Ventilation and gas exchange in unrestrained harp seals (Phoca groenlandica)

0300-9629/81/080809-05SO2.WO Copyright 0 1981 Pergamon Press Ltd

Cmp Bwrhrm Phmiol. Vol. 69A. pp. 809 lo 813. 1981 Prmted m Great Britain. All rights reserved

VENTILATION AND GAS EXCHANGE IN UNRESTRAINED HARP SEALS (PHOCA GROENLANDICA) G. J. GALLIVAN* Department of Zoology, College of Biological Science, University of Guelph, Guelph, Ontario, Canada (Received 29 December

1980)

Abstract-l. Unrestrained adult harp seals (Phoca groenlandica) spent 87.7 + 2.2% (X f SD) of the time diving and the mean dive time was 278.0 k 35.3 SD. 2. The mean metabolic rate was 3.24 k 0.69 ml O,.kg-‘.min-‘. 3. The minute ventilation during the surface periods was 62.45 k 7.32 I.min-’ and the oxygen extraction was 7.34 * 0.40%. 4. There was a strong negative correlation between metabolic rate and the percentage of time spent diving, and between metabolic rate and mean dive time. There was no correlation between metabolic rate and minute ventilation, or between metabolic rate and oxygen extraction. 5. These results indicate that the ventilatory response of diving seals to an increase in the metabolic O2 requirements is due to a change in dive pattern rather than an increase in ventilation or gas exchange.

INTRODUCTION Marine mammals have several adaptations to facilitate respiratory exchange during brief surface periods. Among these are an increased tidal volume (Vr) and O2 extraction (F,_EOZ) (Scholander, 1940; Scholander & Irving, 1941), and structural support of the small airways to improve air flow (Denison et al., 1971). As Vr is relatively large, Scholander & Irving (1941) suggested that the inspiratory reserve volume of marine mammals is limited and that increases in the O2 requirements must be met by an increase in breathing frequency us) which will shorten the dive time. In dolphins and manatees, which breath once each time they surface, there is a strong correlation between metabolic rate (MR) and fs (Hampton et al., 1971; Gallivan & Best, unpublished observations) and dive time decreases as MR increases. In contrast to dolphins and manatees, the phocid seals breathe several times after a dive and have a relatively large inspiratory reserve volume (Scholander & Irving, 1941). Kooyman et al. (1971) found that the minute ventilation (V,) after diving increased as a function of dive time, and the increases in I’s were due to increases in both VT and fR. However, Pasche (1976a, 1976b) showed that the ventilatory response to hypoxia and hypercapnia was due to an increase in the surface time relative to the dive time, and that V’ did not change significantly. Despite the numerous studies of the respiratory physiology of phocid seals, there is little information on the ventilation and gas exchange of unrestained seals. Kooyman et al. (1971, 1973) examined the relationship between dive time and ventilation and gas exchange, and Pasche (1976a,b) studied the ventilatory control. The present work is part of a study of ventilation and gas exchange in unrestrained harp * Present address: Department of Anaesthesia, McMaster University, Hamilton, Ontario, Canada.

seals (Phoca groenlandica). It reports the observations of metabolic rate, ventilation, gas exchange and diving pattern, and examines the relationships between these variables. MATERIALS AND

METHODS

Three adult harp seals whose physical characteristics are given in Table 1 were used in this study. For the data collection the seals were confined to a 1.8 x 0.8 x 1.1 m cage submerged in a 3.6 x 3.0 x 1.2m tank. The only access to air was a mask which covered a hole in the top of the cage. The mask was fitted with one-way valves (Institute of Zoophysiology, University of Oslo, Oslo, Norway) and when the seal was breathing, the dead space of the mask and valves was approx 1OOml. The expired air flow was monitored with an anemometer (Oxygen Consumption Computer, OCC 1000, Technology Incorporated, Dayton, Ohio) which was connected to a chart recorder (Brush 260, Gould Instruments, Cleveland, Ohio). A Douglas bag (Warren E. Collins, Inc., Braintree, Massachusetts) was connected to the outflow of the anemometer for the collection of expired air. The volume of the collected samples was determined by evacuating the Douglas bag through a Kofranyi-Michaelis gasmeter (Max Planck Institute, Gottingen, FRG) and the O2 and COz concentration of the samples was measured with a 0.5 cc analyzer (Scholander, 1947). Experimental protocol

Data was collected on 9 days with C9 and 22 days each with D3 and DS. The seals were confined to the cage at Table 1. Physical characteristics of the three harp seals (Phoca groenlandica) used in this study Animal

c9

D3

D5

Sex Age (yr) Weight (kg) Standard length (cm)

F 6 154 170

M 6 108 155

F 6 160 175

809

G. J. GALLIVAN

810 Table 2. Mean values for ventilation

Animal

N

c9

54

D3

130

D5

128

Total

3

MR* (I.min-‘)

tiozt (I,min-r)

