1.022 0.813 1.121 1.311
_ + + _ + _
0.361 0.324 0.436 0.291 0.230 0.210
+ + + + + _
0.44 0.51 0.87 0.25 0.38 0.54
Summer Winter
B. digitalis
Summer Winter
B. pura
Respiratory rate of a 100 mg animal (plO2mg/hr)
Temperature (' C)
Summer Winter
Regression analysis a + SD b _+ SD
0.088 0.033 0.018 0.049 0.067 0.078
0.005 0.002 0.003 0.011 0.009 0.008
a and b are the constants in the equation logtoVo 2 = a + b IogtoW where W is the dry mass in mg. "n" indicates the number of animals used.
temperature and species, and are well within the published range. The respiration rates for the Bullia species reported here compare well with the metabolic rates of other gastropods. Sandison (1966) reported respiratory rates of 1.0 and 1 . 5 # 1 0 2 m g - t h r -~ at 18°C for Thais lapil/us and Bayne & Scullard (1978) gave values of _+ 1.5/A 0 2 m g - J h r - ~ for the same species. Newell & Pye (1970) measured standard metabolic rates of 0.254).80 #1 O2 m g - t h r - ~ in L. /ittorea and active rates of 1.0-5.0/~1 0 2 rag- ~ h r - ~ in the same species. Studies on Bu/inus africanus by Heeg (1977) yielded a metabolic rate of 1.44 #1 0 2 m g - t h r - t at 25°C, and this seemed to be unaffected by starvation up to 21days. Studies on various littoral snails have yielded metabolic rates of between 1.0 and 2.5 #1 O2 m g - ~ h r - t at 20°C ( M c M a h o n & Russel-
3
Hunter, 1977). Brown et al. (1978) reported respiratory rates of 2.3/A 0 2 rag- t h r - ~ in B. digitalis at 15'~C. A study of the effect of turbulence on the respiratory rate of B. digitalis by Brown (1979) revealed that while a constant level of turbulence (stirring) did not affect the respiratory rate, an increase of approximately 37°o in oxygen c o n s u m p t i o n occurred when the turbulence was continually changing. This level of activity was equated by Brown with conditions in the swash zone of the beach, and appears to approximate the natural active state of the animals. The results of the present study therefore underestimate the active rate by approximately 37%. Both B. rhodostoma and B. digitalis have low and fairly constant Qlo values, independent of season or
w
QIO
[7t L
1"751 ~ ~ " " ",~,
,o
,'~
,~
,;
~'~
~'~
Temperature *C
.......
5OOmg I00 mg IO mg
Fig. 4. The effect of temperature on Qto in Bullia rhodos-
torrut in summer (S) and winter (W).
25J I0
13
S
16
19
22
25
Temperoture °C ....... .......
200mg IOOmg IO rng
Fig. 5. The effect of temperature on Qto in Bullia digitalis in summer (S) and winter (W).
110
A, H. DYE and L. McGwVNNE
S,s ,I,s .f'° ~, f f'W
~°
~.
W
Q~ c_o x O
...... I0
13
IL6
119
22
0
I 0 0 mg
.50 mg
.......
IO rng
-w-
25
Temperature °C .......
-__-'- . . . . . . . .
IO
1'5
20
25
Temperature *C 200rr~
Fig. 6. The effect of temperature on Q~0 in Bulliu pura in summer (S) and winter (W).
tO0 mg IO mg
Fig. 8. Acutely measured rate/temperature curves for three size classes of Bulliu di.qitalis in summer (S) and winter (W).
W J
f.S"
/ "I
./ /
3
!
•/"
~-
./
,! .,~"f
o, iO
"
~
/
S
15 20 Temperature *C
~5 0J ~0
......
