J. Anat.

(2005) 207, pp365380

An allometric study of lung morphology during

development in the Australian pelican, Pelicanus
conspicillatus, from embryo to adult
Blackwell Publishing, Ltd.

S. Runciman,1 R. S. Seymour,2 R. V. Baudinette2 and J. T. Pearson3

1

Anatomy & Histology, Flinders University of South Australia, Adelaide, South Australia 5001
Environmental Biology, University of Adelaide, Adelaide, South Australia 5005
3
Department of Physiology, Monash University, Clayton, Victoria, Australia 3800
2

Abstract
Pelicans produce altricial chicks that develop into some of the largest birds capable of sustained flight. We traced
pulmonary morphological development in the Australian pelican, Pelicanus conspicillatus, from third trimester embryos
to adults. We described growth and development with allometric relationships between lung components and
body mass or lung volume, according to the equation y = ax b. Pelican lung volume increased faster than body mass
(b = 1.07). Relative to lung volume, the airways and vascular spaces increased allometrically (b > 1) in embryos, but
isometrically (b 1) after hatching. Parabronchial mantle volume decreased (b < 1) prior to hatching and increased
isometrically thereafter. Surface area of air capillaries, blood capillaries and the bloodgas barrier increased relative
to lung volume (b > 0.67) before and after hatching. Barrier thickness decreased before hatching, remained constant
in juveniles and decreased by adulthood. The anatomical diffusing capacity significantly increased before hatching
(b = 4.44) and after hatching (b = 1.26). Although altricial pelicans developed pulmonary complexity later than precocial
turkeys, the volume-specific characteristics were similar. However, lungs of volant adult pelicans became significantly
larger, with a greater capacity for gas exchange, than lungs of terrestrial turkeys. Exchange characteristics of growing pelican lungs were inferior to those of adult birds of 26 other species, but converged with them at maturity.
Key words altricial; bird; development; morphometry; pulmonary.

Introduction
Pulmonary morphometry has been shown to be a
valuable approach for understanding the links between
form and function in relation to the evolution of animal
design and behaviour (Maina, 2002). In particular,
morphometric techniques have led to the identification of the functional subunits involved in determining
diffusing capacity, which is the primary measurement
of pulmonary function. They have further provided the
basis for pulmonary modelling, which allows analysis of
the design of the gas exchanger in relation to its func-

Correspondence
Dr Sue Runciman, Department of Anatomy & Histology, Flinders
University of South Australia, GPO Box 2100, Adelaide, South Australia
5001. E: sue.runciman@flinders.edu.au
Deceased.
Accepted for publication 29 June 2005
Anatomical Society of Great Britain and Ireland 2005

tional requirements, as determined by behaviour, size

and environment. The adult avian lung has been
qualitatively and quantitatively investigated in a large
number of species (Duncker, 1972; Abdulla, 1977; Dubach,
1981; Abdulla et al. 1982; Maina & King, 1982a,b, 1984,
1989; Maina, 1982, 1993; Powell & Mazzone, 1983;
Maina et al. 1989; King et al. 1992; Maina & Nathaniel,
2001). These studies and a number of reviews comparing
lung structure and function across avian species (Maina
et al. 1989; Maina, 2000, 2002), flying bats (Maina &
King, 1984) and other mammals (Maina et al. 1989)
have contributed significantly towards understanding
pulmonary gas exchange.
The developing lungs of embryonic and juvenile birds,
however, have received little attention. There is nothing on structural development of lungs in a recent
comprehensive review of morphological development
in birds (Starck, 1998). Jones & Radnor (1972) described
the morphological events in the developing lung in the

366 Lung growth in the pelican, S. Runciman et al.

White Leghorn domestic fowl, Gallus gallus, from the

13th day of incubation to hatching. Duncker (1977)
described lung development in precocial domestic fowl
and Khaki-Campbell ducks, Anas platyrhynchos, and in
altricial domestic pigeons, Colomba livia, in the parahatching period. His study identified some of the morphological differences in the lung between altricial and
precocial species at the time of hatching and related
these differences to motor activity and behaviour. It
also provided the first description of the rapid development of the gas exchange tissue that coincides with the
onset of pulmonary respiration. More recently, attention has been paid to the development of the avian
bronchial airway (Maina, 2003a,b). The only morphometric study of avian lung development we are aware
of is that of the Timmwood et al. (1987) on the precocial turkey, Meleagris gallopavo, which quantified the
changes that occur from 22 days of incubation to maturity. That light-microscopic study was limited, however,
because some critical measurements (e.g. diffusion
distance) were not reported.
We investigated the development of the lung in the
Australian pelican, Pelicanus conspicillatus (Temminck),
using light and transmission electron microscopy, and
have applied morphometric techniques to quantify the
changes that occur during the last third of incubation
through to maturity. This species lays large eggs (140
210 g) from which large altricial hatchlings (8090 g,
yolk free) emerge after an incubation period of 33
34 days (Pearson et al. 2002). The hatchlings are naked,
uncoordinated and unable to thermoregulate, but they
develop into one of the largest birds (9 kg) capable of
strong, sustained flight. We present our data in allometric form, in relation to body mass and lung volume,
specifically to compare the ontogeny of pulmonary
structure in the volant pelican with that in the domestic
turkey, a precocial species that is essentially terrestrial
(Timmwood et al. 1987). Where possible, we also draw
comparisons with adult lung structure and function in
26 avian species using data from Maina et al. (1989).
This study continues a programme investigating the
development of respiration in the Australian pelican
(Pearson et al. 2002; Seymour et al. 2004).

Materials and methods

Lungs were collected from pelicans ranging in age from
24-day incubation embryos, 34-day hatchlings, nonvolant juveniles and one adult. The eggs and birds were

collected from a breeding colony at Outer Harbour,

Adelaide, South Australia. Eggs were incubated in the
laboratory (Pearson et al. 2002). The 11- and 21-day
post-hatch birds were raised from hatchlings in the laboratory, and the five juveniles and one adult (a breeding male attending a nest) were collected from the
colony and used immediately. Techniques of obtaining
and fixing lung specimens from these birds are described
elsewhere (Seymour et al. 2004). Briefly, birds were
asphyxiated with CO2, the trachea tied, the body weighed
and the CO2-filled lungs fixed with 2.5% glutaraldehyde
in a 0.01 mol L1 phosphate buffer solution (pH 7.4,
350 mOsm) with the reservoir located 20 cm above the
level of the sternum. The lungs were then removed and
sliced into sections in the plane of the costal sulci. Small
lungs from the embryos and smaller birds were cut into
slices 1.02.5 mm thick. Larger lungs were cut into slices
57 mm thick. The total volume of both lungs (VL),
including air and tissue, was determined with the
Cavalieri method (Howard & Reed, 1998). Samples were
taken from the left lung for light microscopy and from
the right lung for transmission electron microscopy.

