RespirationPhysioIogy(1976) 26, 183-194; North-HollandPublishingCompany, Amsterabm

THE EFFECT OF HYPERCAPNIA ON RESPIRATORY CHARACI’ERISTICS AND DIVING BEHAVIOUR OF J!REELY DIVING SEALS

ARVID PASCHE Instituteof Zoophysiology, Universityof Oslo, Box 1051, Blimiem, Oslo 3, Norway

A&n&. I%rce trained young seals, one harp seal, Pagophihtsgroe&ndicus, and two hooded seals, Cystophoracristata, have been used to study the effect of bypercapnia on respiratory cbara&&ics and diving behaviour. The seals were allowed free movements within a circular pool, while diving and respiratory behaviour wfze recorded. During the experiments the alveolar Co, tension was cont.im~&y recorded. There was a significant decrease in duration of dives with increasing PA, for all animals. ‘sr~ increased sigQi&xultly with increasing PA,. This increase was caused by more fqucnt surfacing rat& than by a higber rqiratory frequency during tbe breathing periods. Tidal volume increased from 3 to 43% when inspind CQ was increased from 0.03 to 9 ~01%.The seals were all found to be less sensitive to CO2 than man. A decreased sensitivity to CO, with age is suggested from the results. AlvcoIar gas Control of breathing Harp seal

Hooded seal Hypm‘apnia Ventilatory effects of CO,

A number of investigations on the respiratory effect of CO2 in diving animals have been reported in the literature (Orr and Watson, 1913; Hiestand and Randall, 1941; Irving et al., 1935; Irving, 1938; Salt and Zeuthen, 1960). It has been suggested that the ventilator-y parameters are relatively insensitive to CO& diving animals. Recent studies, however, indicate that seals (Robin et al., 1963; Bainton et al., 1973) and ducks (Andersen and L&i& 1964) are not insensitive to Cot, but rather that they show a lower sensitivity than man. Bentley ef al. (1967),with reference to Robin et al. (1963), examined the effects of CO2 breathing on ventilation in echidna, They compared an increase in alveolar CO2 to the increase in ventilation and found that seals were only slightly less sensitive than man.

Acceptedfor publication20 November 1975. ’ This study was supported by grants from the Norwegian %&kg Council. 183

184

A. P&HE

All previous studies of the respiratory response to CO2 breathing in diving animals have been done on restrained animals which may have affected the results. Moreover, information concerning the effect of CO2 breathing on the diving behaviour has not earlier been reported even from studies on restrained animals. In the present study the effect of different inspired CO1 concentrations on the ventilatory parameters and diving behaviour of freely diving seals have been recorded. Three trained animals were used, one harp seal (Pagophilus groenlandicus) and two hooded seals (Cystophora cristata).

Materials and methods One female harp seal (Pagophilus groenlandicus) and two hooded seals (Cystophora cristata), one of either sex, were captured as pups close to Jan Mayen and transported on board a sealing vessel to Norway. The animals were kept in captivity at the Institute of Zoophysiology, University of Oslo, where they lived in a circular freshwater pool large enough to allow relatively unrestricted movements. During captivity the seals were fed a diet of herring, added sea salt, minerals and vitamins, and they seemed to be in excellent condition during the experiments. Records of weight and age during the experimental period of all animals are presented in table 1. TABLE 1 Records of weight and age of the three seals during the experimental period Sex ? Hooded seal Hooded seal Hooded seal Harp seal

Age

Weight

(mth)

(kg)

6-11 9-11 18-21 9-11

44.C 63.0 57.0- 61.3 90.6-102.5 42.7- 46.2

d

x X X X

Diving behaviour and ventilatory parameters were studied during periods lasting 3 months. The male hooded seal was used in two such periods. The first period took place when the seal was at the age of 9-l 1 months, the next period at the age of 18-21 months. During the experiments the other animals were removed from the circular test pool and the surface of the pool was covered by a net which prevented the experimental animal from breathing except at a plastic dome, the ‘blowhole’ (fig. 1). This plastic dome thus came to function as a face mask during breathing. Valves attached to the dome gave undirectional inspiratory and expiratory flows. The animal was allowed free movement within the pool. A sensitive copper+zonstantan thermocouple connected to a Beckman RS dynograph was placed just behind the membrane of