0.59 (0.09) 0.37 (0.07) 0.40 (0.06) 0.45 (0.12)

4.06 (0.41) 3.53 (0.39) 3.51 (0.50) 3.70 (0.31)

and gas exchange

1/co,t (Fmin~‘)

R

3.01 (0.31) 2.65 (0.38) 2.61 (0.28) 2.76 (0.22)

0.74 (0.01) 0.74 (0.02) 0.75 (0.02) 0.74 (0.01)

based on the 0.5 hr sampling

ri,t (I.min-‘) 70.06 (8.96) 61.83 (6.84) 55.46 (7.63) 62.45 (7.32)

/,t (bpm)

VI (1)

26.4 (1.6) 27.8 (1.7) 28.9 (2.X) 27.7 (1.3)

2.65 (0.20) 2.22 (0.18) 1.92 (0.21) 2.26 (0.37)

periods F,-EO, (“,,) 7.18 (0.37) 7.05 (0.45) 7.x0 (0.34) 7.34 (0.40)

F,

,coz (“,,)

5.51 (0.28) 5.42 (0.35) 6.10 (0.28) 5.68 (0.37)

The values in brackets are the SD. * Calculated for the whole collection period (surface time + dive time) t Calculated for the breathing periods (surface time only).

07:30 each day and all of the data was collected between 09:30 and 17:OO hr. Prior to this study all of the seals had been introduced to the cage system on at least two previous occasions, and before any data was collected in this study a further 4 to 10 days were allowed for acclimation. There were 6 data collection periods per day. Each collection period was approximately 0.5 hr in duration, and began and ended when the seal submerged after breathing. The dive times (t,,), surface times (t,) and the percentage of time spend diving (PCTD),was calculated from the chart records. The 0, uptake (1/02), 0, extraction (F,_E02), CO, output (FCOZ), CO, exchange (F,_,C02). respiratory exchange ratio (R), minute ventilation (Fe), breathing frequency (1s) and tidal volume (Vr) were calculated for the surface periods as ventilatory exchange occurs only when the seal is at the surface. Calculations based on the total time would have obscured the difference between a change in ventilatory exchange per se, and a change in dive patterns. The metabolic rate (MR) was calculated by dividing F02 by the total time (rd + t,) as metabolism does not cease during a dive, even though ventilation does. The level of significance for all statistical testing was 957,, and all values are presented as mean + standard deviation X + SD) unless otherwise indicated. Relationships between variables were plotted and correlation coefficients were calculated. A relationship was only considered to be signiticant if there was a significant correlation for all three animals.

Table 3. Diving Variable

c9 N

Dive time (set)

&I Range N

Surface (set)

time

Percentage of time spent dtving

parameters

SG Range N S”D Range

524 302.8 144.0 6.7-676.3

RESULTS

The mean values for ventilation and gas exchange are presented in Table 2., and the diving parameters are presented in Table 3. There was a correlation (f = 0.66 + 0.19) between t, and t,, and an even stronger correlation (? = 0.85 + 0.06) between the mean dive time (t&)and mean surface time (t:) for the 0.5 hr collection periods. Mean surface time did not increase in direct proportion to mean dive time and the slope of the relationship was 0.09 _+ 0.03, whereas the slope for unity was 0.13 + 0.03.. Thus, there was a positive correlation (U = 0.67 + 0.25) between PCTD and 1;. The distribution of td is presented in Fig. 1. Dive time appeared to be sequentially random within the collection periods. All of the animals had a strong negative correlation between MR and PCTD (Fig. 2B) and between MR and t&(Fig. 2A), whereas MR was not correlated with either V, (? = -0.18 + 0.19) or FIYE02 (1. = 0.20 k 0.35). For the breathing periods, V02 was more highly correlated with I” (? = 0.89 k 0.07) than with F,_,Oz (? = 0.59 + 0.28). Minute ventilation was more highly correlated with Vr (? = 0.82 + 0.08) than with fk (). = 0.69 rfr 0.14). Minute ventilation was cor-

of the animals D3 946 237.8 145.3 3. I-596.

in this study D5

I

Total

730 293.8 192.3 6.8-950.0

3 278.0 35.3 3. I- 950.0

524 53.5 23.1 1.2. 115.2

946 28.4 12.0 1352.6

730 37.9 20.0 1.2. 124.8

3 39.9 12.7 1.2-124.8

54 85.20 2.90 76.5 90.1

130 89.32 2.45 82.5-92.6

128 88.46 2.58 79.3393.3

3 87.66 2.17 76.5-93.3

For dive time and surface time N refers to the total number of dives observed, and for percentage of time spent diving N refers to the number of 0.5 hr collection periods. Total is the mean for the three animals.

