Journal of Anatomy - 2020 - Bakkeren - A Morphometric Analysis of The Lungs of High Altitude Ducks and Geese

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Received: 15 November 2019 Revised: 12 February 2020 Accepted: 18 February 2020
DOI: 10.1111/joa.13180
ORIG INAL PAPER
A morphometric analysis of the lungs of high-altitude ducks

and geese
Ciska Bakkeren1 | Emily Smith1 | Julia M. York2 | Beverly Chua1 |

Kevin G. McCracken3,4,5,6 | William K. Milsom1
1
Department of Zoology, University of
British Columbia, Vancouver, BC, Canada Abstract
2
Department of Integrative Biology, We examined the morphology of the lungs of five species of high-altitude resident
University of Texas at Austin, Austin, TX,
ducks from Lake Titicaca in the Peruvian Andes (yellow-billed pintail [Anas georgica],
USA
3
Department of Biology, Rosenstiel School
cinnamon teal [Anas cyanoptera orinomus], puna teal [Anas puna], speckled teal [Anas
of Marine and Atmospheric Sciences, flavirostris oxyptera], and ruddy duck [Oxyura jamaicensis ferruginea]) and compared
University of Miami, Coral Gables, FL, USA
4
them with those of the high-altitude migratory bar-headed goose (Anser indicus) and
Department of Marine Biology and
Ecology, Rosenstiel School of Marine and the low-altitude migratory barnacle goose (Branta leucopsis). We then determined
Atmospheric Sciences, University of Miami, the relationship between mass-specific lung volume, the volume densities of the
Coral Gables, FL, USA
5 component parts of the lung, and previously reported hypoxia-induced increases in
Human Genetics and Genomics, University
of Miami Miller School of Medicine, pulmonary O2 extraction. We found that the mass-specific lung volumes and the
University of Miami, Coral Gables, FL, USA
6
mass-specific volume of the exchange tissue were larger in the lungs of high-altitude
University of Alaska Museum and Institute
of Arctic Biology, University of Alaska resident birds. The bar-headed goose had a mass-specific lung volume that fell be-
Fairbanks, Fairbanks, AK, USA tween those of the low-altitude species and the high-altitude residents, but a mass-
Correspondence specific volume of exchange tissue that was not significantly different than that of
Ciska Bakkeren, Department of Zoology, the high-altitude residents. The data suggest that the mass-specific volume of the
University of British Columbia, Vancouver,
BC, Canada V6T 1Z4. lung may increase with evolutionary time spent at altitude. We found an inverse re-
Email: c.bakkeren@shaw.ca lationship between the percentage increase in pulmonary O2 extraction and the per-
Funding information centage increase in ventilation across species that was independent of the volume
NSERC of Canada; National Science density of the exchange tissue, at least for the resident Andean birds.
Foundation, Grant/Award Number:
IOS-0949439; University of Miami
KEYWORDS
altitude, birds, hypoxia, lungs, morphometry, pulmonary exchange tissue, pulmonary O2

extraction
1 | I NTRO D U C TI O N was hypothesized that transient high-altitude performance favoured

the evolution of enhanced convective O2 uptake in hypoxia, whereas
In a previous study, it was reported that some high-altitude resident lifelong high-altitude residency favoured the evolution of morpho-
waterfowl, such as the Andean goose (Chloephaga melanoptera), have logical enhancements to the lungs that increase lung-O2 diffusion
evolved fundamentally different mechanisms for maintaining oxy- capacity (Lague et al., 2017). In a subsequent study, it was shown
gen (O2) supply in hypoxic (low O2) environments at altitude com- that the Andean goose does indeed possess pulmonary structural
pared with the bar-headed goose (Anser indicus). The bar-headed specializations that produce a mass-specific total pulmonary O2
goose, which migrates at high altitude to cross the Himalayas, re- diffusing capacity of the lung that is among the highest values re-
sponds to hypoxia by increasing ventilation and heart rate, whereas ported in birds (Maina et al., 2017). More recently, a study under-
the Andean goose, which resides year-round at altitude, increases taken on multiple species residing at the same high elevations in
lung O2 extraction and cardiac stroke volume (Lague et al., 2017). It the Andes of Peru found that distinct physiological strategies for
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188 © 2020 Anatomical Society wileyonlinelibrary.com/journal/joa Journal of Anatomy. 2020;237:188–196.