185

CONTROL OF BREATHING IN SEALS

3 Fig. 1. Experimental set-up for measuring the ventilation and diving behaviour of freely diving seals. See text for detailed description.

the expiration valve. Duration of dives, and breathing periods as well as respiratory frequency were estimated from the temperature recordings. The desired inspiratory gas composition was mixed by means of an AGA gasmixer and stored in 5004iter PVC bags. The gas mixtures used are listed in table 2. During an experiment the bag with the gas mixture was connected to the inspiration valve with a flexible rubber hose. All expired gas was collected in a Douglas bag and then expelled through a dry gas meter type D 10/U 24. Continuous monitoring of CO2 TABLE 2 Composition of the inspiratory gases used Gas No.

COz content (vol%)

1 2 3 4 5

0.03 3.0 ca. 6.0 cu. 9.0 ca. 12.0

cu.

O2 content (vol%) 20.93 20.9 ca. 20.9 co. 20.9 ca. 20.9

cu.

N, content @ol%) cu.

18.0

ea. 76.0 cu. 73.0 cu. 70.0 cu. 67.0

186

A, PKSCHE

tensions in expired air was performed by means of an infrared CO, analyzer connected with a rubber hose to the expiratory valve (fig. 1). End-tidal CO2 tensions were considered equivalent to mean alveolar CO2 tensions. Average tidal volume was determined by connecting a Wright gas meter to the expiratory valve. Tidal volumes as well as total expired volumes were corrected for the vohunes diverted to the CO2 analyzer, Concentrations of CO2 and O2 in the inspired gas mixture and in the expired air were determined in duplicate with a ‘Scholander 0.5 cc gas analyzer’ (Scholander, 1947). Exposure to each gas mixture was sustained until the alveolar CO2 tensions had s~b~~~ at a certain level before co&&ion of gas started. When the gas mixtures were given step by step, with an increase in CO2 content of only 3 ~01%in each step, this exposure time generally was about i0 min total lapsed time.

0

..”

187

CONTROL OF BREATHING IN SEALS

During the experiments the animals were usually swimming continuously at moderate speed. The female hooded seal, however, showed a different behaviour; she rested at the bottom of the pool for a 30-min period three times during the experiments. During this period her only activity was to enter the‘blowhole’to breathe. After finishing the breathing she sank to the bottom again. The results from these 30-min periods are marked with a circle. The results are given as mean values based on data obtained from a total of 103 experiments. The mean number of dives in each experiment was 44. The results were treated statistically using Student’s r-test, and 5% was used as the accepted limit of significance (Sverdrup, 1964).

Figure 2 expresses duration of dives against alveolar CO2 tensions (PACT). All seals tested show a significant decrease in dive duration with an increase in alveolar CO2 tension (P < 0.005). The diagram from the harp seal has a breaking point at PAW2 = 63 mm Hg. It is reasonable to assume that this breaking point was caused by gas mixtures with a COz content too high for the seal. The harp seal presented clear evidence of anxiety when the CO2 content of the inspiratory air exceeded 6 ~01%.

J+

sb

:b

$0

;b

sb

io

I

100

1

110

PA CO2 (mmHg) Fig. 3. Duration of the breathing period shown as a function of alveolar CO1 tension. The results are given as means *SE. A harp seal, 0 female hooded seal, m male hooded seal (9-11 mth), 0 male hooded seal (18-21 mth).

