Mechanical properties of the harbor porpoise lung, Phocoena phocoena

Respiration Physiology (1979) 36, 287-300 © Elsevier/North-Holland Biomedical Press

MECHANICAL PROPERTIES OF THE HARBOR PORPOISE LUNG, PHOCOENA PHOCOENA

G. L. KOOYMAN and E. E. SINNETT * Physiological Research Lahoratory, Scripps Institution of' Oceanography, University of' California, San Diego. La Jolla, CA 92093, U.S.A.

Abstract. The pressure-volume and pressure-flow characteristics of the excised lungs of 5 harbor porpoise were determined. It was found that: (I) in comparison to terrestrial mammals the lung volume relative to body weight is large, (2) the lungs are capable of emptying to < 17"1., of total lung capacity, (3) peak expiratory flowrates of 5 to 10 vital capacities (YC) . sec -I are relatively high for mammals, (4) isovolume pressure flow curves showed a clustering of flowrate plateaus from 40 to 80~/o yc. with a marked drop in the flow rate plateau at 20/0 yc. (5) the profile of flow-volume curves is unusually square shaped with flows remaining above 2 ye· sec -I at a lung volume of 20% Ye. (6) this feature is responsible for the short emptying time of <0.2 sec. It is concluded that cartilaginous airway reinforcement, which extends to the alveolar sac. is responsible for the unusual flow-volume properties. These porpoises have the capability of exchanging a large percent of their lung gas very rapidly during their brief pass through the air-water interface. Flow volume Isovolume pressure flow Pressure volume

Flow time Peak flow Phocoena phocoena

Some years ago, Scholander (1940) noted that the residual lung volume was unusually low in the grey seal, Halichoerus grypus, and in two species of whale Balaenoptera physalus and Phocoena phocoena}. He was aware also of the unusual amount and distribution of cartilage in the airways of those few species of marine mammals studied. Based on this knowledge he proposed a hypothesis for the function of reinforced airways. His premises were: (1) a rigid airway system would compress less easily than the alveoli; (2) during dives to depth the lungs would be compressed and since the alveoli were more compliant than the airways they would compress more rapidly, emptying their gas contents into the airways; (3) at depth this action Acceptedfor publication 16 December /978

*

Present address: Harvard School of Public Health. 665 Huntington Avenue. Boston. MA 02115. U.S.A. 287

288

G. L. KOOYMAN AND E. E. SINNETT

would result in collapsed alveoli and reduced gas exchange; (4) consequently, during deep dives, blood and tissue would not be exposed to high nitrogen tensions and the subsequent risk of decompression sickness as the animal returned to the surface. Recent studies of lung mechanics of the California sea lion, Zalophus californianus, (Denison, Warrel and West, 1971), and the fin and sei whales, (Balaenoptera physalis, and B. borealis) (Leith, Lowe and Gillespie, 1972), confirm that some marine mammal lungs can be emptied to very low volumes. Furthermore, in a survey of all major marine mammal taxa it was found that all have substantially reinforced airways, although there is much variation in the distribution of reinforcement (Denison and Kooyman, 1973). Seals represent one extreme, possessing a length of non-cartilaginous terminal airway, while the other extreme is represented by the small whales (porpoises and dolphins) and the sea lion. These latter two groups have airways with thick rings, plates, or spirals of cartilage which extend to the alveolar sac entrance. Denison and Kooyman were impressed that the cartilaginous support of the terminal airways of porpoises and sea lions is much stronger than is necessary to insure alveolar collapse upon compression during dives to depth. Furthermore, the airway structure of river dolphins (Inia) , which obviously do not dive deeply, is similar to that of their oceanic relatives. These facts seem to contradict the hypothesis that armored airways are an adaptation to deep diving, or at least to suggest that there are other important functions. The model of airway dynamics reviewed by Bouhuys (1974) seems pertinent. According to this model, expiratory flowrates are limited at low lung volumes by segments of peripheral airways which compress or even close during forced expirations. Flowrate is limited by this collapse, and the degree of limitation is a function of lung inflation. The purpose of this study was to determine the static and dynamic mechanical properties of the lungs of the harbor porpoise. It was our hypothesis that the overall airway armoring of these lungs might allow very high flowrates at all lung volumes and specifically that flowrates at low lung volumes might be maintained at high levels due to the extensive peripheral airway support.