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14697580, 2020, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/joa.13180, Wiley Online Library on [11/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
BAKKEREN et al. 189
coping with hypoxia exist across different high-altitude lineages of the Animal Care Committee at the University of Miami (17-107) and
ducks (Ivy et al., 2019). In this study, six populations of ducks that University of British Columbia (A16-0019) in accordance with the
independently colonized the Peruvian Andes were compared with Canadian Council on Animal Care.
six closely related low-altitude populations or species. Individuals
from all populations responded to hypoxia with large increases in
total ventilation combined with significant increases in pulmonary 2.1 | Fixation of the lungs
O2 extraction, regardless of whether they were taken from high- or
low-altitude populations. Two species, the yellow-billed pintail (Anas The birds were weighed and then killed by intravenous injection of
georgica) and the torrent duck (Merganetta armata), had significantly propofol into the tibiotarsal vein (>20 mg/kg). With the body in a
greater increases in total ventilation on exposure to severe hypoxia supine position, the lungs and the air sacs were fixed by intratra-
compared with their low-altitude counterparts. Although there was a cheal instillation with 2% glutaraldehyde buffered with either so-
trend for all high-altitude birds to increase pulmonary O2 extraction dium cacodylate or phosphate (osmolarity 350 mOsm and pH 7.4)
more than their low-altitude counterparts, this was significant only at a pressure head of 3,000 Pa (1 cm H2O = 100 Pa). The top of the
for the yellow-billed pintail (Ivy et al., 2019). funnel was held 30 cm above the sternum of the supine bird. When
Air entering the bird lung flows from the primary bronchus into it stopped flowing by gravity, the body wall was gently massaged
multiple secondary bronchi that give rise to the parabronchi. These repeatedly to expel the air in the lung and the air sacs and allow
parabronchi give rise to the atria and infundibula at the entrance better penetration of the fixative. The trachea was ligated and the
to the air capillaries. These air capillaries are closely connected to fixative left in the respiratory system for approximately 4 hr at room
blood capillaries and are the site of gas exchange (Brown et al., 1997). temperature. After 4 hr, the lungs were removed, immersed in fixa-
For the present study we obtained the lungs from five of the tive, and stored at 4°C for 48–72 hr. They were then stored in buffer
same species of high-altitude ducks studied previously by Ivy et al. without glutaraldehyde at 4°C until sampling.
(2019). We also obtained the lungs of the high-altitude migratory
bar-headed goose as well as the low-altitude migratory barnacle
goose. We examined the morphology of these lungs to determine 2.2 | Determination of the lung volume (VL)
the relationship between previously reported hypoxia-induced in-
creases in pulmonary O2 extraction and the mass-specific lung vol- The extrapulmonary primary bronchus was trimmed close to the
umes, and the volume densities of the component parts of the lung hilum, and all adhering fat and connective tissue were removed.
(primary bronchus, secondary bronchus including parabronchi, atria Volume of the fixed lung (VL) was then determined by the weight
and infundibula, blood vessels larger than capillaries and exchange displacement method of Scherle (1970). Due to the narrowing of the
tissue). We hypothesized that the morphological features of the lungs at the sulci, the volume may be a slight underestimate; how-
high-altitude resident species would be more similar to the Andean ever, our estimates are comparable to those previously reported by
goose than other low-altitude species. We also hypothesized that Maina et al. (2017).
there would be a positive correlation between the mass-specific vol-
umes of exchange tissue and blood vessels in the high-altitude resi-
dent species and their reported values for pulmonary O2 extraction, 2.3 | Sampling and analysis of the structural
and an inverse relationship with the magnitude of their ventilatory components of the lung
responses.
Details on lung sampling, tissue processing for microscopy, and mor-
phometric analyses are outlined in Maina (2002) and are described
2 | M ATE R I A L S A N D M E TH O DS briefly below.
