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Heart rates of sea snakes diving in the sea
HEART RATES OF SEA SNAKES DIVING IN THE SEA HAROLD HEATWOLE,* ROGER S. SEyMouRt and M. E. D. WEBS~ER~ *Department of Zoology, University of New England, Armidale, N.S.W., 2351, Australia; tDepartment of Zoology, University of Adelaide. Adelaide. IDepartment of Physiology, University of New England. Armidale, (Received
10 March
S.A., Australia; N.S.W.. 2351. Australia
1978)
Abstract-l. 2. Activity
Classical diving bradycardia was not evident in sea snakes diving in the sea. increases heart rate both in apneic and in breathing snakes: there is a breathing tachycardia in the laboratory and in the sea. 3. Heart rates obtained from animals diving in the sea (26 m depth) were similar to those obtained under laboratory conditions if allowances are made for activity differences. 4. Handling and stress increases heart rates of sea snakes.
INTRODUCTION
with signal lights attached to a float. It was also likely that the drag from the EKG leads (total weight 7.5 g) sometimes hindered free movement of the smaller snakes. Despite all of these difficulties, clear records of cardiac and electromyographic activity were obtained for several hours in four instances. Useful data were also obtained from one snake on two occasions. The data presented below represent the only information currently available on heart rates of sea snakes in their natural environment.
In laboratory aquaria, the heart rate of sea snakes is higher during breathing than during apnea (Heatwole, 1977). However, laboratory conditions greatly restrict the range of currents, depths and other factors normally encountered in the sea and they may prevent expression of normal activity pattern. The present study was therefore undertaken to ascertain whether the heart rate changes observed in the laboratory were similar to those of snakes in their natural marine environment.
RESULTS Satisfactory
MATERIALS
AND METHODS
tophis
data were obtained
from three Acalyp-
in the sea. One of them had of 46 beats per minute (b.p.m.) at the peronii
a heart
time of breathing at the surface; 6 min after diving this dropped to 38 b.p.m. Eleven minutes later the snake surfaced and remained active there for 35 min during which time electromyographic signals and movement artifacts obscurred the EKG recording. A second individual had heart rate of 43 b.p.m. immediately before entry into the sea. On entry, heart rate increased and was 5@55 b.p.m. during 36 of the 38 min it swam actively on the surface (for the two exceptional minutes, heart rates were 49 and 45 b.p.m.). The recording became unreadable upon diving. A third individual maintained heart rate between 48 and 54 b.p.m. for 74 min during most of which it was active on the surface; it breathed once, and dived once with little correlation between heart rate and any of these activities. The reluctance of this small and slender species to dive under the experimental conditions, its unusually high level of activity and heart rate suggests that these snakes were affected by the EKG leads. However, this problem was encountered only during periods of very strong currents in the larger, bulkier Aipysurus /a&s, and the remaining data were obtained from a 115Og individual of that species (Table 1, Fig. 1). The highest heart rates (X = 42.1 b.p.m.) were encountered when the snake’s locomotion was influenced by a strong tidal drag on the EKG lead; on another dive, mean heart rate was 28.8 b.p.m. rate
Sea snakes, Aipysurus laeuis and Acalyptophis peronii, were captured by hand-netting or with Pilstrom tongs at Ashmore Reef, Timor Sea, in January 1973. They were kept in sea water in large plastic garbage bins in a temperature-controlled laboratory (25-28°C) aboard the R.V. Alpha Helix for several days before use. Heart rate was monitored using 400 m of double-strand, enamelled, copper bathythermograph wire. Approximately 1 cm sections of bared wire inserted through the skin laterally and rostra1 or caudal of the heart served as electrodes. The sites of attachment were sealed and waterproofed with tissue adhesive followed by an application of latex cement. The electrocardiograph signal received was generally in the range l&30 pV, having been attenuated by the long length of wire lead. Electromyograph patterns from movement and exhalation were also recorded via these leads. Signals from the electrodes were passed through a narrow band filter (50-80 Hz) to reduce noise artifacts and were then amplified by a Tectronix 122 pre-amplifier and Hewlett& Packard Oscilloscope amplifier giving an overall system gain of at least 1000. EKG and EMG activity were continuously recorded on a Brush 2-channel pen-recorder. Snakes equipped with electrodes were released into the sea from bins lowered from the ship’s fantail. The EKG line was played out from a reel as the snake’s movements demanded. An observer on the fantail passed commentary on snakes’ activities to the recording laboratory via a two way intercommunication system. The ship was anchored in 26 m (85 ft) of water. Electrical noise, water currents and snagging of the long EKG leads on coral and other obstructions presented considerable difficulties. Attempts by divers to report on snake activity patterns under water were also sometimes frustrated by strong currents and difficulties in visual contact
when the snake was hindered pulling it back to the ship. Just 453
in its locomotion by after (and presumably
HAROLD Htx’IWoLt,
454
I
ROGI:R S. SFYMOIIR
I
I
JO
20
and
M. E. D. WI ISI I-K
I
I
I
I
I
I
30
40
50
60
70
80
Min
Fig. 1. Heart rate of an Aipysurus Iamis in the sea. Arrow the surface. Activity after diving was variable but moderate.
