Respiration Physiology, 68 (1987) 63-75 63

Elsevier

RSP 01266

Lung mechanical properties in the West Indian

Manatee (Trichechus manatus)
Michael Bergey and Horst Baier
Rosenstiel School of Marine and Atmospheric Science and the Pulmonary Division, University of Miami,
MiamL FL 33101, U.S.A.
(Accepted for publication 24 December 1986)

Abstract. Airway dimensions, extent of cartilage reinforcements and lung mechanical properties were
examined in excised lungs of the West Indian Manatee (Trichechusmanatus). All airways with a mean inside
diameter of more than 0.6 mm had complete cartilaginous rings in their walls, and cartilage reinforcement
extended into the respiratory bronchi. Expiratory flow rates over the vital capacity range were higher than
those encountered in humans varying between 20 and 50 ~o of peak flow at 25 ~o of vital capacity. They were,
however, lower than in other marine mammals. The ratio of lung compliance to lung weight was found to
be 0.67 ml/(g • cm H20 ) compared to 0.18 ml/(g •cm H20 ) in terrestrial mammals. This together with a high
gas-tissue ratio of 11 mg/g for the inflated manatee lung indicates that strong airway reinforcements are
necessary to prevent airway collapse during exhalation.

Airways; Compliance; Dead space; Lung; Marine mammal; Mechanics of breathing; Volume

Lungs of m a n y marine mammals are characterized by extensive cartilage reinforcement

in large and small airways (Wislocki and Belanger, 1940; Denison et al., 1971). This has
been interpreted as a mechanism to prevent decompression sickness in deep diving
animals because alveoli are compressed more readily than reinforced airways and thus
nitrogen is excluded from contact with the alveolar epithelium (Scholander, 1940;
Ridgway and Howard, 1979). N o t all marine m a m m a l species, however, are deep divers,
yet all major taxa have substantially reinforced airways (Denison and K o o y m a n , 1973).
Others have theorized that the extensive cartilaginous support of airways allows the very
high expiratory flow rates observed in marine mammals by maintaining airway patency
under driving pressures which would cause airway collapse in land mammals. The
greater cartilaginous support would therefore allow an extremely rapid and large tidal
ventilation with a major proportion of total lung volume exchanged with each normal
breath (Denison et al., 1971; K o o y m a n and Sinnett, 1979).

Correspondence address: Horst Baier; M.D., University of Miami, Pulmonary Division (D60), P.O. Box
016960, Miami, FL 33101, U.S.A.

0034-5687/87/$03.50 © 1987 Elsevier Science Publishers B.V. (Biomedical Division)

64 M. BERGEY AND H. BAIER

To substantiate this hypothesis we investigated expiratory flow characteristics and

airway morphology of excised lungs of the West Indian manatee (Trichechus rnanatus),
a shallow water diver. We found that heavy cartilage reinforcement of the airway enables
the animal to fill and empty its lungs rapidly without large changes in flow resistance.
This allows it to follow a 'high tidal volume, low breathing frequency' pattern and
maintain an adequate minute ventilation without the need for frequent trips to or
extended time spent at the water surface.

Methods

Dead stranded manatees were obtained through the Manatee Salvage Program
administered by the United States Fish and Wildlife Service, Denver Wildlife Research
Center, Gainsville (FL) Field Station under permit P R T 2-8430. Lungs were removed
from 1 to 80 h after death (table 1) and shipped to Miami on ice by air freight.

Morphology and morphometry. Samples of airways and lung tissue for light microscopy
were taken within one hour of death from animal No. 1 ( D W R C Field No. M-202) and
from the other animals after the tests of lung mechanics (see below) were performed.
Standard histological techniques were used to process the tissue. Presence or absence
of cartilage reinforcements were evaluated from sections of uninflated lung by using a
low power magnification.
A vinyl acetate resin cast was made of the unfixed lung of animal No. 4 by enclosing
the lung in an airtight plywood box and maintaining pressure around the lung at - 15 cm
H 2 0 with a vacuum regulator attached to a standard hospital vacuum system. Vinyl
acetate resin was poured at room temperature through a cannula extending through the
box wall and tied into the main bronchus. Lung inflation pressure varied from 20 cm
H 2 0 at the opening of the first lateral bronchus to 75 cm H 2 0 at the dependent part
of the lung due to the hydrostatic pressure of the resin (density 1.06g/ml).