500 mg I00 mg I0 mg
Fig. 7. Acutely measured rate/temperature curves for three size classes of Bullia rhodostoma in summer (S) and winter (Wt
mass. B. p , r a has a higher and more variable Qlo, particularly at the lower temperatures, suggesting a lesser degree of metabolic regulation over the measured temperature range t h a n in the other species. This is borne out by the considerable degree of counter-clockwise rotation of the rate/metabolism curve for the small size classes in winter, a characteristic shared to a much smaller extent by B. rhodostoma and not at all by B. digitalis. These findings in the case of B. digitalis correspond with those of Brown (1979) for the west coast populations. The conclusion made by
b
-
-
~
15 20 Temperature *C
......
25
IOOmg 50rng I0 mg
Fig. 9. Acutely measured rate/temperature curves for three size classes of Bullia pura in summer IS1 and winter (Wl.
Brown (1979) that B. digitalis is not acclimatory adaptive ,to temperature is supported in the data for the Indian Ocean population as well as for B. rhodostoma. Bullia pura on the other hand does appear to show a degree of winter and summer acclimation to temperature.
Acknowledgements--The University of Port Elizabeth and the Department of Planning and the Environment are thanked for their financial assistance. Professor T, Erasmis and Dr. A. McLachlan are thanked for their constructive comments and for reading the manuscript.
Respiration in gastropods REFERENCES
BAYNE B. L. & SCULLARD C. (1978) Rates of oxygen consumption by Thais (Nucella) lapillus (L.). J. exp. mar. Biol. Ecol. 32, 97-111. BROWN A. C. (1961) Physiological ecological studies on two sandy beach gastropoda from South Africa; Bullia digitalis Meuschen and Bullia laevissima (Gmelin). Z. Morph. Okol. Tiere. 49, 629-657. BROWN A. C., ANSELL A, D. & TREVALLION A. (1978) Oxygen consumption by Bullia (Dorsanum) melanoides (Deshayes) and Bullia digitalis Meuschen (Gastropoda, Nassaridae~-an example of non-acclimation. Comp. Biochem. Physiol. 61A, 123-125. BROWN A. C. & DA SILVA F. M. (1979) The effect of temperature on oxygen consumption in Bullia digitalis Meuschen (Gastropoda, Nassaridae). Comp. Biochem. Physiol. 62A, 573-576. BROWN A. C. (1979) Oxygen consumption of the sandybeach whelk Bullia digitalis Meuschen at different levels of activity. Comp. Biochem. Physiol. 62A, 673-675. HEEG J. (1977) Oxygen consumption and the use of metabolic reserves during starvation and aestivation in Bulinus (Physopsis) africanus, (Pulmonata : Planorbidae). Malacologia 16~ 549-560.
111
MCLACHLAN A. (1977) Composition, distribution, abundance and biomass of the macrofauna of four sandy beaches. Zool. afr. 12, 279-306. MCLAcHLAN A., COOPER C. t~ VAN DER HORST G. (1979) Growth and production of Bullia rhodostoma Reeve (Mollusca, Gastropoda) on an open sandy beach in Algoa Bay. S. Aft. J. Zool. In press. MCMAHON R. F. & RUSSEL-HUNTER W. D. (1977) Temperature relation of aerial and aquatic respiration in six littoral snails in relation to their vertical zonation. Biol. Bull. 152, 182-198. NEWELL R. C. (1973) Factors affecting the respiration of intertidal invertebrates. Am. Zool, 13, 513 528. NEWELL R. C. & PVE V. 1. (1970) Seasonal changes in the effect of temperature on the oxygen consumption of the winkel Littorina littorea (L.) and the mussel Mytilus edulis L. Comp. Biochem. Physiol. 34A, 367 383. SANDISON R. L. (1966) The oxygen consumption of some intertidal gastropods in relation to zonation. J. Zool. (London) 149, 163-173. TREVALL1ON A. (1971) Studies on Tellina tenuis Da Costa IlL Aspects of general biology and energy flow. J. exp. rrutr. Biol. Ecol. 7, 95-122. ZEUTHEN E. (1953) Oxgen uptake as related to body size in organisms. Q. Rer. Biol. 28, 1-12.