Light microscopy (LM)

All slices from the small lungs and ten equidistantly
spaced slices from the larger lungs were processed for
LM. Slices were dehydrated in an ascending series of
ethanol (70100%), cleared in chloroform and embedded
in paraffin wax with the rostral surface down. A 5-m
section was cut from each embedded slice, mounted on
a glass slide, stained with Haematoxylin and Eosin, and
viewed with a Leitz microscope.

Transmission electron microscopy (TEM)

Ten pieces of tissue, 2 mm in diameter, were sampled
from the right lungs as described by Weibel (1984).
Lung pieces were stained with 2% osmium tetroxide,
en bloc stained with 2% uranyl acetate, dehydrated in
an ascending series of alcohol, cleared in propylene
oxide and embedded in Durcupan embedding resin
(Fluka Chemie AG, Sigma Chemicals, St Louis, MO, USA).
Gold to silver sections were cut with a diamond knife,
with the ultramicrotome set to cut at 100 nm, from
blocks trimmed to contain only gas exchange tissue of
the interparabronchial mantle. Sections were collected
on copper thin-bar 200 square mesh grids and stained
with lead citrate prior to viewing in a Joel JEM 1200-EX
Anatomical Society of Great Britain and Ireland 2005

Lung growth in the pelican, S. Runciman et al. 367

transmission electron microscope at an acceleration

voltage of 80 kV.

Morphometry
A four-level cascade sampling design (Cruz-Orive &
Weibel, 1981) was employed as follows. Sampling cascade
levels and phases of interest: level 1, parenchymal and
non-parenchymal (large blood vessels, bronchi, connective tissue) volume at 4 magnification; level 2,
parenchymal composition (secondary and tertiary
parabronchi, atria and interparabronchial mantle) volume
at 20 magnification; level 3, air and blood capillary
volume and surface densities at 8000 magnification;
level 4, the tissue barrier at up to 32 000. Morphometric
measurements as described by Weibel (1979) were
used to estimate volume and surface densities.

Light microscopy
Point counts were carried out at 4 and 20 magnification. Counts at low magnification were carried out on
all lung sections of the smaller lungs. Counts on the
larger lungs and counts at 20 magnification were
carried out on sections and fields sampled using a systematic sampling technique (Weibel & Cruz-Orive, 1991). A
minimum of ten entire sections at 4 magnification and
a minimum of 20 fields at 20 magnification were
counted. Images of the sampled sections and fields were
captured by using a Canon EOS-1 camera mounted on
an Olympus BX50 microscope and imported into Coreldraw 9 (Corel Corp.). Grids were superimposed on the
images. Images at 4 magnification were used to determine the volume densities of the non-parenchyma
(Vvnp) and parenchyma (Vvp). The non-parenchymal
component included bronchi (Vvbr), large blood vessels (Vvbl) with a diameter greater than 25 m and connective tissue (Vvct). The parenchymal component of
the lung included parabronchial lumina (Vvpbl), atria
(Vvatr), interparabronchial tissue (Vvpm), interatrial
septa (Vvias) and small blood vessels (Vvsbv). Volume
densities of the parenchymal components were determined at 20 magnification.

Transmission electron microscopy

Ten sections from each bird lung were viewed at 2000
magnification and sampled using the systematic quadrats subsampling technique (Mller et al. 1981). Six fields
Anatomical Society of Great Britain and Ireland 2005

were sampled from each section, giving 60 fields per

lung. Images of the sampled fields were imported into
Coreldraw 9. A grid was superimposed on the image
and the zoom option in the program was used to magnify the image, maintaining the correct proportions, so
that parameters could be clearly identified and distances measured accurately. Images were magnified up
to 400% for point and intersection counts, and up to
1600% for intercept length measurements.
The volume densities of the air capillaries (Vvac), blood
capillaries (Vvbc) and tissue (Vvt) were determined by
point counts, and the surface densities of the air spaces
plus air capillaries (Sva), and the blood capillaries (Svc)
were determined according to Maina et al. (1989). Surface area of the bloodgas barrier (St) was measured by
counting line intersections between air capillaries and
blood capillaries. Pelican lung parenchyma is similar in
appearance to that of other bird lungs. Maina et al.
(1989) investigating lungs from 42 species determined
that the arrangement of the air and blood capillaries in
the gas exchange tissue is isotropic. Horizontal and vertical intersection counts to determine surface densities
were made on an internally pipped specimen, a hatchling, a 21-day-old chick, a juvenile and the adult
pelican. The counts were not significantly different
(MannWhitney, P > 0.05). Further measurements were
made horizontally only.
The harmonic mean thickness of the bloodgas tissue
barrier (ht) was calculated as ht = 2/3[n/(1/L)]M1, where
n is the number of measured intercepts, 1/L is the sum
of the reciprocal of the intercept lengths and M is the
final magnification (Weibel, 1979). Absolute volumes
and surface areas were calculated using the reference
volume, for example Vp = Vvp VL. The ratio St /ht
multiplied by Kroghs coefficient of oxygen diffusion
(2.46 107 cm2 min1 kPa1) was used to determine the
anatomical diffusing capacity of the bloodgas tissue
barrier.
Asphyxiation with carbon dioxide is an accepted
method of killing birds and assists the infusion of fixative
into the air sacs and the lung as it readily diffuses from
air to blood. The fixation and tissue preparation procedures used in this study closely matched those of other
studies involving LM and TEM (Abdulla et al. 1982;
Timmwood et al. 1987; Maina & King, 1989; Maina
et al. 1989) so that any shrinkage that occurred was
comparable with that of lung tissue in other studies
used for comparison. We did not attempt to adjust
morphometric values for shrinkage.