TABLE 1
Manatees studied

Animal Length Weight Sex Interval Cause of death

(cm) (kg) between death
and examination

1 233 254 F 1h Bacterial infection

2 123 14 F unknown Orphaned calf?.
3 259 266 F 80 h at 10 °C Entanglement
4 195 174 F 36 h at 4 ° C Boat collision
5 260 297 M 18 h on ice 'Red tide' poisoning
6 320 628~ M less than 24 h Caught in flood control gate

a Body weight calculated from length data using regression published by OdeU et al. (1981).
 LUNG MECHANICSIN WEST INDIAN MANATEE 65

Measurements of length and diameter of all bronchi and subdivisions from the first
lateral bronchus were taken using calipers after lung tissue was removed by maceration.
A uniform 'shrinkage factor' of 8~o was added to all measurements. This factor was
derived empirically by pouring resin into sections of known diameter rubber and plastic
tubing and measuring the dimensions of the resulting casts. The asymmetrically
branching lung model of Horsfield et al. (1982) was used for labeling airway generations
and to estimate the degree of asymmetry. In order to obtain an estimate of airway
distensibility and hence compliance, airway cross sectional areas from the lung casts
(Ac) were compared with those of the diameters of the main and secondary bronchi of
the uniflated contralateral lung (Ao) in animal No. 4.

Lung mechanics. Pressure-volume and pressure-flow curves were measured

according to Macklem and Mead (1969) and Kooyman and Sinnett (1979). The lung
was placed inside a plethysmograph (box volume 119 L) and connected to a standard
plumbing pipe projecting through the wail of the box. Expiratory maneuvers were
simulated by inflating the lung to 30 cm H20 and venting it into a vacuum reservoir
(220 L oil drum). Maneuvers were repeated at vacuum reservoir pressures varying from
5 to 220 cm H20. The rate of lung deflation (expiratory flow rate) was equal to the air
entry through a pneumotachograph mounted in the wail of the plethysmograph. Due
to differences in lung size, a Fleisch No. 3 pneumotachograph was used for manatee
No. 2 and a 'flow straightener' (Meriam Instruments Inc., Cleveland, OH) for the other
animals together with a Validyne MP 45 pressure transducer (Northridge, CA). A
Hewlett Packard (San Diego, CA) model 7041A x-y recorder was used for data
recording. The system was calibrated with a 3 L syringe by delivering volume pulses at
different speeds. The system was linear within the range of 0.1 to 8.0 L/see for the
Fleisch No. 3 pneumotachograph and within the range of 0.5 to 35.0 L/see when used
with the flow straightener element. Flow-time tracings were digitized by hand for later
computer analysis. Results were discarded if the expiratory driving pressure provided
by the vacuum reservoir changed by more than 10~o during the measurements.
Pressure-volume curves were obtained by varying the pressure on the surface of the
lung from 0 to - 35 cm HzO (TLC) and back to 0 cm H20 in increments of 5 cm H20.
Equilibration periods of 30 sec were allowed between each measurement. Volume
changes were measured with a Tissot spirometer. Static compliance was taken as the
slope of the deflation leg at 50~o of TLC.
Minimum air volume (Vm) was obtained by weighing each lung and then immersing
it (with the main bronchus clamped) in saline solution to obtain total displacement.
Parenchymal tissue volume (assumed to have a density of 1 g/ml) was subtracted from
total displacement to obtain Vm.
Total respiratory system compliance was measured in the field by cannulating the
trachea of animal No. 4 and inflating and deflating the lung with a syringe while
measuring tracheal pressure with a manometer. Functional residual capacity (FRC) was
estimated by measuring the volume of air exhaled from the animal's lungs as they
collapsed after piercing of the hemidiaphragms, and adding this volume to Vm obtained
later from the excised lungs.
66 M. BERGEY A N D H. BAIER

TABLE 2
Central airway dimensions (bronchial cast) from manatee No. 4

Secondary bronchi Main bronchus

Cross Ao/Ac Segment Cross Segmenl

sectional length a sectional lengt ha
area (era 2) (cm) area b (cm 2) (era)