Materials and methods During the summer collection of 10 harbor porpoise, Phocoena phocoena, by Canadian biologists, we were permitted to remove the lungs from the last five animals collected soon after death. The lungs were placed in cold storage for 3-19 hours before pressure-volume (PY) and pressure-flow (PF) data were collected. The total body mass of each animal was estimated from the measured body length and its known relationship to total body mass. The equation for this estimate, MB (kg) = -42.4 +0.59 ·NF (cm) for males and MB = -36.7 +0.59 ·NF for females, was based on numerous measurements of this species made by Dr. D. Gaskin (personal communication). MB is mass in kg and NF is nose to fluke length in cm. Minimum air volume (MAY), which is defined as the volume of air in the lungs at

289

PORPOISE LUNG MECHANICS

S

TWV

~:'-'~:<::'\ \'.

F4'i -9-

F3i

BV

VR

Fig, L Apparatus for the measurement of pressure-volume and pressure-flow curves, Not drawn to scale, From left to right the symbols are: F3 and F4, Fleisch pneumotachographs, sizes #3 and #4; L, lung; Pao, airway opening pressure connector; P box ' box pressure port; s, 7 I syringe; TWV, 3-way valve; T2, Validyne DP-15 high pressure transducer with interchangeable membranes; TL Validyne MP-45 low pressure transducer; FL Fleisch pneumotachograph. size # I; BV, 5-cm butterfly valve mounted in a 5-cm 10 plastic pipe; NV, needle valve; and VR, 220 liter vacuum reservoir. The box enclosing the lung was 50 cm on a side and had a removable lucite lid. Connections shown with solid lines were used to produce pressure-volume data. Stepwise changes in Pbox were made by bleeding air through NV into VR; see the text for further details on the pressure-volume procedures. To obtain pressure-flow data, F3 and/or F4 were inserted into the box ports and the connections indicated by the dotted lines (to Tl. T2, and S; FI was removed) were established. The syringe and 3-way valve were used to inflate the lung prior to opening BV and exposing the lung to the low pressure in VR. For further details on the pressure-flow procedures. see the text.

a transpulmonary pressure of zero, was obtained by weighing the lung and by determining the total lung volume of the uninflated lung measuring the saline water it displaced; a specific gravity of I g . ml- i of lung tissue was assumed. The pieces of equipment used to generate the pressure-volume (PV) and pressureflow (PF) data are shown in fig. I and are described in the legend. Essentially, PV curves were generated by placing a lung inside a rigid, fiber-glass-lined box with a lucite lid and measuring air flow at the trachea (with a pneumotachograph open to the atmosphere) while the pressure in the box surrounding the lung was made less than or greater than atmospheric. Pressure flow curves were made by converting the box to a flow plethysmograph (see fig. 1) and deflating the inflated lung with varying degrees of suction on the airway. All data on pressure, flow and volume were recorded on paper with a two-channel-chart recorder. Before the lung was attached, however, the following procedures were followed to check the calibration of the equipment. For PV curves, pressure calibrations were performed with a water manometer. Volume was measured by integrating the flow signal from the pneumotachograph which was to be in series with the trachea; the calibration was checked by passing known amounts of air through the pneumotachograph with a calibrated 7-1 syringe. For PF curves, the pressure transducer (with a stiffer diaphragm) was calibrated over the appropriate range with a mercury manometer. The flow calibration (with the box in its PF configuration (see fig, I) was checked routinely by first integrating the flow signal while delivering

