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The heart and water flow rates of Mya arenaria (bivalvia: Mollusca) at different metabolic levels
Camp. Biochem. Physiol., 1972, Vol. 41A, pp. 487 to 494. Pergamon Press. Printed in Great Britain
THE HEART AND WATER FLOW RATES OF MYA ARENARIA (BIVALVIA: MOLLUSCA) AT DIFFERENT METABOLIC LEVELS G. A. LOWE*
and E. R. TRUEMAN
Department of Zoology, The University of Manchester (Receiwed 15 July 1971) The heart and water flow rates of Mya arenaria were continuously monitored during spontaneous and artificially induced periods of activity and inactivity. 2. During activity, as measured by the flow of water through the mantle cavity, the heart rate responded markedly to changes in temperature. When the water flow rate was minimal the heart showed less change in respect of temperature. It is suggested that the former is equivalent to an active metabolic level and the latter is to a standard rate. 3. The heart rate appears to be directly related to metabolic level and is a useful means of continuously monitoring this parameter.
Abstract-l.
INTRODUCTION THE RESPONSEof
various molluscs, such as Cardium edule and Littorina littorea, to changing temperatures is considered by Newell & Northcroft (1967) to vary according to their metabolic state. The standard metabolic rate varies little with temperature (Halcrow & Boyd, 1967; Newell & Northcroft, 1967) but the active metabolic rate alters markedly with temperature (Newell & Pye, 1970). Techniques have been developed recently which enable the heart rate of bivalve molluscs to be continuously monitored (Trueman, 1967). The effect of temperature change on Mya heart rate is recorded on a number of occasions to ascertain first, whether Mya shows two levels of heart activity and second to what extent the heart rate can be taken as diagnostic of different levels of metabolism. Active and standard metabolic rates are also investigated in terms of the flow of water through the mantle cavity and a critical examination is made of the relationship between heart rate and water flow. Previous methods to determine the flow rate produced by the gills of a bivalve have involved direct measurements of water volume, or indirect measurements which determine the rate of particle retention. Galtsoff (1926,1928) calculated flow rates produced by the gills of oysters by inserting a tube in the mantle cavity, and measuring the flow of a column of carmine in a graduated tube. * Present Scotland.
address:
Gatty
Marine Laboratory, 487
The
University,
St. Andrews,
Fife,
488
G. A. LOWE AND E. R. TRUEMAN
Loosanoff & Engle (1947) determined the flow rate of Ostrea virgin&z by collecting the water passed over the gills, using a “rubber apron” stretched over the valves in the region of the exhalant current. Both of these methods have the serious disadvantage of causing great disturbance to the animal, and as Jorgensen (1960) points out, the flow rate of water across the gills can vary enormously with experimental procedure. Indirect measurements of flow rate have been carried out by Jorgensen (1949) and Rao (1953) working using a photo-electric method to determine the rate of clearing of a suspension of particles or by Allen (1962) who calculated the rate of extraction of labelled phosphorus from the water. Mya was chosen for this study since it is suitable for monitoring both heart and water flow rates. Flow measurements may be readily made from the functionally separate inhalant and exhalant siphons without disturbance to the animal by use of a flow meter probe modified from Heusner & Enright (1966).