1st lateral 0.28 0.91 0.84 2.84 2. I

1st dorsal 0.053 0.87 0.58 2.41 2.2
2nd dorsal 0.038 0.87 0.26 2.09 1.3
2nd lateral 0.27 0.93 1.20 2.01 1.8
1st medial 0.023 0.87 0.88 1.77 0

3rd dorsal 0.031 0.84 0.31 1.77 3.2

4th dorsal 0.031 0.84 0.55 1.65 0.7
2nd medial 0.066 0.89 0.71 1.54 1.2
3rd lateral 0.35 0.86 1.64 1.33 1.3
5th dorsal 0.071 0.82 0.47 1.23 0.3

3rd medial 0.045 0.84 1.05 1.23 3.0

4th medial 0.035 0.94 0.80 1.13 0.3
6th dorsal 0.075 0.83 0.45 1.04 2.9
4th lateral 0.27 0.9t 1.40 0.95 2.3
5th medial 0.096 0.86 0.40 0.90 1.1

7th dorsal 0.057 0.79 0.30 0.79 1.2

6th medial 0.057 0.89 0.90 0.87 1.8
7th medial 0.018 0.93 0.44 0.75 0.9
5th lateral 0.15 0.98 0.88 0.79 2.7
8th medial 0.086 0.86 0.78 0.62 2.5

6th lateral 0.13 0.87 1.72 0.64 2.0

9th medial 0.080 0.90 0.53 0.52 2.0
8th dorsal 0.028 0.93 0.45 0.44 0.3
lOth medial 0.035 0.89 0.72 0.45 1.1
7th lateral O.12 0.92 0.90 0.42 1.0

1 lth medial 0.031 0.91 0.52 0.29 1.9

9th dorsal 0.025 0.88 0.30 0.30 0.7
10th dorsal 0.028 0.93 0.81 0.22 1.1
12th medial 0.031 0.80 0.53 0.20 0.8
8th lateral 0.096 0.96 0.84 0.16 -

a Segment length denotes length of airway between branching points.

b Cross sectional area of main bronchus at branching points of secondary bronchi.
Ao/Ac, ratio of airway cross sectional areas of uninflated lung (Ao) and lung cast (Ac).
 LUNG MECHANICS IN WEST INDIAN MANATEE 67

LI~//L2 L3 L4 L5 L6 T"
L'~~L
L"
L 8
// ,:

Fig. 1. Schematic of branching pattern of large airways. T = trachea; M = main bronchus; L, M,

D = lateral, medial, dorsal bronchi, respectively.

Results

The manatee lung is long and flat without external lobulation. Figure 1 shows a
schematic of the branching pattern of the large airways. A large 'main bronchus' which
extends outside the lung parenchyma is located close to the diaphragmatic surface of
the lung for most of its length. A varying number (8-12 each) lateral, medial and dorsal
bronchi branch off the main bronchus at regular intervals. The dimensions of these
airways are given in table 2. All airways with a mean inside diameter of more than
0.6 mm have complete cartilaginous rings. Respiratory bronchioles originate from
terminal bronchioles with an average diameter of 0.48 mm and cartilaginous reinforce-
ments can still be found at this level (fig. 2). Table 3 gives the dimensions of the
peripheral airways. Cross sectional areas of bronchi obtained in animal No. 4 from the
uninflated lung (Ao) and the lung cast (Ac) are given in table 2. The ratio Ao/Ac varied
between 0.79 and 0.98 indicating a low airway distensibility.
Respiratory parameters of the animals examined are given in table 4 and maximum
expiratory flow rates at 75 ~ , 5 0 ~ and 25 ~ of vital capacity in table 5. Representative
isovolume-pressure-flow curves for the excised left lung of animal No. 5 are shown in
fig. 3a and expiratory flow volume curves in fig. 3b. The curves reached a plateau at
driving pressures above 100 cm H20 at low lung volumes. Expiratory pressure-volume
curves obtained from animal No. 4 are shown in fig. 4. The curve for the chest wall was
calculated by subtracting recoil pressure of the lungs from total recoil pressure. Static
lung compliance was greater by an order of magnitude when compared to terrestrial
mammals.
68 M. B E R G E Y A N D H. B A IER

Fig. 2. Microphotograph of terminal airways and respiratory bronchi showing extensive cartilage reinforc~
ments. Magnification x 75. : '