138

A. PkHE

Gas mixtures with COz content as high as 12 ~01%was consequently not used in the experiments with this animal. The male hooded seal generally made shorter dives at the age of 1EL21months than at the age of 9-l 1 months. This difference might be due to the fact that at the age of 13-21 months the seal was rather big for the pool and was restrained in its movements. Mean dive duration of the female hooded seal during the resting period at the bottom of the pool was 235 sec. Compared with the mean diving length during activity the mean duration of the dives during rest was more than doubled. There was not a clear tendency towards a change in the length of each breathing period with increasing alveolar COz tension (fig. 3). However, the decrease in duration of the breathing period of the harp seal are significant (P < 0.05) while the male

100

50

PA co2

(mm tig)

Fig. 4. Relationship of respiratory minute volumt to a&e&r CO, tension (mean values f SE). A harp seal, 0 fernale hooded seal, a male hooded seaI (9-11 mth), c) male hooded seal (IS-21 mth).

189

CONTROL OF BREATHING IN SEALS 3

2 r J 1=

/.7+

------a___ -

>'

~

1

,

_ 0 . ~~~:.+_._._._._.-.-.-~~ _- - p -+L

(

4



I

L

I

1

I

I

1

40

50

60

70

60

90

100

110

PA CO,

(mm Hg)

Fig. 5. Relationship of respiratory tidal volume to alveolar COz tension (mean values *SE). A harp seal, 0 female hooded seal, n male hooded seal (9-l 1 mth), 0 male hooded seal (H-21 mth). 50

-~2+%+______ !



1

_.___.--=;-

40

___._.--. +

_.-.

.E

--iL-‘---‘-’

-WC’-’

E 3 L 5 30

0’

0 Lc

........

,~~_..........________~ ...+a -. .....q+E.:.Y.:::. .......... 4_

c-

4”‘”

_

,,.,,

......................

*

20

0

f/

’ 40

I

50

I

60

70

PA CO2

80

I

I

1

90

100

110

(mmHg)

Fig. 6. Respiratory frequency calculated from the breathing periods as a function of alveolar CO1 tension (mean values f SE). A harp seal, 0 female hooded seal, n male hooded seal (9-l 1 mth), 0 male hooded seal (H-21 mth).

190

A.,PJ&CTHE

hooded seal showed a si~~~nt increase in duration of the breathing period both at the age of 9-l 1 months and 18-21 months (P < 0.005). The results from all the tested seals show a considerable increase in PE with increasing alveolar CO2 tension (fig. 4). The harp seal showed the most marked increase in ?E with increasing inspired CO2 content. An increase in PA,, from 48 to 63 mm Hg was associated with an increase in 9~ of 160%. The values for the female hooded seal during rest show that VE was only 60% of the value found in the active animal at the same PAN*,. In fig. 5 tidal vohnne (VT) is plotted against alveolar CO, tension. There is a significant increase in tidal volume with increasing PA,, for all the seals (P < 0.025). An increase in PA,, from 48 mm Hg when breathing air to a PA,, of 63 mm Hg (Frco, = 6 ~01%) resulted in an increase in tidal volume of 65% for the harp seal. Furthermore, an increase in PA,, in the female hooded seal from 41 mm Hg when breathing air to 61 mm Hg when breathing 6 ~01% CO2 brought an increase in tidal volume of only 3%. With an increase in PAN, from 50 mm Hg (FI,, = 0.03 ~01%) to 67 mm Hg (FI,,, = 6 ~01%) the increase was 7% for the male hooded seal. The tidal volume for the resting female hooded seal is 12% larger than the tidal volume during swimming activity at the same PA,,. Respiratory frequency, measured in the breathing period (f) and calculated for 25 -

20 -

"; '5 15 . r" 5 L f! 10 t

5-

OY/

’ 40

I

50

60

90

I

I

100

110

Fig. 7. Respiratory fiuquency calculated for the total experimental period as a function of alveolar COz tension (mean values + SE). A harp seal, 0 female hooded seal, m male hooded seal (%l 1mth}, Cj male hooded seal (W-21 mth). 8

the total experimental period (fr) were also tested. The values for the female hooded seal showed a significant increase in frequency (f) with increasing PACT (P < 0.005) (fig. 6). The male hooded seal also showed a significant increase in respiratory frequency with increasing PA,, when the age was 9-l 1 months (P < 0.01). At the age of 18-21 months the corresponding values tended to show a decrease. However, this decrease was not found to be significant (P > 0.05). The respiratory frequency of the harp seal was practically constant when the animal inspired the different gas mixtures, with the exception of experiments with gas mixture of 3 ~01%C&. Ail animah showed a signifkant increase in respiratory frequencies cakulated for the total length of the experimental period (fT) with increasing alveolar CC2 tension {P < 0.005) (fig. 7). This is due to the fact that the seals enter the dome to breathe more frequently rather than from a higher respiratory frequency during the breathing period. 600 -