368 Lung growth in the pelican, S. Runciman et al.

The estimate of lung volume using the Cavalieri method

removed the problem of underestimation due to water
entering the lung and allowed more accurate measurement of small lung volumes. As lung volume was determined after fixation and before tissue processing, and
as we used a buffered glutaraldehyde solution of
350 mOsm, shrinkage would have been minimal at this
stage. We therefore expect any error to be small.
Surface areas in the pelican were calculated from
measurements captured at 2000 magnification and
increased by 400% whereas a magnification of 400 was
used to determine the values in the turkey (Timmwood
et al. 1987). Higher values for surface areas result from
measurements at higher magnifications because of
greater image detail the so-called Coast of England
Effect (Weibel, 1979). This may account for the higher
surface area values found in pelicans than in turkeys.
Differences in measurement of volumes were not
subject to this potential error as measurements were
carried out at similar magnifications, and measurement of volume density is stable at a wide range of
magnifications.
Volume density measurements from paraffin-embedded
sections are not affected by shrinkage (Weibel, 1979),
and surface density measurements from tissue processed
for TEM shrink 5% or less (Weibel & Knight, 1964).
Therefore, we did not correct for shrinkage. Timmwood
et al. (1987) carried out surface density measurements
on paraffin-embedded sections and corrected for
shrinkage, whereas Maina et al. (1989) used the same
techniques as in this study and also did not correct for
shrinkage. Thus the three studies are comparable.
Microsoft Excel was used for data collection, morphometric calculations, regression analysis and plots.
Analysis of covariance was used to test differences in
regression slopes and elevations (Zar, 1998). Significance
is indicated by 95% confidence intervals (CI). When the
slopes were significantly different, regions of significantly
different y-variables were identified with the Johnson
Neyman technique, and P values are reported (White,
2003). The results were considered in two groups, both
of which contained the hatchlings: Group P1 comprised
data from the embryos and hatchlings and Group P2
contained data from hatchlings through to the adult bird.

Results
The morphological changes that occur during lung
development are illustrated in Fig. 1. At day 24 of incu-

bation small-diameter, smooth-walled parabronchi are

found throughout the mesenchymal tissue (Fig. 1a).
Maina (2003b) and Jones & Radnor (1972) distinguish
parabronchi from secondary bronchi. Secondary bronchi are lined with a simple layer of cuboidal epithelium
with an underlying layer of smooth muscle. Developing
parabronchi are lined by tall cells with luminal surfaces
that protrude or bulge into the lumen. The wall is usually 23 cells thick in parabronchi prior to the development of the atria. The smooth muscle layer underlying
the epithelium is more substantial, both in continuity
and in thickness of secondary bronchi. Shallow atria and
a few infundibula and putative air capillaries appeared
at day 30 of incubation. Interatrial septa were short
and thick with club-shaped ends containing smooth
muscle cells. At internal pipping, around day 32 of incubation, atria and infundibula had deepened, and a few
air capillaries were seen (Fig. 1b). Expanded parabronchi
were found throughout the lung in the hatchling. The
interparabronchial mantle was thin, atria had increased
in width and depth, and interatrial septa had lengthened.
Smooth muscle was prominent in the club-shaped luminal ends (Fig. 1c). By 11 days after hatching, the parabronchial mantle had increased in thickness, the atria
had deepened, infundibula were well developed and
small-diameter air capillaries with adjacent blood
capillaries were numerous (Figs 1d and 2a).
Further lung development was characterized by a
thickening of the interparabronchial mantle, development of numerous small-diameter air capillaries (Fig. 2a,b)
surrounded by blood capillaries, deepening and widening of the atria, lengthening and thinning of the interatrial septa, and further decrease in cellularity of the
interparabronchial mantle. In the lung of preflight
juveniles, blood capillary to blood capillary contact was
common, but relatively little air capillary to air capillary
contact occurred. Substantial interstitial tissue intervened between the blood capillary endothelium and
the air capillary epithelium (Figs 1e and 2a). In the lung
of the adult, interstitial tissue and blood capillary to
blood capillary contact was markedly decreased (Fig. 1f).
Attenuated epithelial cells sharing a basement membrane separated adjacent air capillaries (Fig. 2b,c). The
air/blood barrier consisted of a very thin epithelial layer
separated from the capillary endothelium by a fused
basement membrane, resulting in a very thin air/blood
barrier with a harmonic mean thickness of 0.174 m
(Fig. 2c). Connective tissue was sparse throughout development and was concentrated around large blood
Anatomical Society of Great Britain and Ireland 2005

Lung growth in the pelican, S. Runciman et al. 369

Fig. 1 All sections were stained with Haematoxylin and Eosin and are at the same magnification. a, atria; bv, blood vessels;
pb, parabronchi; m, mesenchymal tissue; sb, secondary bronchus. Arrowheads indicate smooth muscle cells. Arrows denote
infundibula. (a) The lung in the pelican embryo at 24 days of incubation. Parabronchi with narrow lumina can be seen in the loose
mesenchymal tissue. The cluster of cells indicated by the asterisk is the site of development of a new parabronchus. (b) At internal
pipping, about 2 days before hatching, shallow atria open from the parabronchi. The interatrial septa are thick and have
club-shaped luminal tips. Infundibula indicated by arrows extend into the parabronchial mantle that contains a small amount
of mesenchymal tissue and blood vessels. Small-diameter airspaces in the mantle may be air capillaries or infundibula. The
arrowheads indicate a layer of smooth muscle underlying the parabronchial epithelium in a region where atria have not yet
developed. (c) In the hatchling lung, atria have deepened, infundibula are more common and a few small-diameter airspaces
are seen. The parabronchial tissue is markedly reduced and there is little mesenchymal tissue. (d) At 11 days after hatching the
thickness of the parabronchial mantle (pm) has increased. Atria and infundibula are well developed and lead into air capillaries
that are surrounded by a network of blood capillaries. Smooth muscle cells are seen at the luminal tips of the interatrial septa.
Small areas of undifferentiated tissue are seen in the parabronchial mantle (*). (e) At 21 days after hatching atria are deep and
infundibula extend far into the parabronchial mantle. Blood vessels, indicated by the asterisks, are located at the bases of the
interatrial septa. The mantle contains a network of air and blood capillaries as well as larger air spaces and is still very cellular.
There is no interparabronchial septum of connective tissue. (f) In the adult lung interatrial septa have thinned but have retained
their club shape due to the group of smooth muscle cells at the tip. This smooth muscle forms a ring around the openings of the
atria and provides structural support maintaining the patency of the atria (Duncker, 1972). The parabronchial mantle is thick,
and the cellularity has largely been replaced by a network of air and blood capillaries. Blood vessels are seen at the bases of the
interatrial septa (*). Infundibula extend and branch deep into the parabronchial mantle.

vessels and large airways. There was no interparabronchial septum and the mantles of the adjacent parabronchi merged (Fig. 1cf).
Body mass (Mb), total lung volume (VL), absolute
volumes, surface areas and thicknesses are presented
Anatomical Society of Great Britain and Ireland 2005

in Tables 1 and 2. Body mass (yolk free) ranged from

16.24 g in the 24-day embryo to 7.19 kg in the adult
bird. One of the juveniles weighed 8.83 kg. VL ranged
from 0.28 cm3 at 24 days of incubation to 316 cm3 in
the adult. VL increased significantly faster than body