MATERIALS
AND METHODS
Specimens of Mya armaria L. were collected from the shore at Lytham, Lancashire, 2 days before laboratory recordings commenced, and were stored in an aquarium with a sea-water circulation, maintained at a temperature of 5°C. A tank for experimental work was filled with suflicient sand to enable five specimens to be buried, with their siphons exposed to the water, and was placed in a constant temperature unit with a controllable heating element, which allowed the temperature to be altered at the desired rate. Fine holes were drilled, one in each valve, for the insertion of silver electrodes into the pericardial cavity. The electrodes were attached to a length of light screened cable which led to an impedance pneumograph (Narco Ltd.) designed to detect pulsatile changes. A small oscillatory current (2 PA, 25 kc/s) was passed between the electrodes and the pulsatile changes of ventricular contraction affected the impedance between them, and altered the deflexion of a pen recorder to which the instrument was connected by a.c. coupling. After electrode implantation the specimens were allowed to settle in the tank for 24 hr at 5°C before recordings were made. Water flow recordings were carried out on animals using a flow meter probe and circuitry modified from a method described by Heusner & Enright (1966). The flow meter probe consisted of two miniature glass bead thermistors (S.T.C. thermistor Model U23 US/MP). One thermistor was mounted at the tip of the probe and was exposed to the water flowing out of or into the siphons of Mya. The other thermistor was shielded from the flow, but exposed to the surrounding water. Both thermistors were wired together in such a way that they were heated by a 6 V dry cell to O.S”C above the ambient temperature of the water. The thermistor exposed to the siphonal flow was cooled by the water flowing over it, the difference in temperature between the two thermistors was compared by a wheatstone bridge circuit, and measured as a deflexion on a pen recorder, the amplitude of deflexion depending on the rate of flow. Prior to each series of recordings it was necessary to calibrate the flow meter. The probe was placed in a tank of water, at a measured distance from a tube of known diameter, connected to a burette. The volume of water flowing out of the tube was measured by noting the level in the burette. Calibration was carried out by allowing water to flow out of the burette and each 1 ml was marked on the recorder by the event marker. A series of different flow rates were recorded, giving correspondingly different pen deflexions. To calibrate the flow rates recorded from a specimen, corrections were made for the different diameters of the lumen of the siphons and the internal diameter of the calibration tube. The distance between the probe and the siphons or calibration tube was kept as constant as possible at 2-3 mm.
HEART
AND
WATER
FLOW
RATES
OF
MYA
489
ARENARIA
Although spontaneous periods of low activity were used to make recordings of the effect of temperature change in some experiments, they occurred too spasmodically for use in investigations of flow rate. It was thus found convenient to induce standard rate metaholism by reducing the oxygen content of the water. The water in the experimental tank was aerated by using a piston-type aerator which maintained the oxygen concentration above 80% saturation, measured with a laboratory oxygen analyser (Model 777, Beckman Instruments Inc.). For experiments requiring a reduced oxygen concentration, nitrogen was passed through the water. This method reduced the oxygen concentration to less than 20% saturation and all experiments in reduced oxygen concentration were carried out at this level. Heart rates, in aerated water and water at a reduced oxygen concentration, were recorded continuously while the water temperature was altered at the rate of 1 ‘C/l0 min. Flow rates could only he recorded at steady temperatures as the instrument was affected by temperature changes whilst recordings were made. Therefore it was necessary to select certain temperatures (5, 10, 15 and 20°C) and to maintain them for 10 min while recordings were made. This procedure was carried out both in aerated water and water at a reduced oxygen concentration. RESULTS
The heart of Mya shows two rates according to the level of activity of the clam (Fig. 1) the high rate corresponding to the siphons being open and water flowing through the mantle cavity. A temperature drop of 7°C results in a slowing of both
0
1
4
5
15
IO
20
25
min
FIG. 1. Graph of the response of heart rate (beats/min) to temperature change (“C) (upper graph) during natural periods of activity (a) and inactivity (b) of M. arenaria. Actual temperature reduction was in (a) 24-17°C and in (b) 19-12°C.
490
G. A. LOWE ANDE. R.
TRUEMAN
rates, but there are two degrees of response, a heart beating at a fast initial rate alters markedly (Fig. la), whereas the heart beating at a slow initial rate changes little (Fig. lb). Comparable results were obtained from specimens subjected to a fall in temperature, as illustrated, or a rise in temperature. During natural heart beat suppression the flow rate produced by the action of gill cilia in Mya is very low, but upon acceleration of the heart rate, the flow rate shows a marked increase (Fig. 2). A measurable rate of flow was noted before the exhalant siphon apparently opened, but once the siphon was open the flow rate increased rapidly, showing an
3216 9 . 5-
FIG. 2. Extract from trace showing heart rate of M. arenaria (beata/min) and the rate of flow of water through the mantle cavity (ml/min) recorded from the exhalant siphon. Time mark in min. Siphonal opening indicated by the event mark, 0.