290

G. L. KOOYMAN AND E. E. SINNETT

a known volume from the 7-1 syringe. Once the integrator had been calibrated, a blower controlled bya Variac was used to draw air through the box at a constant rate. The rate was adjusted until a desired volume was integrated during a period of one second, thus providing a known flow for the calibration of the flow output. The linearity of the system was checked before and after the entire study by continuously drawing air into the box through the pneumotachograph heads and then back out through a calibrated 5 cm orifice flowmeter. The system was linear to 20 I . sec -I, and a complete calibration curve was obtained for flows up to 50 I . sec -I. Following the calibration procedures, the lung was attached to an appropriate tracheal cann ula and was placed in the box as shown in fig. 1. To produce PV curves, the pressure in the box was lowered (and then raised) in a stepwise fashion (5 cm HcO/step, minimum box pressure -30 cm HP, maximum box pressure + 10 cm HP). The pressure was held at each step until a volume plateau was reached. Measurements of box pressure relative to atmospheric pressure yielded data on transpulmonary pressure. The PF curves were produced by inflating the lung to a transpulmonary pressure of 35-40 cm HP and then rapidly opening the butterfly valve separating the inflated lung from a vacuum reservoir. By changing the pressure in the vacuum reservoir, PF curves with maximal and submaximal flows were obtained. We follow the standard sign convention where pressure differences which tend to inflate the structure in question are referred to as positive while pressure differences which tend to deflate the structure are negative. Thus as box pressure was reduced during lung inflations for PV curves, the tracheal pressure became more positive with respect to box pressure as inflation proceeded. For the PF curves, tracheal pressure drops with respect to box pressures as deflation proceeds. The analog records of the PV curves of each excised lung were edited and selected curves were analyzed. The analysis consisted of taking the paired data of the curves and transferring them to computer cards. In the case of specimen # 10, the only lung for which peak flows exceeded the linear range of the plethysmograph, the flow data were tabulated by hand and corrected to true flow figures according to to the calibration curve derived for these high flows. These data were then keypunched and added to the other data. The cards were analyzed with an IBM 1800 computer programmed to collate the data in tabular form, integrate the flow signals and plot PV, flow correlated with time (FT), flow correlated to volume (FV), and isovolume pressure flow (lVPF) curves (that is, flowrates correlated to transpulmonary pressure at specific lung volumes of 80, 60, 40, and 20% of vital capacity).

Results

The general physical traits of the lungs studied are summarized in tables I and 2. The lung weights ranged from 2.2 to 4.4% of body weight. The total lung capacity

291

PORPOISE LUNG MECHANICS TABLE I Physical features of the animals studied Animal

Sex

MB (kg)

ML (kg)

6 7 8 9 10

Q

45 25 37 31 39

1.00 0.58 1.61 0.80 1.25

d d Q

d

ML/MB (%) 2.2 2.3 4.4 4.0 3.0

TLC (I)

MAV (I)

2.9 3.4 4.0 3.0

0.46 0.11 0 0.46 0.50

MB, body mass; ML. lung mass; TLC is the total lung capacity measured at +30 cm H 20 pressure; MA V, minimum air volume. Minimum air volume is that volume remaining in the lung when transpulmonary pressure is zero. Note that our animals begin with 6 to correspond with the collection numbers of the Canadian biologists.

TABLE 2 Dimensions of total lung capacity and minimum air volume relative to lung and body mass Animal