indicates diving just after a breath on Dashed lines indicate periods in which
the trace was not readable. during) handling and placement of the leads, heart rate was elevated to rather high levels (X = 32.5 b.p.m.). These high rates can be attributed to emotional disturbance and to unusual physical exertion and although they do indicate the scope of heart rate in emergencies. they may not pertain to conditions experienced during daily activities. In calm water when currents were weak. the mean apneic heart rate was about 21 b.p.m. during variable but moderate activity but increased to just over 36
Table
1. Heart
rates of an Aipysurus
luecis in the sea and
in a bin of water on deck BEATS PERMINUTE
b.p.m. when highly active (compared to about 22 and 23 b.p.m., respectively, for inactive and moderately active apneic snakes on deck). At the surface while breathing, mean heart rate was about 34 b.p.m. as compared to 29 b.p.m. for the same snake inactive but breathing on deck. The resting heart rate measured when the snake was observed to be on the bottom of the sea was 13 b.p.m. This was lower than resting rates obtained on deck for most periods but was very similar to those of one 1%min period (?c = 14.3 b.p.m.: Table I). A similariy low heart rate was later obtained for long periods from a submerged inactive snake. presumed to be on the bottom, but not directly observed there. In the present study. breathing values obtained on deck were somewhat higher than the breathing heart rates previously reported for this species in the laboratory although the ranges considerably overlapped (20-32, R = 29.0 in the present study; 20-24. S = 21.2; Heatwole, 1977). DISCUSSION
BR!&4IHING Deck
29.0
20-32
25
sea
33.8
34-36
5
N refers to numbers of minutes of readable recording.
The present study shows that stress and activity are the main factors affecting the heart rate of both apneic and breathing sea snakes, The bradycardia typically shown by endothermic divers despite high levels of activity does not occur in sea snakes. This view is supported by the findings of Seymour & Webster (1975), Heatwole & Seymour (1976) Baldwin & Seymour (1977) and Heatwole (1977) which indicate that significant levels of anaerobic metabolism leading to the build-up of lactate does not normally take place, nor does depletion of oxygen reserves occur. Ten species of terrestrial and aquatic snakes, including four sea snakes, showed no correlation between diving behavior and levels of glycolytic enzymes (lactate dehydrogenase, phosphofructokinase, phosphorylase and hexokinase) (Baldwin & Seymour, 1977); furthermore, lactic acid concentration was generally quite low in the blood of three
Heart
rates of diving
species of sea snake captured immediately following voluntary dives at sea (Seymour, unpublished data). During most dives, these snakes apparently remain aerobic. Indeed, in view of the marked ability of sea snakes to exchange respiratory gases cutaneously (Graham, 1974; Heatwole & Seymour, 1975~. h, in press) the “diving response” syndrome would be disadvantageous as it would reduce the effectiveness of cutaneous perfusion (Heatwole, 1978). Heatwole (1977, 1978) has suggested that observed heart rate changes in sea snakes represent breathing tachycardia which promotes lung perfusion and oxygen uptake when ventilation occurs. The heart rates obtained from animals in the sea were similar to those obtained under laboratory conditions for animals of comparable activity. The heart rate of the snake on the bottom (13 b.p.m.) was identical to the mean resting apneic heart rate of four individuals (71 min total) of this species reported by Heatwole (1977) and similar to the lower values of the snake of the present study when apneic and inactive on deck (Table 1). Although