overshoot phenomenon. Mya, therefore shows different rates of flow, controlled by the siphonal aperture or ciliary activity, which are correlated with heart rate. Whether this correlation is due to simultaneous neural control of both heart and cilia or to a result of reduced oxygen tension was not investigated. The heart rate of Myu, when recorded from an animal acclimated to 5°C actively siphoning in aerated water, showed a marked increase in rate with rising temperature (Fig. 3a), Q10 = 2.16, but very little change in water flow rate, Qr,, = 1.05. The heart rate of Mya was suppressed when nitrogen was passed through the water (Fig. 3b) and showed a less marked increase Q1,, = l-84, in water at a low oxygen concentration (Fig. 3b), though the flow rate increased at a similar rate, Q1,, = 1.30, as that from an animal in aerated water. Furthermore, the heart rate of Mya in aerated water was faster than that for Mya in water of reduced oxygen concentration, over the whole range of experimental temperatures (Fig. 3). The
HEART
AND
WA%
FLOW RATES OF &WA ARENARIA
481
FICW
rate
Heart rate
Temperature
Heart rote
5
dp5
I
IO
85
20
Temperature FIG, 3. Graphs of flow rate (ml/min) and heart rate (beats/xx&Q against temperature (“C) in M. arenario. Each point on the graph represents the mean of five specimens with the standard deviation shown by the vertical line about each point. a. Recordings made whilst immersed in aerated sea water; b. Recordings made whilst in water of reduced oxygen concentration.
ow rates recorded from Mya in aerated water were all faster than those recorded from specimens in water of reduced oxygen concentration. In both instances the flow rates of 34~~ increased little with increasing temperature. The flow rates recorded from M@z in water of a reduced oxygen concentration were low even when the siphons were open, therefore the suppressed flow rate is probably due to reduced ciliary activity. DISCUSSION
and standard rates of metabolism have been demonstrated in L. Zittorea and C, edub by Newell & Nor&croft (1967) and in ~~~i~ edu& by Newell & Pye (1970). But these authors leave the meaning of the term “active” open in respect Active
492
G. A. LOWEAND E. R.
TRUEMAN
of bivalves and the use of the terms “active” and “standard” raises the question of what in a sessile bivalve amounts to activity. A bivalve could be considered to be active at any time when the valves or siphons are open and water currents are passing in and out of the mantle cavity. It was thus clearly relevant to monitor water flow and heart rate and to consider how diagnostic are these of different metabolic levels. The heart rate of Mya shows two different responses to temperature change (Fig. 1) which, from the definition of Newell & Northcroft (1967), may be considered to indicate active and standard metabolic levels. Trueman & Lowe (1971) transferred IsognomDn alutus from water to air, when the valves remained very narrowly agape. There was little change in heart rate when the temperature was substantially the same, but movement from water to cooler air gave a recording which was directly comparabfe to that obtained on immersion in cooler water. There was no sign of any overshoot following aerial exposure such as happens as a consequence of valve closure or during littoral exposure of M. eduZis(Helm & Trueman, 1967) and consequent oxygen deficiency. This would suggest that, at shade temperatures, adequate oxygen exchange can take place across the narrow opening of the valve margins where the water contained in the mantle cavity is exposed to the air. Even during direct exposure to the sun in the drying atmosphere of a gentle breeze, Isognomon did not completely close its valves; the heart accelerated in the same manner as if it had been continuously immersed and the water temperature had been raised. Although there can be no inhalant water current, the possibility of the ciliary currents continuing may be envisaged. Thus the mantle cavity water would be circulated, so facilitating oxygen exchange and maint~ning an active rate of metabolism. Reduction of heart rate when in air would suggest reduced activity, but this only occurred either in air or in water, when the valves were completely closed so as to cut off any supply of oxygen. 1. ulutus spasmodically closed its valves completely during continuous immersion with consequent bradycardia (Trueman & Lowe, 1971). This suggests that an active rate obtains whenever the valves or siphons are open and ciliary activity is taking place. Whether two rates of activity occur in other functions of a bivalve was tested by recording the heart rate and water flow rate of M. urenariu. When Mya was subjected to water with an artificially low oxygen concentration, the standard rate was apparently induced. The heart rate of Mya was markedly affected by temperature change only in well-aerated water. Thus the heart rate of Mya shows two levels of response to temperature depending on the availability of oxygen. Water flow rates of bivalves have been shown to increase with increasing temperature in 0. r@%z&z (Galtsoff, 1928; Loosanoff, 1958) and Mercenaria mercenaria (Hamwi, 1969). Although the flow rate of Myu was faster in wellaerated water than in water of reduced oxygen concentration, the flow rates did not show a marked increase with a rise in temperature in either case. From the definition of Newell & Northcroft (1967) it would appear that both these flow rates are at a standard rate, being only slightly affected by temperature. But the flow rate of Myu does here show two distinct rates, depending on oxygen concentration.