The left lung of each bird was cut into five slices along the
Five species of ducks were captured at high altitude (3,812 m) at the costal sulci and the slices in turn cut into halves dorsal to the pri-
Lake Titicaca National Reserve (near Puno, Peru): yellow-billed pin- mary bronchus. The 10 half-slices were processed and embedded
tails (A. georgica; .53 ± .02 kg, n = 3) cinnamon teal (Anas cyanoptera in paraffin wax with the cranial face of the lung facing anteriorly.
orinomus; .41 ± .10 kg, n = 3), puna teal (Anas puna; .41 ± .05 kg, n = 3), Sections were cut at 8 µm thickness and stained with haematox-
speckled teal (Anas flavirostris oxyptera; .31 ± .01, n = 2), and Andean ylin and eosin. The first five suitable slices off each lung section
ruddy ducks (Oxyura jamaicensis ferruginea; .63 ± .05 kg, n = 3). Bar- were used for analysis (Maina, 2002). Slices were not taken ran-
headed geese (A. indicus; 2.8 ± .14 kg, n = 3) and barnacle geese domly and a vertical section (VUR) method was used. Images
(Branta leucopsis; 2.4 ± .16 kg, n = 3) were obtained from the Sylvan of the slides were taken field-by-field using a Zeiss Axioplan
Heights Bird Park, NC, USA. Waterfowl from Lake Titicaca were col- Fluorescent Microscope. The images were analysed using Image J
lected in accordance with permits issued by the Servicio Nacional de software. The volume densities of the lumina of the intrapulmo-
Áreas Naturales Protegidas (001-2017-SERNANP-DGANP-RNT/J). nary primary bronchus, the secondary bronchi and parabronchi
All procedures were conducted according to guidelines approved by (including the atria and infundibulae) (Pb), the exchange tissue
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190 BAKKEREN et al.
F I G U R E 1 Sample haematoxylin and

eosin-stained section of a bird lung with
a 192-point grid lattice superimposed.
Secondary bronchi and parabraonchi,
blood vessels larger than capillaries, and
exchange tissue are indicated. Scale bar:
100 µm
(air and blood capillaries), and the blood vessels larger than cap- than those of all birds from this study (F(7,10) = 51.9, p < .0099], includ-
illaries were determined field-by-field by point-counting using a ing the bar-headed goose by more than a factor of two.
192-point grid lattice at a final magnification of ×100 (Figure 1). In Figure 3, an example of a low-power histological micrograph
The volume densities were calculated by averaging the percentage of the lung from each species is shown illustrating the parabronchi
component of each slice. The absolute volumes of the structural leading into the exchange tissue. Intra-parabronchial septa can be
parameters were calculated by multiplying the V L with the per- seen in some, but not all sections. This was true for the lungs of all
centage volume density. species.
Standard errors were calculated to determine consistency within
species and an ANOVA with a Tukey–Kramer post hoc test was per-
formed in GraphPad Prism and was used to test for statistically sig-
nificant differences between species.
In Figures 2, 4, and 5, BG is low-altitude, BHG is high-altitude
migratory, and all other species are ducks that reside at high altitude.
3 | R E S U LT S
The mean body mass and lung volumes (VL) of all species are given in
Table 1 and the mass-specific lung volumes are illustrated in Figure 2.
In absolute terms, VL was largest for the ruddy duck and smallest for
the speckled teal among these five species (Table 1). In proportion
to bodyweight, the lungs of the barnacle goose were significantly
smaller than those of all the high-altitude species (F(7,10) = 51.9, p <
.0137) except the bar-headed goose (F(7,10) = 51.9, p = .0534). The
bar-headed goose lungs, in turn, were significantly smaller than F I G U R E 2 Mass-specific lung volumes (cm3 kg–1) of the
those of the yellow-billed pintail (F(7,10) = 51.9, p = .0063) and the species in this study. Barnacle goose, bar-headed goose, yellow-
speckled teal (F(7,10) = 51.9, p = .0068). For the Peruvian ducks from billed pintail, cinnamon teal, ruddy duck, puna teal, speckled teal,
this study the only significant difference was between the ruddy and Andean goose. Values for the Andean goose taken from Maina
et al. (2017) are presented for comparison. Error bars represent
duck and the speckled teal (F(7,10) = 51.9, p = .0431), with the speck-