during apnea, heart rates were slightly lower at sea than on deck, the heart rates of the snakes when breathing were higher at sea. The snake on deck had a mean breathing heart rate of 29 b.p.m. whereas when in the sea it was about 34 b.p.m. This difference is probably attributable to an effect of activity superimposed upon breathing tachycardia; on deck the snake had only to raise its head to the surface to breathe whereas in the sea it had to swim up from the bottom, and therefore undergo greater activity, to do so. It appears overall that heart rates of sea snakes obtained under laboratory conditions are similar to
455
snakes
those experienced by the animals in nature as long as allowances are made for differences in activity level. Acknowlcdgernents~This work was supported by the Nat&al Science Foundation (U.S.A.) under grants GA-35835, GA-34948 and CD-34462 to the Scripps Institution for the Alpha Helix Research Program. We are grateful to W. A. Dunson for aid and encouragement, to Waiter Schneider for technical assistance and to Viola Watt and Neva Walden for help in preparation of the manuscript. REFERENCES BALDWIN J. & SEYMOURR. S. (1977) Adaptation to anoxia in snakes: levels of glycolytic enzymes in skeletal muscle. Aust. J. Zoo/. 25. 9-13. GRAHAM J. B. (1974) Aquatic respiration in the sea snake Pelamis platurus. Respir. Physiol. 21, l-7. HEATWOLE H. (1977) Heart rate during breathing and apnea in marine snakes (Reptilia, Serpentes). J. Herp. II, 67-76. HEATWOLE H. (1978) Adaptation of marine snakes. Am. Sci., In press. HEATWOLE H. & SEYMOUR R. (1975~) Pulmonary and cutaneous oxygen uptake in sea snakes and a file snake. Comp. Biochem. Physiol. 51A, 399-405. HEATWOLE H. & SEYMOUR R. (1975h) Diving physiology. In The Biology of Sea Snukes (Edited by DUNSON W. A.), pp. 289-327. University Park Press, Baltimore. HEATWOLE H. & SEYMOUR R. (1976) Respiration of marine snakes. In Respiration of Amphibious Vertebrates (Edited by HUGHES G. M.), pp. 375-389 Academic Press, New York. HEATWOLEH. & SEYMOURR. (in press) Cutaneous oxygen uptake in three groups of aquatic snakes. Aust. J. Zool. SEYMOURR. S. & WEBSTERM. E. D. (1975) Gas transport and blood acid-base balance in diving sea snakes. J. exp. Zoo\. 191, 169-181.
10 March
S.A., Australia; N.S.W.. 2351. Australia
1978)
Abstract-l. 2. Activity
Classical diving bradycardia was not evident in sea snakes diving in the sea. increases heart rate both in apneic and in breathing snakes: there is a breathing tachycardia in the laboratory and in the sea. 3. Heart rates obtained from animals diving in the sea (26 m depth) were similar to those obtained under laboratory conditions if allowances are made for activity differences. 4. Handling and stress increases heart rates of sea snakes.
INTRODUCTION
with signal lights attached to a float. It was also likely that the drag from the EKG leads (total weight 7.5 g) sometimes hindered free movement of the smaller snakes. Despite all of these difficulties, clear records of cardiac and electromyographic activity were obtained for several hours in four instances. Useful data were also obtained from one snake on two occasions. The data presented below represent the only information currently available on heart rates of sea snakes in their natural environment.
In laboratory aquaria, the heart rate of sea snakes is higher during breathing than during apnea (Heatwole, 1977). However, laboratory conditions greatly restrict the range of currents, depths and other factors normally encountered in the sea and they may prevent expression of normal activity pattern. The present study was therefore undertaken to ascertain whether the heart rate changes observed in the laboratory were similar to those of snakes in their natural marine environment.