HEARTANI3WATERFLOW RATESOF MYA
ARENARIA
493
Apart from valve and siphonal movement there can be little other activity besides water flow through the gills which could be used as a criterion of activity in Mya. Ciliary activity, which produces water currents, does exhibit at least two levels of rate of water flow. These can be taken as being diagnostic of standard or active metabolic levels, in Mya and possibly also in the majority of bivalves. The heart rate of Mya varies with oxygen tension and shows variation in rate with temperatures in the same manner as Newell & Northcroft (1967) have described as active and standard metabolic rates. It therefore seems that heart rate is directly related to metabolism and is a useful means of continuously monitoring metabolic levels in the field or in the laboratory. Criticism of the concept of active and standard rates has been raised by various authors (Tribe & Bowler, 1968; Barnes & Barnes, 1969) but this approach by use of factors to measure activity other than metabolic levels, supports Newell and Northcroft’s hypothesis. REFERENCES ALLEN J. A. (1962) Preliminary experiments on the feeding and excretion of bivalves using Phaeodactylum labelled with 3aP. J. mar. Biol. Ass. U.K. 42, 609-623. BARNESH. & BARNESM. (1969) Seasonal changes in the acutely determined oxygen consumption and effect of temperature for three common cirripedes, Balanus balanoides (L.), Balanus balanus and Chthamalus stellatus (Poli). J. exp. mar. Biol. Ecol. 4, 36-50. GALTSOFFP. S. (1926) New methods to measure the rate of flow produced by the gills of oysters and other molluscs. Science, N. Y. 63, 233-234. GALTSOFFP. S. (1928) The effect of temperature on the mechanical activity of the gills of the oyster (Ostrea virginica Gm.). J. gen. Physiol. 11, 415-431. HALCROWK. & BOYD C. M. (1967) The oxygen consumption and swimming activity of the amphipod Gammarus oceanicus at different temperatures. Comp. Biochem. Physiol. 23, 233-242. HAMWI A. (1969) Oxygen consumption and pumping rates of the hard shelled clam Mercenaria mercenaria L. Ph.D. thesis, Rutgers State University, Diss. Abstr. 30 (7) 3433-B. HELM M. M. & TRUEMANE. R. (1967). The effect of exposure on the heart rate of the mussel Mytilus edulis L. Comp. Biochem. Physiol. 21, 171-177. HEUSNERA. A. & ENRICHT J. T. (1966) Long term recording in small aquatic animals. Science, N. Y. 154, 532-533. JORGENSENC. B. (1949) The rate of feeding of Mytilus in different kinds of suspension. J. mar. Biol. Ass. U.K. 28, 333-344. JORGENSENC. B. (1960) Efficiency of particle retention and rate of water transport in undisturbed lamellibranchs. J. Cons. perm. int. Explor. Mer. 26,94-l 16. LOOSANOFFV. L. (1958) Some aspects of behaviour of oysters at different temperatures. Biol. Bull. mar. biol. Lab., Woods Hole 114, 57-70. LOOSANOFF V. L. & ENGLE J. B. (1947) Effect of different concentrations of micro-organisms on the feeding of oysters (Ostrea virginica). Fishery Bull. Fish. Wildl. Serv. U.S. 51, 31-57. NEWELL R. C. & NORTHCROFT H. R. (1967) A reinterpretation of the effect of temperature on the metabolism of certain marine invertebrates. J. Zool., Lond. 151, 277-298. NEWELL R. C. & PYE V. I. (1970) Seasonal changes in the effect of temperature on the oxygen consumption of the winkle Littorina littorea and the mussel Mytilus edulis. Comp. Biochem. Physiol. 34, 367-383.
494
G. A. LOWB ANDE. R.
TRUEMAN
K. P. (1953) Rate of water propulsion in ~yti~~ cffl~o~i~~s as a function of latitude. Biol. SuU. tnar. biol. Lab., W55dr Hole 104, 171-181. TIUBE M. A. & BOWLBRK. (1968) Temperature dependence of “standard metabolic rate” in a poikilotherm. Cozn~. Biochem. Physiol. 25, 427-436. TRWMAN E. R. (1967) Activity and heart rate of bivalve molluscs in their natural habitat. Nature, Lord. 214, 832-833. TRUEMANE. R. & Lowe G. A. (1971) The effect of temperature and littoral exposure on the heart rate of a bivalve mollusc, Isognomon alatus, in tropical conditions. Camp. Biochem. Physiol. 38A, 555-564. ho
Key Word Index-Heart arena&z.