370 Lung growth in the pelican, S. Runciman et al.

mass (b = 1.07 0.04 CI) (Fig. 3). There was no break in

the slope of the regression between the embryo to
hatchling group (P1) and the hatchling to adult group
(P2) (P = 0.51).
Because this study was designed to quantify the
differentiation and maturation of the lung during
development, all further allometric descriptions relate
pulmonary variables to total lung volume (VL). Volumes
scaling isometrically with VL, i.e. they increase in proportion to VL by uniform enlargement, are expected
to scale with VL to the power 1.0 (VL1). Surface areas
scaling isometrically increase with VL0.67. Linear distances
scaling isometrically increase with VL0.33. Deviations
from these exponents indicate changes in structure
other than simple enlargement.
The parenchymal component (Vp) was approximately
75% of lung volume, the non-parenchymal component
(Vnp) occupying the remainder. Both parameters increased
isometrically with lung volume (Vp = 0.741VL1.000.01,

Fig. 2 Transmission electron micrographs of the tissue of the

parabronchial mantle. a, atria; ac, air capillaries; bc, blood
capillaries; i, infundibula; bm, basement membrane; e,
erythrocyte; en, endothelium; ep, epithelium. (a) At 11 days
after hatching infundibula extend from the atria into the
parabronchial mantle. Blood capillaries line the atria and
infundibula. Small air capillaries are apparent. (b) In the
mature pelican lung interstitial tissue (*) is greatly reduced
and air capillaries are surrounded by blood capillaries. (c) The
bloodgas tissue barrier in the lung of the mature pelican is
composed of the thin epithelium of the air capillary separated
from the endothelium of the blood capillary by a fused
basement membrane. Air capillaries are separated by a barrier
of thin epithelial cells sharing a common basement
membrane. Erythrocytes lie in the blood capillary.

R2 = 0.999, Vnp = 0.255VL0.990.04, R2 = 0.99) with no significant difference in slope between P1 and P2 for Vp
(P = 0.13) or for Vnp (P = 0.10).
Within Vnp, the volume of the bronchi (Vbr) increased
significantly more rapidly relative to lung volume in P1
than in P2 (ANCOVA P = 0.003), as did the volume of large
blood vessels (Vlbv) (P = 0.001) (Fig. 4a,b). In P1, the
slopes for Vbr (b = 1.53 0.47) and Vlbv (b = 1.85 0.54)
were significantly greater than 1, indicating that these
variables increased more rapidly than the lung as a
whole. In P2, both Vbr (b = 0.93 0.10) and Vlbv (b =
1.06 0.12) scaled isometrically with lung volume. There
was no difference in slope between the two parameters
in either P1 (P = 0.33) or P2 (P = 0.09). Within Vp, results
for parabronchi and secondary bronchi, which do not
differ structurally, were combined (Maina, 2002). Increase
in the volume of the parabronchial lumen (Vpbl) increased
faster than lung volume in P1 (b = 1.51 0.25) and
slowed in P2 to increase isometrically with lung volume
(b = 0.99 0.07) (Fig. 4c).
The slope for parabronchial mantle volume (Vpm) in
P1 (b = 0.79 0.09) was significantly less than unity,
indicating that it increased more slowly than lung
volume (Fig. 5a). In P2, however, Vpm scaled isometrically
with lung volume (b = 1.02 0.04). There was a significant change in slope at hatching (P < 0.0001). Small
blood vessel volume (Vsbv) increased much more rapidly in relation to lung volume in P1 (b = 2.24 0.41),
but became isometric in P2 (b = 0.95 0.23). The difference in slope for P1 and P2 was significant (P < 0.0001)
Anatomical Society of Great Britain and Ireland 2005

Lung growth in the pelican, S. Runciman et al. 371

Table 1 Age, body mass (Mb; g), lung volume (VL; cm3) and absolute volumes (V; cm3) of components of the lung in the
pelican determined with light microscopy. Yolk-free mass is given for all embryos up to internal pipping (IP) and for hatchlings.
Vp, parenchyma; Vpbl, parabronchial lumen; Vatr, atria; Vpm, parabronchial mantle; Vsbv, small blood vessels;
Vnp, non-parenchyma; Vbr, large airways; Vlbv, large blood vessels; Vct, connective tissue
Age

Mass

VL

Vp

Vpbl

Vatr

Vpm

Vsbv

Vnp

Vbr

Vlbv

Vct

Embryos
24 days

16.24
19.36
21.73
24.68
63.85
49.9
67.11
97.26
88.03
110.19
122.24
123.19
553.1
905.8
1870
1994
3724
4181
5541
6821
8834
7190

0.28
0.44
0.52
0.76
1.62
1.4
1.28
1.72
2.4
2.54
3.36
2.78
20.38
23.46
49.88
49.36
93.92
153.04
210.32
228.063
267.7
316.35

0.211
0.307
0.380
0.574
1.343
0.935
0.873
1.191
1.882
2.014
2.696
2.112
15.704
16.902
38.124
39.393
67.386
103.204
170.929
161.948
209.453
247.393

0.020
0.026
0.093
0.120
0.339
0.175
0.246
0.458
0.572
0.651
0.819
0.587
3.772
2.984
8.964
13.323
26.022
29.339
43.017
46.304
65.629
58.962

0
0
0
0
0.115
0.080
0.045
0.065
0.217
0.171
0.176
0.312
1.417
1.954
3.201
5.463
7.841
6.731
8.262
12.209
8.029
7.422

0.191
0.275
0.280
0.446
0.860
0.665
0.561
0.612
0.976
1.086
1.500
1.106
9.372
10.722
24.679
19.361
31.250
61.439
107.970
86.387
123.577
173.175

0
0.003
0.008
0.007
0.028
0.015
0.022
0.056
0.117
0.106
0.201
0.107
1.143
1.241
1.281
1.246
2.273
5.695
11.680
17.047
12.218
7.834

0.069
0.133
0.140
0.186
0.277
0.465
0.407
0.529
0.518
0.526
0.664
0.668
4.676
6.558
11.756
9.967
26.534
49.836
39.391
66.115
58.247
68.957

0.005
0.013
0.067
0.054
0.138
0.265
0.142
0.351
0.224
0.329
0.277
0.241
2.033
1.909
3.637
4.983
11.549
8.241
11.255
29.717
14.120
23.460

0.004
0.004
0.010
0.021
0.022
0.085
0.091
0.033
0.251
0.105
0.373
0.318
2.440
3.972
7.794
4.351
12.599
32.178
22.509
23.049
25.299
29.147

0.059
0.116
0.063
0.111
0.117
0.115
0.174
0.145
0.043
0.092
0.014
0.109
0.203
0.677
0.325
0.633
2.386
9.418
5.627
13.344
18.827
16.351