standard error. * Indicates a significant difference between the
led teal having the largest mass-specific VL and the ruddy duck the
groups indicated by the bar, † indicates a significant difference
smallest (Figure 2). Relative to body mass, the lungs of the Andean with all but the species indicated by the bar and ns, ‡ indicates a
goose (values taken from Maina et al., 2017) were significantly larger significant difference with all other species
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BAKKEREN et al. 191
TA B L E 1 Body mass (BM), absolute volume of the lung (VL), intrapulmonary primary bronchi (IPB), secondary bronchi and parabronchi
(Pb), blood vessels larger than capillaries (BV) and exchange tissue (ET). Values are given as ± standard deviation
Species n BM (kg) VL (cm3) IPB (cm3) Pb (cm3) BV (cm3) ET (cm3)

a
Barnacle goose 3 2.38 ± 0.16 26.0 ± 3.5 4.4 ± 3.2 6.0 ± 4.5 15.6 ± 3.6
Yellow-billed pintail 3 0.53 ± 0.02 13.1 ± 0.1 0.5 ± 0.2 4.0 ± 1.0 1.4 ± 0.2 7.3 ± 0.7
Cinnamon teal 3 0.41 ± 0.10 9.8 ± 0.1 0.3 ± 0.1 2.5 ± 0.5 0.9 ± 0.1 6.1 ± 0.5
Ruddy duck 3 0.63 ± 0.05 13.3 ± 0.1 0.6 ± 0.5 3.5 ± 0.8 1.3 ± 0.3 7.9 ± 1.5
Puna teal 3 0.41 ± 0.05 11.2 ± 0.1 0.5 ± 0.1 3.6 ± 0.5 1.0 ± 0.2 6.1 ± 1.2
Speckled teal 2 0.31 ± 0.01 9.5 ± 0.1 0.3 ± 0.1 2.6 ± 0.1 0.8 ± 0.2 5.7 ± 0.3
a
Andean goose 3 2.67 ± 0.07 112.6 ± 5.4 32.4 ± 6.5 10.7 ± 3.3 69.5 ± 10.2
a
Bar-headed goose 3 2.77 ± 0.14 46.9 ± 3.2 4.5 ± 2.9 8.8 ± 8.5 33.6 ± 8.9
a
Species for which the volume of the IPB was not measured, as the IPB was removed before sampling.
The volumes of the main structural components of the lungs 4 | D I S CU S S I O N

are given in Table 1, and the mass-specific volumes of the structural
components are illustrated in Figure 4. There were no differences The high-altitude speckled teal and puna teal diverged from their
among species in the mass-specific volumes of intrapulmonary low-altitude ancestors approximately 1 million years ago or more,
primary bronchi (F(4,9) = .3397, p > .7895) and blood vessels larger as did the Andean goose (McCracken et al., 2009). The other
than capillaries (F(7,14) = .4744, p > .7895). The mass-specific volume three species have only been established at altitude for multiples
occupied by secondary bronchi and parabronchi was significantly of tens of thousands of years, as estimated by population diver-
smaller in barnacle and bar-headed geese than in the Peruvian spe- gence times calculated from genetic data (McCracken et al., 2009).
cies (F(7,15) = 21.51, p < .0341) but there were no significant differ- Although not significant, the trends in the data from this study
ences among the five species of high-altitude ducks from this study suggest that as time since colonization of high-altitude increases,
(F(7,15) = 21.51, p > .0509); however, the mass-specific volume occu- so does mass-specific lung, secondary bronchi and parabronchi,
pied by secondary bronchi and parabronchi was larger in the Andean and exchange tissue volume. The Andean goose, which likely has
geese than in all other species (F(7,15) = 21.51, p < .0109) except the been established at high-altitude the longest, has the largest lungs
puna teal (F(7,15) = 21.51, p = .0945) and speckled teal (F(7,15) = 21.51, and highest mass-specific exchange tissue volume (Maina et al.,
p = .1012). The mass-specific volume of the exchange tissue was 2017), whereas the bar-headed goose, which is not a resident but
significantly smaller in the barnacle geese than in all other species is transitory at high altitude, has much smaller lungs and a reduced
(F(7,15) = 17.33, p < .0079) except the bar-headed geese (F(7,15) = 17.33, mass-specific volume of exchange tissue compared with the per-
p = .1271) and the ruddy duck (F(7,15) = 17.33, p = .0825), whereas centage of exchange tissue.
that of the Andean goose was greater than in all other species The lungs of the low-altitude barnacle goose were significantly
(F(7,15) = 17.33, p < .0352). smaller than those of all the high-altitude species except the bar-
These measurements expressed as volume densities (percent- headed goose. The bar-headed goose lungs, in turn, were significantly
age of the lung volume occupied by each component) are listed in smaller than those of the yellow-billed pintail and the speckled teal.