rate; water flow rate; metabolic level; temperature;
Mya
THE HEART AND WATER FLOW RATES OF MYA ARENARIA (BIVALVIA: MOLLUSCA) AT DIFFERENT METABOLIC LEVELS G. A. LOWE*
and E. R. TRUEMAN
Department of Zoology, The University of Manchester (Receiwed 15 July 1971) The heart and water flow rates of Mya arenaria were continuously monitored during spontaneous and artificially induced periods of activity and inactivity. 2. During activity, as measured by the flow of water through the mantle cavity, the heart rate responded markedly to changes in temperature. When the water flow rate was minimal the heart showed less change in respect of temperature. It is suggested that the former is equivalent to an active metabolic level and the latter is to a standard rate. 3. The heart rate appears to be directly related to metabolic level and is a useful means of continuously monitoring this parameter.
Abstract-l.
INTRODUCTION THE RESPONSEof
various molluscs, such as Cardium edule and Littorina littorea, to changing temperatures is considered by Newell & Northcroft (1967) to vary according to their metabolic state. The standard metabolic rate varies little with temperature (Halcrow & Boyd, 1967; Newell & Northcroft, 1967) but the active metabolic rate alters markedly with temperature (Newell & Pye, 1970). Techniques have been developed recently which enable the heart rate of bivalve molluscs to be continuously monitored (Trueman, 1967). The effect of temperature change on Mya heart rate is recorded on a number of occasions to ascertain first, whether Mya shows two levels of heart activity and second to what extent the heart rate can be taken as diagnostic of different levels of metabolism. Active and standard metabolic rates are also investigated in terms of the flow of water through the mantle cavity and a critical examination is made of the relationship between heart rate and water flow. Previous methods to determine the flow rate produced by the gills of a bivalve have involved direct measurements of water volume, or indirect measurements which determine the rate of particle retention. Galtsoff (1926,1928) calculated flow rates produced by the gills of oysters by inserting a tube in the mantle cavity, and measuring the flow of a column of carmine in a graduated tube. * Present Scotland.
address:
Gatty
Marine Laboratory, 487
The
University,
St. Andrews,
Fife,
488
G. A. LOWE AND E. R. TRUEMAN
Loosanoff & Engle (1947) determined the flow rate of Ostrea virgin&z by collecting the water passed over the gills, using a “rubber apron” stretched over the valves in the region of the exhalant current. Both of these methods have the serious disadvantage of causing great disturbance to the animal, and as Jorgensen (1960) points out, the flow rate of water across the gills can vary enormously with experimental procedure. Indirect measurements of flow rate have been carried out by Jorgensen (1949) and Rao (1953) working using a photo-electric method to determine the rate of clearing of a suspension of particles or by Allen (1962) who calculated the rate of extraction of labelled phosphorus from the water. Mya was chosen for this study since it is suitable for monitoring both heart and water flow rates. Flow measurements may be readily made from the functionally separate inhalant and exhalant siphons without disturbance to the animal by use of a flow meter probe modified from Heusner & Enright (1966).
MATERIALS
AND METHODS
Specimens of Mya armaria L. were collected from the shore at Lytham, Lancashire, 2 days before laboratory recordings commenced, and were stored in an aquarium with a sea-water circulation, maintained at a temperature of 5°C. A tank for experimental work was filled with suflicient sand to enable five specimens to be buried, with their siphons exposed to the water, and was placed in a constant temperature unit with a controllable heating element, which allowed the temperature to be altered at the desired rate. Fine holes were drilled, one in each valve, for the insertion of silver electrodes into the pericardial cavity. The electrodes were attached to a length of light screened cable which led to an impedance pneumograph (Narco Ltd.) designed to detect pulsatile changes. A small oscillatory current (2 PA, 25 kc/s) was passed between the electrodes and the pulsatile changes of ventricular contraction affected the impedance between them, and altered the deflexion of a pen recorder to which the instrument was connected by a.c. coupling. After electrode implantation the specimens were allowed to settle in the tank for 24 hr at 5°C before recordings were made. Water flow recordings were carried out on animals using a flow meter probe and circuitry modified from a method described by Heusner & Enright (1966). The flow meter probe consisted of two miniature glass bead thermistors (S.T.C. thermistor Model U23 US/MP). One thermistor was mounted at the tip of the probe and was exposed to the water flowing out of or into the siphons of Mya. The other thermistor was shielded from the flow, but exposed to the surrounding water. Both thermistors were wired together in such a way that they were heated by a 6 V dry cell to O.S”C above the ambient temperature of the water. The thermistor exposed to the siphonal flow was cooled by the water flowing over it, the difference in temperature between the two thermistors was compared by a wheatstone bridge circuit, and measured as a deflexion on a pen recorder, the amplitude of deflexion depending on the rate of flow. Prior to each series of recordings it was necessary to calibrate the flow meter. The probe was placed in a tank of water, at a measured distance from a tube of known diameter, connected to a burette. The volume of water flowing out of the tube was measured by noting the level in the burette. Calibration was carried out by allowing water to flow out of the burette and each 1 ml was marked on the recorder by the event marker. A series of different flow rates were recorded, giving correspondingly different pen deflexions. To calibrate the flow rates recorded from a specimen, corrections were made for the different diameters of the lumen of the siphons and the internal diameter of the calibration tube. The distance between the probe and the siphons or calibration tube was kept as constant as possible at 2-3 mm.