Embryos
30 days
Embryos
IP
Hatchlings

11-day
chicks
21-day
chicks
Juveniles

Adult

Table 2 Age, mass (g), volumes (V; cm3) and surface areas (S; cm2) of components of the lung and harmonic mean thickness of
the bloodgas tissue barrier (ht; m) in the pelican determined with transmission electron microscopy. Va, air capillary; Vt, tissue;
Vc, blood capillary; Sa, air capillary; St, bloodgas tissue barrier; Sctot; total capillary
Age

Mass

VL

Va

Vt

Vc

Sa

St

Sctot

ht

Embryos
30 days
Embryos
IP
Hatchlings

63.85
49.9
67.11
97.26
88.03
110.19
123.19
553.1
905.8
1870
1994
3724
4181
5541
6821
8834
7190

1.62
1.4
1.28
1.72
2.4
2.54
2.78
20.38
23.46
49.88
49.36
93.92
153.04
210.32
228.06
267.7
316.35

0.175
0.212
0.195
0.217
0.482
0.342
0.624
4.923
5.076
13.720
10.480
16.147
35.245
60.289
57.319
70.576
113.239

0.638
0.417
0.325
0.359
0.309
0.556
0.403
2.387
2.891
7.441
6.453
9.409
11.784
21.749
21.738
24.909
17.421

0.047
0.036
0.040
0.036
0.184
0.188
0.113
2.062
2.756
3.519
2.426
5.712
14.410
25.932
23.854
28.092
42.532

482.26
348.13
534.80
593.44
1086.32
1050.67
1296.36
11667.07
11672.58
35421.34
29780.82
46180.10
98586.52
181932.28
167762.44
168925.84
401625.65

88.21
52.26
159.76
132.58
571.18
451.82
475.33
5430.25
6293.63
10535.43
13517.90
26514.89
61765.95
114603.51
113445.66
116472.99
271133.12

293.48
75.05
310.45
277.78
835.10
1027.36
1086.26
9568.25
16278.61
26382.59
19126.42
37878.41
75246.91
146664.83
151822.30
155321.56
309441.15

2.88
1.28
1.14
1.244
0.452
0.349
0.553
0.352
0.445
0.439
0.683
0.581
0.466
0.421
0.415
0.450
0.175

11-day
chicks
21-day
chicks
Juveniles

Adult

(Fig. 5b). Atrial volume (Vatr) scaled isometrically with

lung volume (b = 0.94 0.11) (Fig. 5c). As atria were
not present in day 24 embryos, and there was no significant difference in slope for P1 and P2 (P = 0.08), the
data were combined for regression analysis.
Anatomical Society of Great Britain and Ireland 2005

In the parabronchial mantle, there was no difference

in slope for the volume of the air capillaries (Va) between
P1 and P2 (P = 0.22), so the data were combined. Thus,
Va increased faster than lung volume (b = 1.12 0.05)
(Fig. 6a). The data for blood capillary volume (Vc) was

372 Lung growth in the pelican, S. Runciman et al.

Fig. 3 Bi-logarithmic plot of lung volume

(VL) against body mass (Mb) for pelicans
(
) from 24 days of incubation to adult,
turkeys T1 () from 22 days of incubation
to hatchlings and T2 from hatchlings to
adult () and a range of mature birds ().
The data for turkeys are from Timmwood
et al. (1987). Data for the 26 species of
adult birds are from Maina et al. (1989).
Where there was no difference in slope
between the two groups within a species
the data were combined to give a single
slope value. Regression equations: pelicans
(
) VL = 0.02Mb1.07 where Mb is in grams
(R2 = 0.99); (T1) () VL = 0.7 103Mb1.87
(R2 = 0.87); (T2) () VL = 0.04Mb0.91
(R2 = 0.997); adult () VL = 0.02Mb1.01
(R2 = 0.98).

quite variable and the slope not significantly different

from unity in P1 (b = 2.20 1.33) or P2 (b = 1.11 0.11),
but the slopes were significantly different in P1 and P2
(P = 0.03) (Fig. 6b). In P1, tissue volume (Vt) correlated
poorly with change in lung volume (VtP1 = 0.04VL0.081.01,
R 2 = 0.008). In P2, the increase in Vt was slower than
that in lung volume (VtP2 = 0.19VL0.860.08, R2 = 0.98). Air
capillary surface area (Sa) increased rapidly in relation
to lung volume, and there was no significant difference
between the slope for P1 (b = 1.50 0.67) and that for
P2 (b = 1.13 0.07) (Fig. 6c). The equation for the
combined data is Sa = 3.29VL1.160.05 (R2 = 0.99). The
exponent for Sa was significantly greater than 0.67.
The slope for total surface area of blood capillaries
(Sctot) was significantly steeper in P1 (b = 2.68 1.83)
than in P2 (b = 1.12 0.08) (P = 0.005), and both were
significantly higher than 0.67 (Fig. 7a). Increase in surface area of the bloodgas barrier (St) was significantly
more rapid in relation to lung volume in P1 (b = 2.61
1.77) than in P2 (b = 1.22 0.09) (P = 0.012), and both
were significantly higher than 0.67 (Fig. 7b). Changes
in the harmonic mean thickness of the tissue diffusion
barrier (ht) were largely independent of lung volume
(Fig. 7c). The slope for ht was significantly steeper in
P1 (b = 1.83 1.77) than in P2 (b = 0.04 0.12) (P =
0.004).
Diffusing capacity of the blood gas tissue barrier
(DtO2) in relation to lung volume increased more rapidly in P1 (b = 4.44 3.17) than in P2 (b = 1.26 0.19)
(P = 0.003) and the slopes for both stages were significantly greater than 1 (Fig. 8). The relationships between

functional lung parameters and body mass (Mb) for

post-hatching growth are: St = 1.4Mb1.25, ht = 0.40Mb0.02
and DtO2 = 0.0087Mb1.23 (Seymour et al. 2004).