Table 2 and illustrated in Figure 5. When expressed this way, the For the Peruvian ducks from this study, the speckled teal had rela-
volume density of blood vessels larger than capillaries was signifi- tively larger lungs than the ruddy duck, and the lungs of the Andean
cantly greater in the bar-headed geese (F(7,15) = 10.78, p < .0302) and goose (values taken from Maina et al., 2017) were significantly larger
barnacle geese (F(7,15) = 10.78, p < .0014) than in all other species, than those of all other birds in this study. Figure 7 compares the lung
whereas the volume density of the secondary bronchi and parabron- volumes of these birds with those of other avian species for which
chi was smaller in the bar-headed geese than in all other species data are available (Maina et al., 2017; Table 3) and demonstrates that
(F(7,15) = 7.438, p < .0264). Notably, the volume density of the ex- the values measured in the present study are consistent with trends
change tissue was similar across all species. seen more broadly.
The volume densities of the different structural components did Table 3 extends this comparison to a variety of other species.
not differ significantly progressing from the first to the fifth slice cut The values we obtained for the low-altitude barnacle goose in the
along the costal sulci of the lungs (F(4,10) = .1190, p > .1449). There present study compare well to those of other low-altitude species
was a trend for the volume density of the blood vessels to decrease such as the greylag goose, the mallard duck, and species from the
and of the exchange tissue to increase from anterior to posterior, but orders Charadriiformes (shorebirds) and Passeriformes (perching
these trends were very modest and not significant (F(4,10) = .1190, birds). As previously reported (Maina et al., 2017), the Andean goose
p > .1449). These measurements were only taken for the five spe- continues to stand out with an exceptional mass-specific volume of
cies from Lake Titicaca and given that there were no differences be- exchange tissue, whereas the five species of Andean ducks in the
tween species, are averaged together and shown in Figure 6. present study have higher mass-specific volumes of exchange tissue
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192 BAKKEREN et al.
F I G U R E 3 Sample haematoxylin and

eosin-stained section from each species
in this study. (a) yellow-billed pintail, (b)
cinnamon teal, (c) ruddy duck, (d) puna
teal, (e) speckled teal, (f) barnacle goose,
(g) bar-headed goose. Scale bars: 100 µm
except for the bar-headed goose, which
is 50 µm
than the low-altitude species or transient high-altitude migrant. The remain in the lung for longer and more O2 to be extracted per breath
higher mass-specific lung volumes in the resident Peruvian ducks (Maina et al., 2017).
may reflect the reduced muscle mass of these short-distance fliers The ruddy duck, which had the smallest lung volume, is the only
compared with longer distance migratory birds. diving species among these ducks. The vital capacity of the ruddy
As previously mentioned, the Andean goose responds to hypoxia duck, reflecting the volume of the air sacs as well as the lungs, is also
with small increases in ventilation and large increases in oxygen the smallest of these species (York et al., 2017). The lung morphol-
extraction, whereas the bar-headed goose responds with large in- ogy of this species may not be optimized for gas exchange, but rather
creases in ventilation but only extracts half as much O2. It is possible in order to reduce buoyancy and to prevent the structural collapse of
that the entire adaptive features of the bar-headed goose can be the lung while diving (Kooyman and Ponganis, 2002).
explained by the fact that it is exercising at altitude, in which case the The morphological components of the lung, particularly the ex-
respiratory frequency may be habitually and ergonomically coupled change tissue, determine the O2 diffusion capability of the respira-
to wing beat (Scott et al., 2015). The Andean goose, the high-altitude tory structure. For the most part, the mass-specific volumes of the
resident, maintains a low ventilation rate, allowing the inspired air to different components of the lung in the different species reflect the
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BAKKEREN et al. 193
mass-specific differences in total lung volume (compare Figures 2 Large standard deviations in the volume densities of the var-
and 3). ious lung components reflect the large variation in the structural
When expressed as volume densities (the percentage of the lung composition of the lung between individuals within each species.
occupied by each component) the volume density of the exchange Keeping this in mind, in Figure 8 we compare the volume densi-
tissue is relatively uniform across all species. The exchange tissue ties of birds from different habitats (low and high altitude) and
is composed of the air and blood capillaries. Also of note is the re- different locomotor behaviours (flightless, residents, migratory
duction of the volume of the lung occupied by secondary bronchi gliders, and migratory flappers). Again, there is large variability
and parabronchi, and the increase in the volume density of larger within groups, particularly among the low-altitude birds. The
blood vessels in the low-altitude barnacle goose as well as in the bar- large variability within the groups may reflect the phylogenetic
headed goose. The significance of this is not clear. history of the birds, as many of these species have been sepa-
rated by millions of years of independent evolution (Prum et al.,
2015). There appears to be a trend for the percentage of the lung
occupied by blood vessels to increase in the high-altitude spe-
cies (resident and migratory) but two notable exceptions are the
flightless emu and the barnacle goose from the present study.