TLC(ml) ·ML(g)~1

TLC(ml) . MB(g) ~1

MAV(ml). ML(g)~1 MAV·TLC~I·IOO

7 8 9 10

5.0 2.1 5.0 2.4

0.12 0.09 0.13 0.08

0.2 0.003 0.6 0.4

4 0.1 12 17

(TLC, the lung volume at an inflation pressure of 30 cm HzO) ranged from 2 to 5 ml . g ~ 1 of lung weight and 0.08 to 0.13 ml . g ~ 1 of body weight. The minimum air volume (MAV) as determined by water displacement before the first artificial inflation ranged from close to zero to 17% of TLC. Pressure-volume curves were obtained from all five lungs. The opening pressure of first inflation was about 20 cm HzO. During successive PV curves, opening pressures were between 10 and 15 cm H 20, while at 20 cm HzO pressure the lungs had reached 50% of TLC. On the deflation limb of the PV curve it can be seen that the lungs continued to empty at -5 to -10 cm HzO pressure, the highest emptying pressures that we attempted (fig. 2). The peak flows achieved for animals 6 through 10 were: 8, 5, 9, 5 and 10, VC . sec ~ 1, respectively. VC is the vital capacity, which is that volume from maximum inspiration to maximum expiration. In Phocoena the lungs appeared to be empty at the end of the deflation, which indicated to us that VC was a larger proportion ofTLC than in human or dog lungs. The shortest time for a deflation was <0.2 sec for porpoise 10 (fig. 3) and 0.20,0.31,0.27 and 0.32 for animals 6 to 9. FV curves showed that there was a gradual decline in flow as lung volume fell from 80 to ",40% of VC, while the major drop in flow occurred between about 20% and 0% of VC (fig. 4). All of the IVPF curves became flat at endotracheal pressures

292

G. L. KOOYMAN AND E. E. SINNETT

4 Phocoeno #8

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Fig. 2. Series of pressure volume curves obtained from porpoise 8. Volume expressed in liters. and as a percent of total lung capacity (TLC).

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TIME (SECONDS)

Fig. 3. Flow curves obtained from porpoise 10 at different driving pressures. The driving pressures in descending order from the upper to lower curve were 205. 55 and 50 cm H~O. Flow expressed as liters per second (LPS). and in VC per second.

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Fig. 4. The driving pressures for the flow volume curves in descending order from the upper to lower curve were 272, 103. 66 and 84 cm H20. Driving pressures greater than 272 cm H 20 did not result in higher flowrates.

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Fig. 5. Isovolume pressure flow curves derived from a series of flow and pressure measurements of the lungs of porpoise 8. The curves are drawn by eye. Curves of the other porpoises showed even more convergence at 0.4. 0.6 and 0.8 VC . sec -I.

294

G. L. KOOYMAN AND E. E. S[NNETT

between -50 and -150 em Hp (fig. 5). For lung volumes between 60 and 80% of VC the plateaus are at about the same rate of flow. The flow at 40% of VC is slightly lower, and there is a marked reduction in peak flow at 20% of Vc. Even at this low lung volume flow rates are still 2.5 (porpoise 8) to 5.0 (porpoise 10) VC ·sec l (fig. 7).

Discussion In previous attempts to study the lung mechanics of another delphinid porpoise, (Stenella /ongirostrisj, the efforts met with failure when it proved impossible to inflate the freshly dissected lungs of these animals (R. Garvie, personal communication). Stenella have lungs which are similar to those of most other members of the family Delphinidae in having well developed serial sphincter muscles in the terminal airways. We presume that these sphincter muscles had gone into a state of contraction when the animals died in the tuna seining nets and that it was this muscular contraction which prevented the subsequent inflation of the lungs. The harbor porpoise is an exceptional delphinid in that the sphincter muscles in the lung are more poorly developed than in any other delphinid (figs. 6A,B). We reasoned that the near absence of these muscles would enable us to inflate the lungs of the harbor porpoise and to study their mechanical properties; apparently we were correct. Scaling. In the following discussion some of the observed and predicted relations between lung volume, lung mass and body mass are presented. Stahl (1967) derived the following equation to relate lung mass (ML) in g to body mass (MB) in kg: ML = 11.3 MBo99. Table 3 shows that the values we observed were two to four times the predicted values. However, Stahl's equation does not seem to hold very tightly for marine mammals. For example, ML of the sei and fin whale, which were based on estimated body weights, equaled 0.9 and 0.5% of MB, respectively (Leith, Lowe and Gillespie, 1972). These values are slightly less than the expected percent of MB as estimated by Stahl's equation. Quiring (1943) also obtained an ML to MB percentage of 0.67 for the fin whale by weighing both the lung and, in sections, the whole body of the whale. Furthermore, the ML of adult elephant seals was found to be about 1.3% of total MB (Bryden, 1971), a value slightly above Stahl's prediction. Fig. 6. Micrograph of the terminal airways of harbor porpoise (lOA) and the spinner porpoise, Stenella attenuata (lOB). The latter species is closely related and it has a similar lung structure to the S. longirostris mentioned in the text. Serial airway muscles (solid arrow) between the cartilage (open arrows) are much smaller in Phocoena than in S. attenuata. The bar in the upper right corner equals 100 jl.ll1. Histological specimens were obtained from lungs that were preserved by inflating the lungs through the airway with 10':'0 formalin. A pressure of 30 cm H 20 was maintained for about [2 h and then a section of lung was sampl~d for later sectioning and staining. The micrograph shows that the Stenella lung was more evenly inflated, and the airways and alveoli were less congested. This lung was not manipulated, as was the Phocoena lung.