5OO-

14 8

400

;;; k s

300-

>” 200-

iO0

n

L

r

I

100 PA CO,

( mm Hgl

Fig. 8. A ~nl@son of changes in respiratory minute volume (as pc’ cent increase of normal minute volume) ofmanand the tested seals with inw&g alveolar CO1 tension. 4 man, A harp seal, 0 female hoc&d seal, H male hooded seal (9-1X mth), 0 male hooded seal (M-21 mth).

Figure 8 expresses the effects of variable inspired CO, against the per cent increase in &. The results of ventilatory increase with increasing PA- for man have been eakulated by Lambertsen (l%O, 1961).The Qure shows that ventilation in the harp seal is approximately as sensitive as that for man to CO*, but the seal has a higher

192

A.

P&CHE

alveolar CC& tension. The female hooded seal is more sensitive than the male hooded seal, but is not as sensitive as the harp seal. The male hooded seal appears to develop a decreased sensitivity to CO2 with age.

Discussion The responsiveness of seals to hypercapnia appears to be less than that of man. The alveolar P, when breathing air is found to be 41 mm Hg (female hooded seal), 48 mm Hg (harp seal), 63 mm Hg (male hooded seal, 9-l 1 months), and 50 mm Hg (male hooded sea& 18-21 months), respectively. These alveoiar CO, tensions are somewhat higher than the corresponding values for man (Comroe, 1972). An elevated alveolar CO2 tension in seals has also been demonstrated by Robin et al. (1963) and Bainton et al. (1973). However, the reason for this elevated tension is not clear. The present study shows that despite the low responsiveness to high arterial PcoI, hypercapnia does affect the ventilation of the freely diving seals. An increase in the COz content in the inspiratory air from 0.03 to 6 ~01% resulted in a doubling of ventilation &‘E). The results are in agreement with the results reported by Bainton et al. (1973) from their study on harbour seals. 6 ~01% CO2 is somewhat higher than the 4 ~01% necessary to double the ventilation in man (Comroe, 1972). On the other hand, Andersen and L&5 (1964) had to use 7.5 ~01% CO, in the inspiratory air of ducks before ventilation was doubled. The effects of 6 ~01% CO, in the inspired air obtained in my study are very similar to those reported by Bentley et al. (1967) for echidna, a burrowing animal. They found that an increase in the CO2 content in the inspiratory air from 0.03 to 6 ~01% doubled the ventilation of the echidna. The primary effect of CO, on the ventilation of man is an increase of the tidal volume (Haldane et al., 1919). From previous studies on echidna (Bentley et al., 1967) and ducks (Andersen and Ldvd, 1964) one might conclude that also in these species the increase in ventilation during COz breathing is mainly caused by an increase of the tidal volume. This response does not seem typical of the freely diving seals used in the present study. While all seals showed a significant increase in tidal volume with increasing inspired C02, an increase in the inspired CO, content from 0.03 to 9 ~01% brought about an increase in the tidal volume of only 6% (male hooded seal, 18-21 months), 9% (female hooded seal), 36% (male hooded seal, 9-l 1 months), and 43% (harp seal), respectively. These changes are very different from the 400% increase reported in ducks (Andersen and Ldvd, 1964), the 300% increase in echidna (Bentley et al., 1967), and the 500% increase in man (Comroe, 1972) during exposure to the same gas mixture (FI,, = 9 vol%). In man, inspiration of a gas containing 9 ~01% COz would not only affect the tidal volume, but also increase the respiratory frequency by about 100%. A corresponding effect on the respiratory frequency of the duck and the echidna has not been reported. Only the female hooded seal showed a significant increase of the respiratory frequency (f) during CO2 breathing. An increase of FI coI from 0.03 to 9 ~01% resulted in an increase in respiratory frequency