TABLE 3

Airway dimensions of bronchial cast from manatee No. 4

Order Mean diameter s n Mean length s n

number (ram) (ram)

20 5.93 - 1 8.44 - 1
19 4.98 - 1 4.33 - 1
18 2.94 - 1 8.32 - 1
17 3.05 1.2 2 12.88 8.7 2
16 2.16 0.51 2 3.94 3.1 2

15 1.53 0.078 2 6.73 3.6 2

14 2.05 0.88 5 4.04 1.91 5
13 1.52 0.40 7 4.11 1.7 7
12 1.18 0.37 9 4.54 1.3 9
11 1.09 0.308 13 3.32 1.7 14

10 0.950 0.19 21 2.98 1.3 21

9 0.874 0.22 33 2.34 0.80 34
8 0.747 0.17 42 2.31 0.91 48
7 0.677 0.17 57 1.97 0.77 67
6 0.602 0.13 77 1.68 0.56 104

5 0.513 0.13 137 1.42 0.64 170

n = sample size; s = + standard error.

 TABLE 4
Respiratory parameters

Animal lungs

No. 2 No. 3 No. 4 No. 5 No. 6 2~

Right
Right Left Right Left Right Left Right Left

WL (kg) 0.16 0.95 0.98 0.27 0.28 0.97 1.05 1.80 1.70
TLC (L) 1.66 11.9 11.8 3.60 3.87 11.5 11.6 21.0 19.2
VC(L) 1.53 11.4 11.1 3.35 3.60 11.0 10.9 19.2 17.5
FRC (L) 8.6 2.7
vm (L) 0.13 0.53 0.77 0.24 0.27 0.52 0.65 1.78 1.70
Vm/TLC ( × 100) 7.83 4.62 5.59 6.94 6.98 4.61 5.52 8.57 8.85
Peak flow (L/see) 3.63 19.8 18.3 34.5 32.8
Peak flow (VC/sec) 2.37 1.80 1.68 1.80 1.87
Exhalation time (sec) 0.82 1.05 1.10 1.07 0.97 ;~
C(St)L (L/cm H20 ) 1.40 1.43 0.369 0.366 1.56 1.62 2.46 2.48
C(st)sp (L/cm H20 ) 0.20 0.24 0.24 0.21 0.19 0.27 0.28 0.23 0.26
C(st)t (L/cm H20 ) 0.379 0.127 L
WL/WB (X 10 -3) 11.4 3.57 3.68 1.55 1.61 3.27 3.54 2.87 2.71
VC/WL (L/kg) 9,56 12.0 11.3 12.4 12.9 11.3 10.4 10.7 10.3
C(St)L/WL (L/kg" cm H20 ) 1.47 1.46 1.37 1.31 1.61 t.54 1.37 1.46

WL = lung weight; TLC = total lung capacity; VC = vital capacity; FRC = functional residual capacity; Vm = minimum air volume; C(St)L = static lung
compliance; C(st)s p = specific lung compliance; C(st)t = total respiratory system compliance; WB = body weight.
70 M. BERGEY AND H. BAIER

2.0 m

75% VC
"6'
@
1.5

u
P.
1.0
5 0 % VC

,-;- 0.5
25% VC

' I I I I
+50 0 -50 -100 -150 -200
Pressure (cmH20)
Fig. 3. (a) Isovolume-pressure-flow curves of the excised left lung of animal No. 5. Numbers on the righl
end of each curve denote percent of vital capacity.

O
@ O
o
ra

iI
0 50 1 O0
Expired V o l u m e (%VC)
Fig. 3. (b) Expiratory flow-volume curve of excised left lung of animal 5.