Discussion
This study quantifies the morphological changes occurring during development of the lung in the Australian
pelican from the 24th day of incubation through to
maturity. Comparison of the data from this altricial
species and a precocial species with a different pattern
of locomotion, behaviour and metabolic demands
allows identification of maturational differences and similarities in development and growth of lung components
involved in gas exchange. Comparison of the regression analyses of the developing lung in the pelican
with those for mature birds provides insight into
the developmental requirements of the pulmonary
system for strong flight in one of the largest flying
birds.
Aspects of our work on altricial pelicans are comparable with only one other published investigation of a
developing bird, fortuitously on the similarly sized, but
highly precocial turkey Meleagris gallopavo (Timmwood
et al. 1987). Three phases of pulmonary growth have
been identified in the turkey. During the pre-hatch
phase of tissue proliferation, lung volume grows more
rapidly than body mass, and air and blood components
grow more rapidly than lung volume. In the early
post-hatch period of equilibrated growth, lung volume
increases slowly in comparison with body mass, and
Anatomical Society of Great Britain and Ireland 2005

Lung growth in the pelican, S. Runciman et al. 373

Fig. 4 Bi-logarithmic plots of lung

component volumes against lung volume
(VL) for pelicans P1 () from 24 days of
incubation to hatchlings and P2 (
)
hatchlings to adult, turkeys T1 () from
22 days of incubation to hatchlings and
T2 () from hatchlings to adult and a
range of mature birds (). The data for
turkeys are from Timmwood et al. (1987).
Data for the 26 species of adult birds are
from Maina et al. (1989). Where there
was no difference in slope between the
two groups within a species the data
were combined to give a single slope
value. (a) Large airway volume (Vbr)
against lung volume (VL). Regression
equations: P1 () Vbr = 0.08VL1.53 (R2 =
0.84); P2 (
) Vbr = 0.11VL0.93 (R2 = 0.97);
T () Vbr = 0.06VL0.79 (R2 = 0.99); adult ()
Vbr = 0.02VL1.18 (R2 = 0.94). (b) Large
blood vessel volume (Vlbv) against lung
volume (VL). Regression equations: P1 ()
Vlbv = 0.03VL1.85 (R2 = 0.85); P2 (
)
Vlbv = 0.09VL1.06 (R2 = 0.97); T1 ()
Vlbv = 0.024VL1.75 (R2 = 0.73); T2 ()
Vlbv = 0.05VL1.15 (R2 = 0.99); adult ()
Vlbv = 0.075VL1.04 (R2 = 0.97). (c)
Parabronchial luminal volume (Vpbl)
against lung volume (VL). Regression
equations: P1 () Vpbl = 0.15VL1.51
(R2 = 0.95); P2 (
) Vpbl = 0.22VL0.99
(R2 = 0.99); T1 () Vpbl = 0.39VL1.31
(R2 = 0.998); T2 () Vpbl = 0.41VL0.93
(R2 = 0.99); adults () Vpbl = 0.4VL1.05
(R2 = 0.99).

blood vessels and air capillaries grow more rapidly than

lung volume. Parabronchial and atrial volume growth
is slow relative to lung volume. The late period is characterized by slowing of lung growth relative to body
Anatomical Society of Great Britain and Ireland 2005

mass and rapid development of air capillaries in relation to lung volume. Compared with the large transition at hatching, however, the transition from the
second to the third phase is minor, gradual and difficult

374 Lung growth in the pelican, S. Runciman et al.

Fig. 5 Bi-logarithmic plots of lung

component volumes against lung volume
(VL) for pelicans P1 () from 24 days of
incubation to hatchlings and P2 (
)
hatchlings to adult, turkeys T1 () from
22 days of incubation to hatchlings and
T2 () from hatchlings to adult and a
range of mature birds (). The data for
turkeys are from Timmwood et al. (1987).
Data for the 26 species of adult birds are
from Maina et al. (1989). Where there
was no difference in slope between the
two groups within a species the data
were combined to give a single slope
value. (a) Parabronchial mantle volume
(Vpm) against lung volume (VL).
Regression equations: P1 ()
Vpm = 0.51VL0.79 (R2 = 0.97); P2 (
)
Vpm = 0.41VL1.02 (R2 = 0.996); T1 ()
Vpm = 0.24 VL1.39 (R2 = 0.999); T2 ()
Vpm = 0.27VL1.08 (R2 = 0.996); adults ()
Vpm = 0.47VL0.92 (R2 = 0.99). (b) Small
blood vessel volume (Vsbv) vs. lung
volume (VL). Regression equations: P1 ()
Vsbv = 0.01VL2.24 (R2 = 0.94); P2 (
)
Vsbv = 0.06VL0.95 (R2 = 0.87); T1 ()
Vsbv = 0.04VL0.61 (R2 = 0.93); T2 ()
Vsbv = 0.05VL0.94 (R2 = 0.98). Adult bird
data not available. (c) Atrial volume
(Vatr) against lung volume
(VL). Regression equations: P (
)
Vatr = 0.07VL0.94 (R2 = 0.96); T1 ()
Vatr = 0.09VL0.25 (R2 = 0.99); T2 ()
Vatr = 0.07VL1.06 (R2 = 0.99). Adult bird
data not available.

to discern. For practical reasons we therefore combine

phases two and three in the turkey and compare the
species with two phases: pre- and post-hatch pelicans
(P1, P2) and pre- and post-hatch turkeys (T1, T2). Birds

on the day of hatch are included in both groups for

allometric comparisons.
In the pelican, lung volume increases more rapidly in
relation to body mass whereas it scales isometrically in
Anatomical Society of Great Britain and Ireland 2005

Lung growth in the pelican, S. Runciman et al. 375

Fig. 6 Bi-logarithmic plot of lung

component volumes and surface areas
against lung volume (VL) for pelicans P1
() from 24 days of incubation to
hatchlings and P2 (
) hatchlings to adult,
turkeys T1 () from 22 days of incubation
to hatchlings and T2 () from hatchlings
to adult and a range of mature birds ().
The data for turkeys are from Timmwood
et al. (1987). Data for the 26 species of
adult birds are from Maina et al. (1989).
Where there was no difference in slope
between the two groups within a species
the data were combined to give a single
slope value. As air capillaries have not yet
developed in 24-day embryos, there are
no data at VL < 1 cm3 in (a) and (c). (a) Air
capillary volume (Va) against lung volume
(VL). Regression equations: P (
) Va =
0.14VL1.12 (R2 = 0.99); T1 () Va = 0.09VL2.25
(R2 = 0.98); T2 () Va = 0.13 VL1.13
(R2 = 0.997); adults () Va = 0.25VL0.97
(R2 = 0.99). (b) Blood capillary volume (Vc)
against lung volume (VL). Regression
equations: P1 () Vc = 0.02VL2.20 (R2 =
0.78); P2 (
) Vc = 0.06VL1.11 (R2 = 0.98); T1
() Vc = 0.09VL2.00 (R2 = 0.997); T2 ()
Vc = 0.12 VL1.03 (R2 = 0.995); adults ()
Vc = 0.18VL0.88 (R2 = 0.99). (c) Air capillary
surface area (Sa) against lung volume (VL).
Regression equations: P (
) Sa = 329VL1.16
(R2 = 0.99);T1 () Sa = 239VL2.22
(R2 = 0.99); T2 () Sa = 359VL1.08
(R2 = 0.99); adults () Sa = 1777VL0.86
(R2 = 0.97).

adult birds (Maina et al. 1989) (Fig. 3). By contrast, increase

in lung volume in the turkey occurs at two distinct rates
in relation to mass, a rapid pre-hatch phase and a slower
post-hatch phase. Lung volume is not significantly
Anatomical Society of Great Britain and Ireland 2005

different in relation to mass in the post-hatch pelicans

and the adult birds, but from 11 days after hatching, in
pelicans with a mass of more than 500 g, the ratio VL /
Mb is greater in the pelican than in the turkey (P = 0.0001).