HEART
AND
WATER
FLOW
RATES
OF
MYA
489
ARENARIA
Although spontaneous periods of low activity were used to make recordings of the effect of temperature change in some experiments, they occurred too spasmodically for use in investigations of flow rate. It was thus found convenient to induce standard rate metaholism by reducing the oxygen content of the water. The water in the experimental tank was aerated by using a piston-type aerator which maintained the oxygen concentration above 80% saturation, measured with a laboratory oxygen analyser (Model 777, Beckman Instruments Inc.). For experiments requiring a reduced oxygen concentration, nitrogen was passed through the water. This method reduced the oxygen concentration to less than 20% saturation and all experiments in reduced oxygen concentration were carried out at this level. Heart rates, in aerated water and water at a reduced oxygen concentration, were recorded continuously while the water temperature was altered at the rate of 1 ‘C/l0 min. Flow rates could only he recorded at steady temperatures as the instrument was affected by temperature changes whilst recordings were made. Therefore it was necessary to select certain temperatures (5, 10, 15 and 20°C) and to maintain them for 10 min while recordings were made. This procedure was carried out both in aerated water and water at a reduced oxygen concentration. RESULTS
The heart of Mya shows two rates according to the level of activity of the clam (Fig. 1) the high rate corresponding to the siphons being open and water flowing through the mantle cavity. A temperature drop of 7°C results in a slowing of both
0
1
4
5
15
IO
20
25
min
FIG. 1. Graph of the response of heart rate (beats/min) to temperature change (“C) (upper graph) during natural periods of activity (a) and inactivity (b) of M. arenaria. Actual temperature reduction was in (a) 24-17°C and in (b) 19-12°C.
490
G. A. LOWE ANDE. R.
TRUEMAN
rates, but there are two degrees of response, a heart beating at a fast initial rate alters markedly (Fig. la), whereas the heart beating at a slow initial rate changes little (Fig. lb). Comparable results were obtained from specimens subjected to a fall in temperature, as illustrated, or a rise in temperature. During natural heart beat suppression the flow rate produced by the action of gill cilia in Mya is very low, but upon acceleration of the heart rate, the flow rate shows a marked increase (Fig. 2). A measurable rate of flow was noted before the exhalant siphon apparently opened, but once the siphon was open the flow rate increased rapidly, showing an
3216 9 . 5-
FIG. 2. Extract from trace showing heart rate of M. arenaria (beata/min) and the rate of flow of water through the mantle cavity (ml/min) recorded from the exhalant siphon. Time mark in min. Siphonal opening indicated by the event mark, 0.