RESULTS Satisfactory
MATERIALS
AND METHODS
tophis
data were obtained
from three Acalyp-
in the sea. One of them had of 46 beats per minute (b.p.m.) at the peronii
a heart
time of breathing at the surface; 6 min after diving this dropped to 38 b.p.m. Eleven minutes later the snake surfaced and remained active there for 35 min during which time electromyographic signals and movement artifacts obscurred the EKG recording. A second individual had heart rate of 43 b.p.m. immediately before entry into the sea. On entry, heart rate increased and was 5@55 b.p.m. during 36 of the 38 min it swam actively on the surface (for the two exceptional minutes, heart rates were 49 and 45 b.p.m.). The recording became unreadable upon diving. A third individual maintained heart rate between 48 and 54 b.p.m. for 74 min during most of which it was active on the surface; it breathed once, and dived once with little correlation between heart rate and any of these activities. The reluctance of this small and slender species to dive under the experimental conditions, its unusually high level of activity and heart rate suggests that these snakes were affected by the EKG leads. However, this problem was encountered only during periods of very strong currents in the larger, bulkier Aipysurus /a&s, and the remaining data were obtained from a 115Og individual of that species (Table 1, Fig. 1). The highest heart rates (X = 42.1 b.p.m.) were encountered when the snake’s locomotion was influenced by a strong tidal drag on the EKG lead; on another dive, mean heart rate was 28.8 b.p.m. rate
Sea snakes, Aipysurus laeuis and Acalyptophis peronii, were captured by hand-netting or with Pilstrom tongs at Ashmore Reef, Timor Sea, in January 1973. They were kept in sea water in large plastic garbage bins in a temperature-controlled laboratory (25-28°C) aboard the R.V. Alpha Helix for several days before use. Heart rate was monitored using 400 m of double-strand, enamelled, copper bathythermograph wire. Approximately 1 cm sections of bared wire inserted through the skin laterally and rostra1 or caudal of the heart served as electrodes. The sites of attachment were sealed and waterproofed with tissue adhesive followed by an application of latex cement. The electrocardiograph signal received was generally in the range l&30 pV, having been attenuated by the long length of wire lead. Electromyograph patterns from movement and exhalation were also recorded via these leads. Signals from the electrodes were passed through a narrow band filter (50-80 Hz) to reduce noise artifacts and were then amplified by a Tectronix 122 pre-amplifier and Hewlett& Packard Oscilloscope amplifier giving an overall system gain of at least 1000. EKG and EMG activity were continuously recorded on a Brush 2-channel pen-recorder. Snakes equipped with electrodes were released into the sea from bins lowered from the ship’s fantail. The EKG line was played out from a reel as the snake’s movements demanded. An observer on the fantail passed commentary on snakes’ activities to the recording laboratory via a two way intercommunication system. The ship was anchored in 26 m (85 ft) of water. Electrical noise, water currents and snagging of the long EKG leads on coral and other obstructions presented considerable difficulties. Attempts by divers to report on snake activity patterns under water were also sometimes frustrated by strong currents and difficulties in visual contact
when the snake was hindered pulling it back to the ship. Just 453
in its locomotion by after (and presumably
HAROLD Htx’IWoLt,
454
I
ROGI:R S. SFYMOIIR
I
I
JO
20
and
M. E. D. WI ISI I-K
I
I
I
I
I
I
30
40
50
60
70
80
Min
Fig. 1. Heart rate of an Aipysurus Iamis in the sea. Arrow the surface. Activity after diving was variable but moderate.
indicates diving just after a breath on Dashed lines indicate periods in which
the trace was not readable. during) handling and placement of the leads, heart rate was elevated to rather high levels (X = 32.5 b.p.m.). These high rates can be attributed to emotional disturbance and to unusual physical exertion and although they do indicate the scope of heart rate in emergencies. they may not pertain to conditions experienced during daily activities. In calm water when currents were weak. the mean apneic heart rate was about 21 b.p.m. during variable but moderate activity but increased to just over 36
Table
1. Heart
rates of an Aipysurus
luecis in the sea and
in a bin of water on deck BEATS PERMINUTE
b.p.m. when highly active (compared to about 22 and 23 b.p.m., respectively, for inactive and moderately active apneic snakes on deck). At the surface while breathing, mean heart rate was about 34 b.p.m. as compared to 29 b.p.m. for the same snake inactive but breathing on deck. The resting heart rate measured when the snake was observed to be on the bottom of the sea was 13 b.p.m. This was lower than resting rates obtained on deck for most periods but was very similar to those of one 1%min period (?c = 14.3 b.p.m.: Table I). A similariy low heart rate was later obtained for long periods from a submerged inactive snake. presumed to be on the bottom, but not directly observed there. In the present study. breathing values obtained on deck were somewhat higher than the breathing heart rates previously reported for this species in the laboratory although the ranges considerably overlapped (20-32, R = 29.0 in the present study; 20-24. S = 21.2; Heatwole, 1977). DISCUSSION
BR!&4IHING Deck
29.0
20-32
25
sea
33.8
34-36
5
N refers to numbers of minutes of readable recording.