CONTROL OF BREATHING IN SEALS

193

of 200/ a rather small increase compared with the corresponding value in man. The respiratory frequency during the total experimental period (fT) increased with increasing F~co, for all the tested seals. There was a clear correlation between dive duration and alveolar COz tension. Duration of the dives of all the seals decreased significantly with increasing alveolar CO2 tension. All seals tested were found to be less sensitive to COz than man. This fact is in accordance with the results of Robin et al. (1963). It is interesting to note, however, that the most CO2 sensitive of the tested seals, the harp seal, is only slightly less sensitive than man. The results from the male hooded seal may indicate a decrease in sensitivity to COz with age. Acknowledgements I wish to thank Professor John Krog for advice and encouragement during the study and for his critical review of this paper. I also wish to thank Mr. M. Bronndal for his help in keeping the animals. References Andersen, H. T. and A. LQvd (1964). The effect of COs on the respiration of avian divers (ducks). Camp. Biochem. Physiol. 12: 451456.

Bainton, C. R., R. Elmer and R. Matthews (1973). Inhaled CO2 and progressive hypoxia: Ventilatory response in a yearling and a newborn harbor seal. Life Sci. 12: 527-533. Bentley, P. J., C. F. Herreid, II and K. Schmidt-Nielsen (1967). Respiration of a monotreme, the echidna, Tachyglossus aculeatus. Am. J. Physiof. 212: 957-961. Comroe, J. (1972). Physiology of Respiration. Chicago, Ill., Year Book Medical Publishers Inc., pp. 59-69. Haldane, J. S., J. C. Meakins and J. G. Priestley (1919). The respiratory response to anoxemia. J. Physiol. (London) 52: 420432.

Hiestand, W. A. and W. C. Randall (1941). Species differentiation in the respiration of birds following carbon dioxide administration and the location of inhibitory receptors in the upper respiratory tract. J. Cell. Comp. Physiol. 17: 333-340.

Irving, L., 0. M. Solandt, D. Y. Solandt and K. C. Fisher (1935). The respiratory metabolism of the seal and its adjustment to diving. J. Cell. Comp. Physiol. 7: 137-151. Irving, L. (1938). The insensitivity of diving animals to CO,. Am. J. Physiol. 124: 729-734. Lambertsen, C. J. (1960). Carbon dioxide and respiration in acid-base homeostasis. Anesthesiol. 21: 642-651. Lambertsen,

C. J. (1961). Chemical factors in respiratory control. In: Medical Physiology, 11th ed., edited by P. Bard. St. Louis, MO., Mosby, pp. 633-655. Orr, J. B. and A. Watson (1913). Study of the respiratory mechanism in the duck. J. Physiol. (Lonaim) 46: 337-348.

Robin, E. D., H. V. Murdaugh, W. Pyron, E. Weiss and P. Soteres (1963). Adaptations to diving in the harbour seal - gas exchange and ventilatory response to CO,. Am. J. Physiol. 205: 1175-l 177. Salt, G. W. and E. Zeuthen (1960). The respiratory system. In: Biology and Comparative Physiology of Birds, edited by A. J. Marshall. New York, Academic Press, pp. 363-409. Scholander, P. F. (1947). Analyxer for accurate estimation of respiratory gases in one-half cubic centimeter samples. J. Biol. Chem. 167: 235-250. Sverdrup, E. (1964). Lov og tilfeldighet I. Oslo,Universitetsforlaget, pp. 57-61 and 196200.

The effect of hypercapnia on respiratory characteristics and diving behaviour of freely diving seals.

RespirationPhysioIogy(1976) 26, 183-194; North-HollandPublishingCompany, Amsterabm THE EFFECT OF HYPERCAPNIA ON RESPIRATORY CHARACI’ERISTICS AND DIVI...
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