overshoot phenomenon. Mya, therefore shows different rates of flow, controlled by the siphonal aperture or ciliary activity, which are correlated with heart rate. Whether this correlation is due to simultaneous neural control of both heart and cilia or to a result of reduced oxygen tension was not investigated. The heart rate of Myu, when recorded from an animal acclimated to 5°C actively siphoning in aerated water, showed a marked increase in rate with rising temperature (Fig. 3a), Q10 = 2.16, but very little change in water flow rate, Qr,, = 1.05. The heart rate of Mya was suppressed when nitrogen was passed through the water (Fig. 3b) and showed a less marked increase Q1,, = l-84, in water at a low oxygen concentration (Fig. 3b), though the flow rate increased at a similar rate, Q1,, = 1.30, as that from an animal in aerated water. Furthermore, the heart rate of Mya in aerated water was faster than that for Mya in water of reduced oxygen concentration, over the whole range of experimental temperatures (Fig. 3). The
HEART
AND
WA%
FLOW RATES OF &WA ARENARIA
481
FICW
rate
Heart rate
Temperature
Heart rote
5
dp5
I
IO
85
20
Temperature FIG, 3. Graphs of flow rate (ml/min) and heart rate (beats/xx&Q against temperature (“C) in M. arenario. Each point on the graph represents the mean of five specimens with the standard deviation shown by the vertical line about each point. a. Recordings made whilst immersed in aerated sea water; b. Recordings made whilst in water of reduced oxygen concentration.
ow rates recorded from Mya in aerated water were all faster than those recorded from specimens in water of reduced oxygen concentration. In both instances the flow rates of 34~~ increased little with increasing temperature. The flow rates recorded from M@z in water of a reduced oxygen concentration were low even when the siphons were open, therefore the suppressed flow rate is probably due to reduced ciliary activity. DISCUSSION
and standard rates of metabolism have been demonstrated in L. Zittorea and C, edub by Newell & Nor&croft (1967) and in ~~~i~ edu& by Newell & Pye (1970). But these authors leave the meaning of the term “active” open in respect Active
492
G. A. LOWEAND E. R.
TRUEMAN
of bivalves and the use of the terms “active” and “standard” raises the question of what in a sessile bivalve amounts to activity. A bivalve could be considered to be active at any time when the valves or siphons are open and water currents are passing in and out of the mantle cavity. It was thus clearly relevant to monitor water flow and heart rate and to consider how diagnostic are these of different metabolic levels. The heart rate of Mya shows two different responses to temperature change (Fig. 1) which, from the definition of Newell & Northcroft (1967), may be considered to indicate active and standard metabolic levels. Trueman & Lowe (1971) transferred IsognomDn alutus from water to air, when the valves remained very narrowly agape. There was little change in heart rate when the temperature was substantially the same, but movement from water to cooler air gave a recording which was directly comparabfe to that obtained on immersion in cooler water. There was no sign of any overshoot following aerial exposure such as happens as a consequence of valve closure or during littoral exposure of M. eduZis(Helm & Trueman, 1967) and consequent oxygen deficiency. This would suggest that, at shade temperatures, adequate oxygen exchange can take place across the narrow opening of the valve margins where the water contained in the mantle cavity is exposed to the air. Even during direct exposure to the sun in the drying atmosphere of a gentle breeze, Isognomon did not completely close its valves; the heart accelerated in the same manner as if it had been continuously immersed and the water temperature had been raised. Although there can be no inhalant water current, the possibility of the ciliary currents continuing may be envisaged. Thus the mantle cavity water would be circulated, so facilitating oxygen exchange and maint~ning an active rate of metabolism. Reduction of heart rate when in air would suggest reduced activity, but this only occurred either in air or in water, when the valves were completely closed so as to cut off any supply of oxygen. 1. ulutus spasmodically closed its valves completely during continuous immersion with consequent bradycardia (Trueman & Lowe, 1971). This suggests that an active rate obtains whenever the valves or siphons are open and ciliary activity is taking place. Whether two rates of activity occur in other functions of a bivalve was tested by recording the heart rate and water flow rate of M. urenariu. When Mya was subjected to water with an artificially low oxygen concentration, the standard rate was apparently induced. The heart rate of Mya was markedly affected by temperature change only in well-aerated water. Thus the heart rate of Mya shows two levels of response to temperature depending on the availability of oxygen. Water flow rates of bivalves have been shown to increase with increasing temperature in 0. r@%z&z (Galtsoff, 1928; Loosanoff, 1958) and Mercenaria mercenaria (Hamwi, 1969). Although the flow rate of Myu was faster in wellaerated water than in water of reduced oxygen concentration, the flow rates did not show a marked increase with a rise in temperature in either case. From the definition of Newell & Northcroft (1967) it would appear that both these flow rates are at a standard rate, being only slightly affected by temperature. But the flow rate of Myu does here show two distinct rates, depending on oxygen concentration.