376 Lung growth in the pelican, S. Runciman et al.

Fig. 7 Bi-logarithmic plot of lung

component surface areas and harmonic
mean thickness of the bloodgas barrier
against lung volume (VL) for pelicans P1
() from 24 days of incubation to
hatchlings and P2 (
) hatchlings to adult,
turkeys T1 () from 22 days of incubation
to hatchlings and T2 () from hatchlings
to adult and a range of mature birds ().
The data for turkeys are from Timmwood
et al. (1987). Data for the 26 species of
adult birds are from Maina et al. (1989).
(a) Total blood capillary surface area
(Sctot) against lung volume (VL).
Regression equations: P1 ()
Sctot = 73.8VL2.68 (R2 = 0.74); P2 (
)
Sctot = 336VL1.12 (R2 = 0.99); T1 ()
Sctot = 172VL3.05 (R2 = 0.98); T2 ()
Sctot = 324VL1.05 (R2 = 0.99); adults ()
Sctot = 1965VL0.82 (R2 = 0.98). (b) Blood
gas barrier surface area (St) against lung
volume (VL). Regression equations:
P1 () St = 37.9VL2.61 (R2 = 0.74); P2 (
)
St = 140VL1.22 (R2 = 0.99); Turkey data
not available. Adults () Sa = 1519VL0.84
(R2 = 0.97). (c) Harmonic mean thickness
of the blood gas barrier (ht) against
lung volume (VL). Adult bird indicated
by *. Regression equations: P1 ()
ht = 2.85VL1.83 (R2 = 0.59); P2 (
)
ht = 0.50VL0.04 (R2 = 0.05); Turkey data
not available. Adults () ht = 0.14VL0.07
(R2 = 0.15).

This is in accordance with the allometric study by Maina

et al. (1989), which shows that VL/Mb for mature
domestic fowl (which have a similar pattern of maturation, locomotion and presumably metabolic demands
as turkeys) is well below the line for other wild species.

As described by Duncker (1977), development and

establishment of some of the lung components occurs
largely in the pre-hatch period and is established by the
time of internal pipping. In P1, the significantly positive
allometric relationships between increase in lung
Anatomical Society of Great Britain and Ireland 2005

Lung growth in the pelican, S. Runciman et al. 377

Fig. 8 Bi-logarithmic plot of total

diffusing capacity of the tissue (DtO2)
against lung volume (VL) for pelicans P1
() from 24 days of incubation to
hatchlings and P2 (
) hatchlings to adult
and a range of mature birds (). Data for
the 26 species of adult birds are from
Maina et al. (1989). Regression
equations: P1 () DtO2 = 0.03VL4.44
(R2 = 0.72); P2 (
) DtO2 = 0.70VL1.26
(R2 = 0.95); Turkey data not available.
Adults () DtO2 = 26.3VL0.78 (R2 = 0.91).

volume and the large airways (Fig. 4a), large and small
blood vessels (Figs 4b and 5b) and parabronchi (Fig. 4c)
indicate that the number, orientation and arrangement
of these components are established prior to hatching
in the pelican. After hatching the slope for these
lung components is isometric, indicating proportional
increases.
In the turkey, the large airways appear to be established by the 22nd day of a 28-day incubation period,
and further development is less than isometric (b =
0.79 0.04) in relation to lung volume (Fig. 4a). From
30 days of incubation to maturity in the pelican, large
airways occupy relatively more of the lung than in
the turkey (P = 0.05). In P1, with a lung volume less
than 50 cm3, large airway volume is significantly
larger in relation to lung volume in comparison with
large airway volume in mature birds (P = 0.05). The
points for juvenile and mature pelicans would lie
on the extrapolated regression line for mature birds
(Fig. 4a).
Large blood vessel development is similar to the
development of the airways, with the pattern being
established prior to hatching and increasing proportionately with lung volume after hatching. The slope
for large blood vessels in the pre-hatch turkeys is similar to that in the pelicans, suggesting that the number
and orientation of large blood vessels in the turkey
may occur later in the incubation period than large airway development (Fig. 4b). Large blood vessel volume
is significantly smaller in relation to lung volume in the
Anatomical Society of Great Britain and Ireland 2005

pre-hatch pelicans in comparison with large blood vessel volume in mature birds (P = 0.05). In the post-hatch
period, the proportion of the lung occupied by large
blood vessels is similar in pelicans and turkeys and
matched that of the adult bird group.
New parabronchi continue to appear during the
10 days before hatching in the pelican, but the data
from the turkey suggest that the number of parabronchi is established by 6 days prior to hatching (Fig. 4c).
Parabronchial volume in relation to lung volume is
significantly lower in pelicans at all ages than in adult
birds and in turkeys (P = 0.05).
In pelicans, establishment of the parabronchi within
the parenchyma in the pre-hatch period occurs at the
expense of the parabronchial mantle tissue, its volume
increasing relatively slowly in relation to lung volume
in the pre-hatch period and isometrically with lung
volume in the post-hatch period (Fig. 5a). Parabronchial
mantle volume makes up a significantly greater proportion of the lung in pelicans than in the turkeys at
all ages (P = 0.05). In pelicans older than 11 days, with
lung volumes larger than 24 cm3, the proportion of
parabronchial mantle volume to lung volume is larger
than in the adult bird group.
Small blood vessel volume increases more rapidly in
the pre-hatch pelicans than in the pre-hatch turkeys,
but from the time of hatching onwards, small blood
vessel volume in relation to lung volume is similar in
the two species (P = 0.05). Comparison with adult birds
is not possible as data are not available (Fig. 5b).