Discussion

The lungs used in this study may have been in different states of preservation because
of logistical difficulties of securing dead animals due to the manatee's status as an
endangered species which does not allow sacrifice for study. Of the animals investigated,
only No. 4 and No. 6 were animals killed quickly by external factors (table 1). Animal
 LUNG MECHANICS IN WEST INDIAN MANATEE 71

TABLE 5
Maximum expiratory flow rates at 75~o, 50% and 25~o of VC

Animal Driving pressure VC/see

lung (cm H20 )
75Z v c 5o% 25% v c

No. 2 left 20 1.13 1.05 0.87

40 1.48 1.44 0.87
60 1.66 1.56 0.85
80 1.82 1.62 0.99
100 1.76 1.58 0.95
120 1.84 1.60 0.85
140 2.03 1.74 0.97
160 1.99 1.82 1.03
180 2.13 1.74 0.91
200 2.27 1.72 0.95

No. 5 right 100 1.52 1.44 0.87

140 1.54 1.40 0.66
160 1.62 1.36 0.71

No. 5 left 40 0.925 0.60 0.25

80 1.38 0.99 0.38
120 1.64 1.18 0.47
160 1.55 1.00 0.42
180 1.66 0.91 0.32
200 1.52 0.89 0.34

No. 6 right 120 1.42 0.93 0.39

160 1.54 1.05 0.43
200 1.56 0.97 0.41

No. 6 left 120 1.38 0.85 0.30

160 1.44 0.97 0.49
180 1.50 1.11 0.55
200 1.68 1.14 0.61

No. 2 was an o r p h a n e d calf which apparently starved to death. Thus, the body weight
was extremely low for the animal's size.
Several authors have described the structure of the respiratory tract of marine
m a m m a l s (Wislocki a n d Belanger, 1940; Murata, 1951; D e n i s o n et al., 1971; H a l d i m a n
etal., 1980). In all species, extensive cartilage reinforcements were f o u n d which
extended to the level of the terminal bronchioles. I n some species (Physeter catodon,
Stenella coeruleoalba) cartilage has been reported to extend into the alveolar ducts
(Murata, 1951). Sea lions (otariids) had the most divergent airway structures in
pinnipeds. I n this species all airways had extensive cartilaginous support a n d emptied
directly into alveolar sacs; respiratory bronchioles a n d alveolar ducts were n o t found
72 M. BERGEY AND H. BAIER

Human
Lung Lung Lung &
100- ~,..,,,,,,,m~*~ ~ Cheat Che~

80-

~ 40-

20-

f
I I i I I I
0 10 20 30 40 50 60
Pressure (cmH20)

Fig. 4. Expiratorypressure-volumecurvesobtainedfromanimalNo. 4. Hatched curvedenoteshuman lung

pressure-volume curve (Agostoni and Hyatt, 1986).

(Denison and Kooyman, 1973). Several papers dealing with the lung morphology of
dugongs (a species related to the manatee) have been published (Pick, 1907; Wislocki,
1935; Engels, 1962). In these studies cartilaginous reinforcements of the tracheobron-
chial tree were found to be extensive and extended into the walls of the smallest
bronchioles. We found a similar distribution of cartilage in the West Indian manatee
with an extension to the level of the respiratory bronchioles.
Studies of lung mechanics of the California sea lion (Zalophus californianus) and fin
and sei whales (Balaenoptera physalis, B. borealis) showed that some marine mammal
lungs can be emptied to very low lung volumes (Leith etaL, 1972; Denison and
Kooyman, 1973).
Reinforcement of peripheral airways in the manatee is of questionable importance as
a mechanism for limitation of nitrogen absorption at depth, as has been suggested for
other marine mammals. Manatees feed on benthic and floating vegetation which is most
abundant in very shallow waters, and the animals seldom need to dive below 10 m
(Hartman, 1979). Investigations of fossils seem to show the same life style for the
manatee's ancestors as well (Domming, 1982). Recent studies in the bottle-nosed
dolphin (Tursiops truncatus) indicate that the animal is not protected from d e c o m -
pression hazards by lung collapse during dives to depths less than 70 m (Ridgway and
Howard, 1979). However, their data indicate that some constraint ofnitr0gen transport
has occurred at shallower depth due to compression shunt. It is thus still conceivable
that airway reinforcements in the manatee lung might have some usefulness in reduction
of nitrogen absorption during dives to a shallower depth.
The conceptual model of expiratory flow by Fry (1958) and Fry and Hyatt (1960)
limits forced expiratory flow at low lung volumes by collapse or compression of
 LUNG MECHANICS IN WEST INDIAN MANATEE 73

segments of peripheral airways. According to the wave-speed concept, flow limitation