Respiration

c9

1

n=524

20 -

0

4

8

12

4

16 D3

20

n=946

0 0

4

8

12

16 D5

n=730

20

0

4

a

12

811

in seals

made at the expense of the other. Thus the only mechanism by which a seal can meet an increase in the metabolic O2 requirements is to change its diving patterns, by a decrease in dive duration and/or the percentage of time spent diving. The correlation between MR and ti and PCTD shows that both changes occur simultaneously. The large differences between the inspired and expired O2 and CO2 concentrations have been reported by previous authors (Scholander, 1940; Scholander & Irving, 1941). These large differences are a result of the low O2 and high CO2 tensions in the venous return following a dive. The low O2 and high COZ tensions increase the alveolar-capillary pressure gradient which increases the rate of gas transfer. In other mammals low venous O2 tensions are considered to cause inefficient gas exchange as they result in a low arterial O2 pressure (West, 1977). In unrestrained seals the alveolar O2 pressure is 71 mm Hg (Gallivan & Ronald, 1979) and the arterial pressure will be even lower. But, this does not necessarily indicate inefficient gas exchange as the maintenance of arterial O2 pressure is secondary to the movement of 0, to the O2 depleted tissues of the body. The cardiac output of resting seals is approximately 2.5 times that predicted on the basis of weight and increases by 60$/i after diving (Murdaugh pt al., 1966). To increase the arterial O2 pressure there must be a drop in cardiac

16

151

A

DIVE TIME (min) I. Histograms

of the frequencies

of

dive times.

c:

.E

s

lo-

0

c9

q

D3 Y.32.1e-5.32

v es

Y.12.99.12.09

V-75.2e-5

MR: r.51;

“44

~5

r-.t9-

wl30

?

~94;

~129

Y

related with PCTD (?= 0.63+ O.ll), but not with t& (f = 0.17_+0.46) or with t: (f = -0.161 0.51).

F

DISCUSSION

The dive times observed in this study were within the range of dive times reported for both wild and captive harps seals (Davydov & Skliarchik, 1965; Britsland & Ronald, 1975; Pasche, 1976a; R. Stewart, B personal communication). The mean dive times and oC9 V-101.39-27.24 MR; ~~96; n.54 the distributions in Fig. 1 show that the seals tended q D3 v-100.24-29.33 MR; r-*7; n.130 to make short dives. This is possibly a consequence of VDS V.100.94.31.43 MR; r-79; n-129 the testing situation where depth was limited to 1.0 m. However, similar dive times and surface times have been reported for wild harbour seals (P. uitulina) (Fancher, 1977) and Kooyman et al. (1980) have also reported that Weddell seals (Leptonychotes we&elk) tend to make short dives. f The results of this study show that the response of diving seals to an increase in the metabolic O2 rea. .I5 .35 .55 .75 quirements is primarily due to an alteration in the diving pattern. V” and F,_B02 are high compared to METABOLIC RATE (I 09.min.-‘) the values predicted for ‘animals of equivalent size Fig. 2. The relationships between metabolic rate and mean (Stahl, 1967). All of the seals had a.negative corredive time (A) and between metabolic rate and the percentlation (i’ = -0.32 + 0.21) between V, and F,-s02, age of time spent diving (B). The lines represent the and this was significant for two of the animals. This regression equations giving the best fit. The end points would suggest that these variables are at their maxirepresent the range of metabolic rates for which the regresmal limits, and further increases in one can only be sion was derived. TBP 694n \