378 Lung growth in the pelican, S. Runciman et al.

Atria develop between 24 and 30 days of incubation

in the pelican, and they are apparent at 22 days in the
turkey. At 30 days in the pelican, atrial volume matches
that of the turkeys on hatch day and development proceeds at a similar rate in the two species (Fig. 5c). Our
data contrast with Dunckers (1977) observation that
altricial birds have shallower atria and his prediction
that atria in strong flying birds would be relatively
small so as to reduce dead space (Duncker, 1972).
Capillaries occur underlying the epithelium in the interatrial septa, at the bases of the atria and the infundibula, in pre-hatching pelicans, providing sites for gas
exchange. As atrial septa elongate with maturity, capillaries continue to line infundibula but not the interatrial septa. There is no information about capillaries in
the interatrial septa of the turkey lung or of mature
bird lungs, so further comparison is not possible. However, atrial volume in relation to lung volume in the
older pelicans is similar to that in turkeys. As already
mentioned, we are not able to compare atrial volumes
so cannot say whether pelican atria are shallower than
those of other mature birds.
Putative air capillaries are first apparent in the 30day embryo pelicans about 4 days before hatching,
whereas in the turkey they appear at 22 days of incubation, 6 days prior to hatching. Air capillary volume in
relation to lung volume increases rapidly in pre-hatch
turkeys, but in pelicans development occurs at the
same rate in the pre- and post-hatch birds and is similar
to that in turkeys after hatching (Fig. 6a). The relatively
high value for the pre-hatch pelicans most likely results
from the difficulty in identifying what constitutes an
air capillary, particularly at the TEM level. Given the
restricted field, it is not always apparent whether a
small-diameter air capillary is a true air capillary or a
developing infundibulum. If blood capillaries are
found subjacent to the epithelium lining the airspace,
it is counted as air capillary because gas exchange can
occur in this air space. Accordingly, data from the 30day incubation pelicans are included in the regression
analysis. This approach in measuring Va may also account
for the lack of a significant difference in slope in the
pre-hatch and post-hatch pelican groups. Air capillary
volume relative to lung volume in the adult birds significantly exceeds that in pelicans until about 11 days
after hatching.
Blood capillary volume increases greatly in relation
to lung volume in both pelicans and turkeys during the
pre-hatch phase, but blood capillary volume relative to

lung volume is significantly lower in the pelican lungs

(Fig. 6b). It is also significantly lower in pelicans than in
mature birds (P = 0.05). The high values for capillary
volume in the turkey, however, may result from difficulty in distinguishing between capillaries and small
blood vessels at a relatively low magnification. After
hatching, in both pelicans and turkeys, blood capillary
growth slows to develop isometrically but relative
volume remains higher in turkeys than in pelicans. Blood
capillary volume relative to lung volume is significantly
less in pelicans with lung volumes of less than 50 cm3
than in mature birds (P = 0.05). The increase in air and
blood capillaries occurs at the expense of tissue volume
in both pelicans and turkeys.
Air capillary surface area in relation to lung volume
increases more rapidly prior to hatching in turkeys,
whereas pre- and post-hatch development is similar in
pelicans. Post-hatch increase, however, is still significantly
higher than isometry in both pelicans and turkeys
(Fig. 6c). In any structure that increases in size, but does
not change shape, the relationship between surface
area (S) and volume (V) is S V 0.67. As the lungs increased
in volume therefore there is a proliferation of surface
area, rather than simple magnification.
The same constraints that applied to measurement
of volume apply to measurement of air capillary surface area and are likely to account for surface areas
in the pre-hatch pelicans being similar to that in the
hatch-day turkeys. Air capillary surface area in pelicans
with a lung volume of less than 90 cm3 is significantly
lower, relative to lung volume, than in mature birds
(P = 0.05).
Total blood capillary surface area in relation to lung
volume in the pre-hatch pelicans and turkeys increases
at a very rapid rate during the last part of incubation
(Fig. 7a). After hatching, total blood capillary surface
area in pelicans exceeds that of turkeys and this
relationship persists through to adulthood (P = 0.05).
In comparison with mature birds total blood capillary
surface area is significantly less in pelicans with lung
volumes less than 90 cm3 and matches that of mature
birds in the pre-volant juveniles and adult (P = 0.05).
The rapid increase in surface area and volume of the
air capillaries and surface area of blood capillaries in
the pre-hatch period indicates a change in shape and
an increase in complexity. These observations are
consistent with the development of numerous smalldiameter capillaries rather than elongation and widening of existing capillaries up to maturity.
Anatomical Society of Great Britain and Ireland 2005

Lung growth in the pelican, S. Runciman et al. 379

The surface area of the bloodgas tissue barrier in

pelicans is significantly lower than in adult birds only
when lung volume is less than 150 cm3, i.e. in juvenile
pelicans that are not yet volant (Fig. 7b). Comparison
with turkeys is not possible, as data for them are lacking.
Harmonic mean thickness of the presumptive airblood
tissue barrier greatly decreases during embryonic life in
pelicans (Fig. 7c). After hatching, and until pre-volant
juveniles reach adult body size, it remains fairly constant,
but decreases further by adulthood. The value for the
adult pelican is adjacent to the extrapolated regression
line for mature birds. With this exception, the barrier is
significantly thicker in pelicans than in adult birds. Data
for turkeys are not available.
Because of rapidly increasing surface area and decreasing thickness of the presumptive airgas barrier in
embryonic pelicans, the calculated oxygen diffusing
capacity increases greatly in relation to lung volume
(Fig. 8). After hatching, its increase is less because of
a relatively slower increase in exchange surface area
(Fig. 7b) and a relatively constant thickness (Fig. 7c).
Diffusing capacity is always less in pelicans than in adult
birds until lung volume reached 300 cm3 (P = 0.05).

Conclusions
This study supports previous observations on the accelerated development of lung components in the period
prior to hatching (Duncker, 1972, 1977; Timmwood
et al. 1987). This rapid development coincides with the
transition between chorioallantoic and pulmonary gas
exchange. After oxygen uptake via the chorioallantois
plateaus in both precocial species and altricial pelicans
(Vleck & Bucher, 1998; Pearson et al. 2002), the embryo
internally pips into the air cell and begins to ventilate
the lungs. Chorioallantoic gas exchange diminishes and
pulmonary gas exchange increases during the period
between internal pipping and hatching (Visschedijk,
1968). In precocial turkeys, there is an initial rapid
development of parameters required for respiration
followed by slower development after hatching. In
altricial pelicans, the pattern of development of lung
components is similar to turkeys until hatching, but they
continue to develop rapidly after hatching, many reaching
values that exceed those of turkeys and match or exceed
those in adult birds in general. These developmental
differences are consistent with expected differences
between altricial and precocial species and reflect differences in metabolic demands for locomotion in adults.
Anatomical Society of Great Britain and Ireland 2005

Acknowledgements
This work was supported by the Australian Research
Council. The experiments were performed with the
approval of the Animal Ethics Committee of the
University of Adelaide (S-49-1999A).

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Anatomical Society of Great Britain and Ireland 2005