in elastic tubes occurs at a speed at which the fluid in the tube propagates pressure waves
and is a function of gas density, tube size and the elastic modulus of the tube wall
(Dawson and Elliott, 1977; Lambert e t a L , 1982). Therefore, extensive cartilage
reinforcement of the manatee airway walls allows greatly increased maximum flow rates
at all lung volumes by reducing expiratory airway wall compliance and thus increasing
wave-speed. Comparison of hydrostatically distended airway cross sections in lung
casts (Ac) with corresponding dimensions in the collapsed lung (Ao) revealed very low
values for manatee airway distensibility (table 2). The ratio of Ao/Ac was never less than
0.79 for any distension pressure or airway size. In humans, a coefficient of distensibility
of this magnitude is found only in the central airways (Lambert etal., 1982). This
suggests that the presence of cartilaginous rings in manatee airways cause airway
characteristics to be uniform throughout the bronchial tree, as contrasted with the rapid
decrease in coefficient of distensibility with decreasing airway size in humans. The
model of Lambert et al. (1982) could not be tested quantitatively for the airways of the
manatee because of its assumption of symmetrical branching which is not found in the
manatee airways.
Throughout the vital capacity range, we observed high flow rates in the excised
manatee lungs in comparison with human lungs. In harbor porpoises, flow rates have
been reported as high as 80~o of peak flow when the lung contained 25~o of VC,
compared to about 20~o of peak flow for the human lung at the same degree of lung
inflation (Kooyman and Sinnett, 1979). Flow rates for the manatee lungs studied here
were intermediate between these two extremes. Flow rates at 25 ~o of VC varied from
20 to 50~o of peak flow, the lowest values yet reported in a marine mammal for this
portion of the MEFV curve (fig. 3b). In excised lungs of the California sea lion, the
harbor porpoise, and balaen whales expiratory flow rates at different driving pressures
did not plateau at high lung volumes even with driving pressures as high as 300 cm H20
(Leith et al., 1972; Kerem et al., 1975; Kooyman and Sinnett, 1979). However, in the
manatee flow limitation occurred at lower driving pressures up to 759/0 of VC.
Compliance of manatee lungs follows the regression published by Stahl (1967) and
Spells (1970) for log compliance vs body weight. However, there are great differences
between other respiratory dimensions in the manatee and terrestrial mammals. The ratio
of lung compliance to lung weight is 0.67 ml/(g- cm HzO ) in the manatee while the
'size-independent' value for terrestrial mammals is only 0.18 ml/(g • cm H20 ). The ratio
of vital capacity to lung weight for the manatee is 11 ml/g, also much larger then the
terrestrial mean of 5.0 ml/g, revealing a high gas/tissue ratio for the inflated manatee
lung. In human lungs, relatively high elastic recoil forces ensure patency of peripheral
airways, whereas in the manatee airway reinforcement may be partially compensating
for the low elastic recoil.
On the other hand chest wall compliance in the manatee is rather low when compared
to other marine mammals (Leith, 1976). Total respiratory system pressure-volume
curves (fig. 4) for the manatee show that both lung and chest wall recoil inward for most
of the VC range. Lung volume at zero inflation pressure (approximately 28~ TLC) is
74 M. BERGEY AND H. BAIER

below the F R C r e p o r t e d for the living m a n a t e e ( S c h o l a n d e r a n d Irving, 1941). This

seems to imply that m a n a t e e s would exhale passively with considerable force at all lung
volumes. In fact, they m a y rarely reach their F R C as defined for h u m a n s (lung elastic
recoil equals chest wall recoil pressure) b e c a u s e o f voluntary closure o f the nostrils or
glottis before this volume is reached. I f the lungs contain 50 ~ o f T L C at the end of
expiration ( S c h o l a n d e r and Irving, 1941), lung recoil pressure will be 3 c m H 2 0 and
chest wall recoil pressure will be 20 c m H 2 0 (from fig. 4). I f we a s s u m e the center of
the animal's lungs to be about 35 cm below the surface when the m a n a t e e ' s nostrils open
for exhalation, a 35 c m H 2 0 hydrostatic pressure gradient will result in a total (passive)
driving pressure o f 58 c m H 2 0 if thoracic muscles were relaxed during exhalation, This
is already above the driving pressure typical for expiratory flow limitations in h u m a n s
(approximately 20 c m H 2 0 ; F r y a n d Hyatt, 1960). It is therefore n o t surprising that
m a n a t e e airways have to be strongly reinforced.

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