PORPOISE LUNG MECHANICS

295

296

G. L. KOOYMAN AND E. E. SINNETT TABLE 3 Lung mass and volume relative to body mass; a comparison to predictions for terrestrial mammals using the equation ML(g) = 11.3 MB(kg)o99 and VL(ml) = 53.5 MB(kg)106 by Stahl (1967) Animal

ML (g)

Predicted ML VL (g) (I)

1000 580 1610 800 1250

490 275 405 340 425

Predicted VL (I)

-~~-~---~--~~----

6 7 8 9 10

2.9 3.4 4.0 3.0

1.6 2.5 2.0 2.6

----~---~--------~-

_._--_.-

.~-

..-

-

Table 3 also contains predicted values of lung volume (VL) based on MB from the following equation, also from Stahl (1967): VL (ml) = 53.5 MB(kg)106. Our data do not agree well with the values predicted by this equation. ranging from 15 to 100% greater than predicted. Leith, Lowe and Gillespie's (1972) data on the sei whale averaged 121 % of predicted, and their fin whale data averaged only 51 % of predicted, again showing the loose fit of marine mammal data to Stahl's equations. Kooyman (1973) derived the relationship VL(l) = 0.135 MB(kg)092 from published data on several species of marine mammals, and our data on porpoise lung volumes seems to fit this equation better than that of Stahl. The observed values average 102% of the predicted values from Kooyman's equation, with the 'worst' observation being 25% greater than predicted. Combining Stahl's equations for lung volume and lung weight, the VL/ML ratio is given by 4.73 MB(kg)OIl7. Our data give VL/ML ratios which range from 2-5 ml/g lung tissue, values only 35-83% of those predicted by the equation. Hoppin and Hildebrandt (1977) state that a normal value for full lung inflation is about 12-14 ml gas per gram lung weight, a value much higher than would be predicted for any animal under 607 metric tons from the ratio of Stahl's equations. Interestingly, the values of VL/ML measured by Leith, Lowe and Gillespie (1972), which range from 9 to 17 ml/g lung tissue overlap both Hoppin and Hildebrandts predictions and the values predicted by Stahl's equations. The low VL/ML ratios that we observed in the porpoise may reflect an unusual amount of blood trapped in the excised lungs. This would also help explain the departure from Stahl's predicted ML to MB relation. In summary, our data on harbor porpoises indicate that, relative to terrestrial mammals, (l) the ML/MB ratio is large, (2) the VL/MB ratio is large, and (3) the VL/ML ratio is small. Pressure-volume relationships. The pressure-volume curves of the harbor porpoise (fig. 2) have features similar to other marine mammals. Our measurements of MA V ranged from 0 to 17% of TLC, which is lower than the average 18% of sea lions (Denison, Warrel and West, 1971) and overlaps the 4-8% observed in sei and fin