1:: \\

G. J. GALLIVAN

812

output, which will increase the capillary transit time, and/or an increase in V,, which will increase the work of breathing. However, the most efficient O2 exchange is across the middle range of the exyhemoglobin dissociation curve where the change in saturation per unit pressure is the greatest. To achieve a high arterial O2 pressure will require a disproportionate increase in transit time as the change in saturation per unit pressure decreases at the upper end of the curve. As the tissue O2 tensions are low following a dive, most of the O2 will be extracted regardless of the saturation. The more rapid loading across the middle range of the oxyhemoglobin dissociation curve means that it is more efficient and tissue oxygenation is achieved more rapidly if the tissues are perfused with a large volume of partly saturated blood than if they are perfused wi!h a much smaller volume of saturated blood. The V, in the present study is similar to that previously reported for unrestrained seals (Kooyman et al., 1971; Pgsche, 1976a.b). Tidal volume and breathing frequency were similar to the values reported by P%sche (1976a.b), but VT was less and ,fRwas greater than the values reported by Kooyman et al. (1971). The difference is probably due to the decrease in VT and increase infR during the breathing period (Gallivan, 1977). In the present study and those of Phche all of the breaths were recorded, whereas Kooyman et al. recorded only the first part 01 the breathing period. The values reported for the V’ of unrestrained diving seals (Kooyman et al.. 1971: P%sche, 1976a.b, this study) are approximately 4 times* those reported for seals restrained out of water (Scholander, 1940; Robin et al., 1963). The mean alveolar O2 and CO1 pressures of seals out of water are 88 and 50mm Hg respectively (Robin et al.. 1963), but in unrestrained seals the alveolar O2 and CO1 pressures are 7 1 and 56 mm Hg (Gallivan & Ronald, 1979). In non-diving seals both hypoxia and hypercapnia are ventilatory stimulants (Bainton et al.. 1973) and the hypoxic and hypercapnic drives are interactive (Cunningham, !974). As diving seals are hypoxic and hypercapanic, V, will be maximally stimulated following a dive. This will limit the potential for further increase in V, in response to increased metabolic demands. In seals ventilatory drive must be the ultimate factor controlling dive duration. P%sche (1976a.b) has demonstrated that both hypoxia and hypercapnia cause a decrease in dive time and the percentage of time spent diving. An increase in MR. by increasing the O2 consumption and CO2 production, will accentuate the development of hypercapnic hypoxia. The respiratory threshold will be reached sooner and the seal will make a shorter dive. However, approximately the same volume of 0, and CO, must be exchanged, and as riE and gas exchange are already maximized by the hypercapnic hypoxia, there is no change in surface time. Thus, an increase in MR is met by a decrease in both dive time and the percentage of time spent diving. The relative decrease in tb was greater than the increase in MR, that is, if MR doubled, t& decreased to less than one-half of the initial value (Fig. 2A). This

disproportionate decrease in t& possibly results from the circulatory changes during diving and their subsequent effects on the metabolic processes. Kooyman & Campbell (1972) have shown that the degree of bradycardia during a dive is a function of dive duration. This suggests that there is less peripheral vasoconstruction during a short dive, thus the lung and blood gas stores would be available to most of the body and the seal would develop hypercapnic hypoxia more rapidly. During longer lives there would be a more intense vasoconstriction and the distribution of the lung and blood gas stores would be limited thereby delaying the development of hypercapnic hypoxia in the blood perfusing the chemoreceptors. Different distributions of blood flow during diving may also,be the cause of the observed correlation between V, and PCTD. If the lung and blood gas stores are available to most of the body throughout the dive, the ventilatory drive will be determined the blood O2 and CO* pressures at the end of the dive. If, however, the distribution of blood flow is restricted, there will be a washout of O2 poor and CO, rich blood from the unperfused tissues after the surfaces. This will add to the ventilatory drive already present at the end of the dive. The mechanism responsible for the variation in the degree of vasoconstriction is probably tissue autoregulation of blood flow, where an increase in tissue MR causes an increase in the local blood flow. An example of this can be found in the decrease in dive time observed during the post-prandial increase in MR (Gallivan. unpublished). The processes of digestion increase the MR of the abdominal organs and this requires an increase in local blood flow to supply O2 and to transfer nutrients from the intestine to the liver or other organs. The increased abdominal blood flow will accentuate the development of hypercapnic hypoxia in the blood perfusing the chemoreceptors and the dive time is decreased. The final part of this discussion is ati examination of the relationship between t: and tl. Although t: is correlated with t&. the relative increase in t: is less than the increase in t&.This relationship is due to the balance between the O2 debt which is accumulated during a dive and MR. The magnitude of the O2 debt is dependent upon the dive duration and MR during diving, while its’ payment depends on the respiratory exchange and the aerobic MR. If the aerobic MR is high then a smaller proportion of the respiratory exchange will be available to repay the debt, and more time must be spent at the surface. Thus, short dives which are associated with high metabolic rates have a relatively longer surface time than long dives which are associated with lower metabolic rates. A~kno~ledgemenrs-This research was conducted with the financial and logistical support of Professor K. Ronald and was made possible by grants from the National Research Council of Canada. Donner (Canadian) Foundation and Canadian National Sportsmen Show. REFERENCES

C. R.. ELSNER R. & MATTHEWS R. C. (1973) Inhaled CO1 and progressive hypoxia: ventilatory response in a yearling and a newborn harbor seal. Life Sci. 12. 527-533.

BAINTON

* GEwas normalized to a function of the value predicted on the basis of weight using the equation (Stahl,

1967).

1’, = 0.379 w“.*

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KOOYMANG. L. & CAMPBELLW. B. (1972) Heart rates in freely diving Weddell seals, Leptonychotes weddelli. Camp. Biochem. Phrsiol. 43A, 31-36. K~~YMANG. L., WAHRENBR~CK E. A., CASTELLINIM. A., DAVISR. W. & SINNETTE. E. (1980) Aerobic and anaerobic metabolism during voluntary diving in Weddell

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