The percentage of the lung occupied by exchange tissue is rela-
tively large in the high-altitude species but is not unique. Several
of the low-altitude species, including the barnacle goose, have
similar values for the percentage of the lung occupied by ex-
change tissue, as does the flightless ostrich. These data suggest
that although life at altitude appears to influence lung structure,
many other factors are also at play in determining lung tissue
composition. Of note in this regard, the flightless birds are com-
prised of the ostrich (Struthio camelus) and the emu (Dromaius
novaehollandiae), both of which have high O2 diffusion capability;
however, they have achieved this in different ways. The ostrich
has a very high-volume density of exchange tissue, whereas the
emu has a very high-volume density of blood vessels. Thus, both
increased perfusion and blood gas surface area can increase O2
diffusion capacity.
It was previously hypothesized that transient high-altitude
performance favoured the evolution of enhanced convective O2
F I G U R E 4 Mass-specific volumes (cm3 kg–1) of the different uptake in hypoxia, whereas lifelong high-altitude residency fa-
components of the lung for each species. Barnacle goose, bar- voured the evolution of structural enhancements to the lungs that
headed goose, yellow-billed pintail, cinnamon teal, ruddy duck,
increase lung diffusion capacity (Lague et al., 2017; Maina et al.,
puna teal, speckled teal, and Andean goose. Values for the Andean
goose taken from Maina et al. (2017) are presented for comparison. 2017). It was subsequently shown that the five species of Andean
Error bars represent standard error. † indicates a significant ducks used in the present study responded to hypoxia with large
difference with all but the species indicated by the bar and ns, increases in total ventilation combined with significant increases
‡ indicates a significant difference with all other species in pulmonary O2 extraction. There was a trend for these species to
TA B L E 2 Volume densities of
Species n IPB (%) Pb (%) BV (%) ET (%)
intrapulmonary primary bronchi (IPB),
a
secondary bronchi and parabronchi (Pb), Barnacle goose 3 17.0 ± 2.30 23.2 ± 3.45 59.8 ± 2.65
blood vessels larger than capillaries (BV), Yellow-billed pintail 3 3.73 ± 1.89 30.53 ± 8.00 10.34 ± 1.80 55.40 ± 5.12
and exchange tissue (ET). Values are given
Cinnamon teal 3 3.07 ± 1.09 25.80 ± 4.80 8.82 ± 0.96 62.31 ± 4.66
as ± standard deviation
Ruddy duck 3 4.74 ± 3.63 26.41 ± 6.09 9.43 ± 2.00 59.39 ± 11.58
Puna teal 3 4.16 ± 0.59 32.12 ± 4.73 8.87 ± 1.64 54.85 ± 6.69
Speckled teal 2 2.92 ± 0.57 27.89 ± 0.05 8.79 ± 2.06 60.4 ± 2.70
a
Andean goose 3 28.8 ± 4.45 9.5 ± 1.43 61.7 ± 7.39
a
Bar-headed goose 3 9.60 ± 1.69 18.8 ± 6.05 71.6 ± 6.36
a
Species for which the volume of the IPB was not measured, as the IPB was removed before
sampling.
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194 BAKKEREN et al.