PORPOISE LUNG MECHANICS

297

whale lungs (Leith, Lowe and Gillespie, 1972, and Leith, personal communication). The variability in our measurements ofMAV is probably due in part to the lack of a standard volume history; however, we feel the measurements are of interest in establishing a minimum range for MAVin these animals, and it quantifies more the observation originally made on Phocoena that the lung would deflate passively to a very low volume (Scholander, 1940). This fact that the lungs can be taken to a nearly airless state at the time of death suggested to Scholander, and we agree, that the alveoli may be capable of withstanding complete collapse during life as well. The application of -10 cm HP transpulmonary pressure during the production of PV curves caused the lungs to empty below MA V another I to 3% of estimated TLC (absolute volumes were not measured during each PV curve). In sea lions, the decrease from MAV averaged 12% of TLC when a transpulmonary pressure of -30 cm HP was applied. Pressure~flow relationships. Hyatt et al. (1958) observed that flow became effort independent in the human lung at volumes as high as 70-75% of Vc. Evidence suggests that this property of the lung is due to increased resistance in airways due to their narrowing as pleural pressure exceeds airway pressure (Macklem and Mead, 1968; Pride et al., 1967). Some of these principles and the history of their development have been reviewed by Mead (1961) and more recently by Bouhuys (1974). As the lung volume diminishes the equal pressure point moves upstream (at or close to the point of airway collapse and flow limitation in terrestrial mammals) from its high lung volume position in the large airways to points in the peripheral airways at low lung volumes. The airways of the porpoise, however, are different from the airways of terrestrial mammals in two important respects. First, the cartilaginous support of the upper airways is continuous; there is no membranous sheet across the dorsal aspect. We believe this support allows transmural pressures to be significantly negative before collapse and flow limitation occurs; flowrates in our porpoises were high and effort independence was not reached until driving pressures were quite large (fig. 5). Second, we know from previous studies that the terminal airways of marine mammals are not weak like those of terrestrial mammals, but are quite strong, especially in sea lions and porpoises (Belanger, 1940; Denison and Kooyman, 1973). It has been suggested that this additional airway reinforcement allows higher, sustained flowrates at low lung volumes, and more complete emptying of the lung (Denison, Warrell and West, 1971). The mechanics of flow limitation in the harbor porpoise lung are thus, significantly different from terrestrial mammals. Two of the harbor porpoise lungs consistently emptied within 0.2 sec (fig. 3). This is slightly faster than the 0.25-0.30 sec observed for young sea lions (Kerem, Kylstra and Saltzman, 1975; Matthews, 1977). Untrained gray whale calves took about 0.5 sec to exhale (Kooyman, Norris and Gentry, 1975), and adult Weddell seal expirations, after returning from 20-50 min dives, lasted 1 sec (Kooyman and Sinnett, unpublished observations). During the flow determinations on the harbor porpoise lungs it was not possible to measure the trapped gas volume (i.e. the gas volume in the lungs when no more gas