The present study shows that stress and activity are the main factors affecting the heart rate of both apneic and breathing sea snakes, The bradycardia typically shown by endothermic divers despite high levels of activity does not occur in sea snakes. This view is supported by the findings of Seymour & Webster (1975), Heatwole & Seymour (1976) Baldwin & Seymour (1977) and Heatwole (1977) which indicate that significant levels of anaerobic metabolism leading to the build-up of lactate does not normally take place, nor does depletion of oxygen reserves occur. Ten species of terrestrial and aquatic snakes, including four sea snakes, showed no correlation between diving behavior and levels of glycolytic enzymes (lactate dehydrogenase, phosphofructokinase, phosphorylase and hexokinase) (Baldwin & Seymour, 1977); furthermore, lactic acid concentration was generally quite low in the blood of three
Heart
rates of diving
species of sea snake captured immediately following voluntary dives at sea (Seymour, unpublished data). During most dives, these snakes apparently remain aerobic. Indeed, in view of the marked ability of sea snakes to exchange respiratory gases cutaneously (Graham, 1974; Heatwole & Seymour, 1975~. h, in press) the “diving response” syndrome would be disadvantageous as it would reduce the effectiveness of cutaneous perfusion (Heatwole, 1978). Heatwole (1977, 1978) has suggested that observed heart rate changes in sea snakes represent breathing tachycardia which promotes lung perfusion and oxygen uptake when ventilation occurs. The heart rates obtained from animals in the sea were similar to those obtained under laboratory conditions for animals of comparable activity. The heart rate of the snake on the bottom (13 b.p.m.) was identical to the mean resting apneic heart rate of four individuals (71 min total) of this species reported by Heatwole (1977) and similar to the lower values of the snake of the present study when apneic and inactive on deck (Table 1). Although during apnea, heart rates were slightly lower at sea than on deck, the heart rates of the snakes when breathing were higher at sea. The snake on deck had a mean breathing heart rate of 29 b.p.m. whereas when in the sea it was about 34 b.p.m. This difference is probably attributable to an effect of activity superimposed upon breathing tachycardia; on deck the snake had only to raise its head to the surface to breathe whereas in the sea it had to swim up from the bottom, and therefore undergo greater activity, to do so. It appears overall that heart rates of sea snakes obtained under laboratory conditions are similar to
455
snakes
those experienced by the animals in nature as long as allowances are made for differences in activity level. Acknowlcdgernents~This work was supported by the Nat&al Science Foundation (U.S.A.) under grants GA-35835, GA-34948 and CD-34462 to the Scripps Institution for the Alpha Helix Research Program. We are grateful to W. A. Dunson for aid and encouragement, to Waiter Schneider for technical assistance and to Viola Watt and Neva Walden for help in preparation of the manuscript. REFERENCES BALDWIN J. & SEYMOURR. S. (1977) Adaptation to anoxia in snakes: levels of glycolytic enzymes in skeletal muscle. Aust. J. Zoo/. 25. 9-13. GRAHAM J. B. (1974) Aquatic respiration in the sea snake Pelamis platurus. Respir. Physiol. 21, l-7. HEATWOLE H. (1977) Heart rate during breathing and apnea in marine snakes (Reptilia, Serpentes). J. Herp. II, 67-76. HEATWOLE H. (1978) Adaptation of marine snakes. Am. Sci., In press. HEATWOLE H. & SEYMOUR R. (1975~) Pulmonary and cutaneous oxygen uptake in sea snakes and a file snake. Comp. Biochem. Physiol. 51A, 399-405. HEATWOLE H. & SEYMOUR R. (1975h) Diving physiology. In The Biology of Sea Snukes (Edited by DUNSON W. A.), pp. 289-327. University Park Press, Baltimore. HEATWOLE H. & SEYMOUR R. (1976) Respiration of marine snakes. In Respiration of Amphibious Vertebrates (Edited by HUGHES G. M.), pp. 375-389 Academic Press, New York. HEATWOLEH. & SEYMOURR. (in press) Cutaneous oxygen uptake in three groups of aquatic snakes. Aust. J. Zool. SEYMOURR. S. & WEBSTERM. E. D. (1975) Gas transport and blood acid-base balance in diving sea snakes. J. exp. Zoo\. 191, 169-181.