HEARTANI3WATERFLOW RATESOF MYA
ARENARIA
493
Apart from valve and siphonal movement there can be little other activity besides water flow through the gills which could be used as a criterion of activity in Mya. Ciliary activity, which produces water currents, does exhibit at least two levels of rate of water flow. These can be taken as being diagnostic of standard or active metabolic levels, in Mya and possibly also in the majority of bivalves. The heart rate of Mya varies with oxygen tension and shows variation in rate with temperatures in the same manner as Newell & Northcroft (1967) have described as active and standard metabolic rates. It therefore seems that heart rate is directly related to metabolism and is a useful means of continuously monitoring metabolic levels in the field or in the laboratory. Criticism of the concept of active and standard rates has been raised by various authors (Tribe & Bowler, 1968; Barnes & Barnes, 1969) but this approach by use of factors to measure activity other than metabolic levels, supports Newell and Northcroft’s hypothesis. REFERENCES ALLEN J. A. (1962) Preliminary experiments on the feeding and excretion of bivalves using Phaeodactylum labelled with 3aP. J. mar. Biol. Ass. U.K. 42, 609-623. BARNESH. & BARNESM. (1969) Seasonal changes in the acutely determined oxygen consumption and effect of temperature for three common cirripedes, Balanus balanoides (L.), Balanus balanus and Chthamalus stellatus (Poli). J. exp. mar. Biol. Ecol. 4, 36-50. GALTSOFFP. S. (1926) New methods to measure the rate of flow produced by the gills of oysters and other molluscs. Science, N. Y. 63, 233-234. GALTSOFFP. S. (1928) The effect of temperature on the mechanical activity of the gills of the oyster (Ostrea virginica Gm.). J. gen. Physiol. 11, 415-431. HALCROWK. & BOYD C. M. (1967) The oxygen consumption and swimming activity of the amphipod Gammarus oceanicus at different temperatures. Comp. Biochem. Physiol. 23, 233-242. HAMWI A. (1969) Oxygen consumption and pumping rates of the hard shelled clam Mercenaria mercenaria L. Ph.D. thesis, Rutgers State University, Diss. Abstr. 30 (7) 3433-B. HELM M. M. & TRUEMANE. R. (1967). The effect of exposure on the heart rate of the mussel Mytilus edulis L. Comp. Biochem. Physiol. 21, 171-177. HEUSNERA. A. & ENRICHT J. T. (1966) Long term recording in small aquatic animals. Science, N. Y. 154, 532-533. JORGENSENC. B. (1949) The rate of feeding of Mytilus in different kinds of suspension. J. mar. Biol. Ass. U.K. 28, 333-344. JORGENSENC. B. (1960) Efficiency of particle retention and rate of water transport in undisturbed lamellibranchs. J. Cons. perm. int. Explor. Mer. 26,94-l 16. LOOSANOFFV. L. (1958) Some aspects of behaviour of oysters at different temperatures. Biol. Bull. mar. biol. Lab., Woods Hole 114, 57-70. LOOSANOFF V. L. & ENGLE J. B. (1947) Effect of different concentrations of micro-organisms on the feeding of oysters (Ostrea virginica). Fishery Bull. Fish. Wildl. Serv. U.S. 51, 31-57. NEWELL R. C. & NORTHCROFT H. R. (1967) A reinterpretation of the effect of temperature on the metabolism of certain marine invertebrates. J. Zool., Lond. 151, 277-298. NEWELL R. C. & PYE V. I. (1970) Seasonal changes in the effect of temperature on the oxygen consumption of the winkle Littorina littorea and the mussel Mytilus edulis. Comp. Biochem. Physiol. 34, 367-383.
494
G. A. LOWB ANDE. R.
TRUEMAN
K. P. (1953) Rate of water propulsion in ~yti~~ cffl~o~i~~s as a function of latitude. Biol. SuU. tnar. biol. Lab., W55dr Hole 104, 171-181. TIUBE M. A. & BOWLBRK. (1968) Temperature dependence of “standard metabolic rate” in a poikilotherm. Cozn~. Biochem. Physiol. 25, 427-436. TRWMAN E. R. (1967) Activity and heart rate of bivalve molluscs in their natural habitat. Nature, Lord. 214, 832-833. TRUEMANE. R. & Lowe G. A. (1971) The effect of temperature and littoral exposure on the heart rate of a bivalve mollusc, Isognomon alatus, in tropical conditions. Camp. Biochem. Physiol. 38A, 555-564. ho
Key Word Index-Heart arena&z.
rate; water flow rate; metabolic level; temperature;
Mya