298

G. L. KOOYMAN AND E. E. SINNETT

can be forced out by further lowering the pressure at the airway opening), while the lungs were still exposed to the large pressure differentials used to empty them. However, the lungs appeared to be empty. If, as we suspect, the live animal is capable of nearly a similar degree of lung deflation, then their VC closely approximates TLC. Thus, the relative measure of flow in VC . sec -I may be a more conservative estimate in porpoises than other mammals. In a review Leith (1976) reports that dogs may reach flowrates as high as 8 VC . sec -I and the bat (species not mentioned) is capable of an exceptional 40 VC . sec -I. The measured peak flowrates in sei and fin whales are I to 2 TLC . sec-I (Leith, Lowe and Gillespie, 1972). Expiratory flows from untrained gray whale calves were not more than 2 VC . sec -I (Kooyman, unpublished observations) and in another study of the California sea lion it was 8 VC . sec -I (Kerem. Kylstra and Saltzman, 1975). The peak flows of the harbor porpoise determined in this study are high. but not exceptional compared to these other mammals. Equally as interesting to us is the unusual profile of the flow-volume curves (fig. 4). Similar to the sei whale (Leith, 1976), and the sea lion (Matthews. 1977), the profile is exceptionally square-waved due to maintenance of the flowrates at low lung volumes. The remarkable bat. despite very high peak flows at large lung volumes, has flowrates similar to the dog at low lung volumes (Leith, 1976). The IVPF curves of fig. 5 show a plateauing of flow rates at endotracheal pressures ranging from -50 to -ISO cm H 20. These pressures are much more negative than the pressures required to reach expiratory flow limitation in man but the fact that plateauing does occur may indicate similar mechanisms are involved in producing effort independence of flowrate. We would postulate that the high flowrates achieved and the high pressure observed before the flow plateaus are a result of airway armoring, which may prevent collapse of airways until a more negative transmural pressure is reached. The convergence of the IVPF curves for 40, 60 and 80% of VC at their plateau value is similar to the convergence observed by Leith (personal communication) in sei and fin whales. This could be explained by a drop in resistance with decreasing lung volume (Leith et al .. 1972). Such a seemingly paradoxical fall in resistance with falling lung volume suggests to Leith (personal communication) that the armored airways of these animals may shorten without decreasing in diameter as lung volume decreases. If a FV curve is plotted from the IVPF data and compared to the typical, healthy human FV envelope (fig. 7) the differences are striking. In the porpoise: (I) flowrates in VC's are much higher, presumably due to the airway strengthening which permits more negative transmural pressures to develop before collapse and significant flow limitation occurs due to airway compression; and (2) flows are maintained at high levels for much of the lung volume. because lung volume has less influence on small airway diameter. The last figure compares the results of our measurements of the dynamic properties of the harbor porpoise lung distal to the glottis and at very high driving

299

PORPOISE LUNG MECHANICS 10

-10

7Pllocoeno I~

6

(f)

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-8

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g

4

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//--~Human

-- ...

//

o /

/

100

/ 80

60

40

20

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VOLUME ( % VC )

Fig. 7. Flow volume profile comparison between the harbor porpoise and man. The harbor porpoise profiles were obtained from the IVPF curves of # 8 and 10.

pressures to those of man in which the flow characteristics also include the resistances of the larynx and mouth, and when the driving pressures are less. We do not know what effects the bony nares, sinuses, and the blowhole have on the flow characteristics of expiration of Phocoena.

Conclusions If the upper airways do not alter the flow characteristics of the lung to any great extent, then the harbor porpoise must be capable of unusually high flowrates over a large percent of its lung volume. Thus, an expiration from TLC to a minimum lung volume can be done in a short time. The natural history of the animal indicates that this rapid and complete turnover is important. It enables the porpoise to achieve a substantial amount of ventilation during the brief period when it rapidly passes through the air~water interface. We conclude that although the small airway reinforcement of marine mammals may be important to deep diving in accordance with Scholander's hypothesis (Scholander, 1940), in some species which have especially robust strengthening of the peripheral airways, such as the small whales, sea lions and fur seals, it has an equally if not more important role in allowing extremely rapid tidal ventilation. This would explain the heavy cartilaginous support in the peripheral airways even of such shallow diving species as the river porpoises, while in the deep diving seals, whose habits do not include the same rapid tidal ventilation, the cartilaginous support is relatively light.

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G. L. KOOYMAN AND E. E. SINNETT

Acknowledgments We are grateful to Dr. D. E. Gaskin, University of Guelph, for sharing his laboratory facilities at Deer Island, New Brunswick; to Dr. D. E. Leith, Harvard School of Public Health, who gave us much help on design and construction of the equipment and on the principles of interpreting flow curves; to Mr. D. L. Urquhart for construction of the pressure-volume, pressure-flow box; and to Mr. R. Howard, who did the computer programming. This work was supported by grants USPHS, HL 16157 and 17731 and Marine Mammal Commission contract MM 4A C012.

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