F I G U R E 7 Comparison of the bird lung volumes in the present

study (circles in red) with those of the population of birds for which
similar data are available (circles in cyan, taken from Maina et al.,
2017: table S8)
TA B L E 3 Mass-specific volume (cm3/kg) of intrapulmonary

primary bronchi (IPB), secondary bronchi and parabronchi (Pb),
large blood vessels (BV), and exchange tissue (ET) for various high-
F I G U R E 5 Volume densities (% of total volume) occupied by
and low-altitude species
the different components of the lung for each species. Barnacle
goose, bar-headed goose, yellow-billed pintail, cinnamon teal, IPB Pb BV ET
ruddy duck, puna teal, speckled teal, and Andean goose. Values b
Andean goose 1.27 10.96 4.04 26.22
for the Andean goose taken from Maina et al. (2017) are presented
for comparison. Error bars represent standard error. * indicates a Speckled teal 0.88 8.43 2.66 18.26
significant difference between the groups indicated by the bar, and Puna teal 1.14 8.78 2.42 14.99
‡ indicates a significant difference with all other species
Cinnamon teal 0.73 6.14 2.10 14.84
Yellow-billed pintail 0.92 7.52 2.55 13.64
Ruddy duck 1.01 5.60 2.00 12.60
Bar-headed goose – 1.63 3.18 12.13
Passeriformesa 0.50 9.19 1.84 12.41
Mallard ducka 0.70 14.85 1.98 11.95
a
Greylag goose 0.43 12.66 1.72 10.02
Charadriiformesa 0.79 16.62 2.74 10.01
Barnacle goose – 1.86 2.54 6.54
a
Maina (2002).
b
Maina et al. (2017).
F I G U R E 6 Mean volume densities of the secondary bronchi,

to be an inverse relationship between the percentage increase in
primary bronchi, blood vessels larger than capillaries and exchange
tissue for sections 1–5 of each lung of each of the five Andean duck pulmonary O2 extraction and the percentage increase in ventila-
species averaged together. The insert is a schematic of the lung tion that are independent of the volume density of the exchange
showing the sulci where the lung interdigitates with the ribs and tissue for the Andean birds. This could reflect differences in the
where the cuts were made to obtain the five sections. Error bars morphometrics of the exchange tissue (barrier thickness, pulmo-
represent standard error
nary respiratory surface area of the blood gas barrier or capillary
density) or physiological differences in perfusion of the lungs. This
increase pulmonary O2 extraction more than related low-altitude remains to be determined.
populations or species do (Ivy et al., 2019). In Figure 9 we compare
the volume density of exchange tissue with the increase in pulmo-
nary O2 extraction vs. the increase in ventilation in various species 5 | CO N C LU S I O N S
of birds breathing a gas mixture containing only 5% O2 . While we
are unable to do statistics on these data, as they were single values Our data indicate that the mass-specific lung volumes and the
derived from mean data from different individuals, there appears mass-specific volume of the exchange tissue are characteristically
|
BAKKEREN et al. 195
F I G U R E 8 Comparisons of volume densities of primary bronchi, secondary bronchi and parabronchi (parabronchi), blood vessels, and
exchange tissues for birds with different lifestyles. Lifestyles are flightless (FL), low-altitude birds (LA), migratory glider (MG), high-altitude
resident (HAR), and high-altitude migratory (HAM). FL: Ostrich (Struthio camelus), Emu (Dromaius novaehollandiae); LA: Barnacle goose (Branta
leucopsis), Canada goose (Branta canadensis), Mute swan (Cygnus olor), Mallard duck (Anas platyrhynchos), Grosbeak weaver (Ambryispiza
albifrons), White-winged robin (Cercotrichas leukophrys), Yellow flycatcher (Chloropeta natalensis), Singing cisticola (Cisticola cantans), Robin
chat (Cossypha cafra), Waxbill (Estrilda astrid), Yellow-bellied waxbill (Estrilda melanotis), African rock martin (Hirundo fuligula), Red-billed
firefinch (Laganosticta senegala), Tropical boubou (Lanius aethiopicus), Fiscal shrike (Lanius collaris), Bronze mankin (Lonchura cucullate), Bronze
sunbird (Nectarina kilimensis), Golden-winged sunbird (Nectarina reichenowi), House sparrow (Passer domesticus), Baglafecht weaver (Ploceus
baglafecht), Black-headed weaver (Ploceus cucullatus), Spectacled weaver (Ploceus ocularis), Holub’s golden weaver (Ploceus xanthops), Tawny
prinia (Prinia subflava), Canary (Serinus canaria), Yellow-fronted canary (Serinus mozambicus), Common starling (Sturnus vulgaris), Redwing
(Turdus iliacus), Olive thrush (Turdus olivaceus). MG: Razorbill (Alca torda), Spectacled guillemot (Cephus carbo), Herring gull (Larus argentatus),
Common gull (Larus canus), Black-headed gull (Larus ridibundus). HAR: Yellow-billed pintail (Anas georgica), Cinnamon teal (Anas c. orinomus),
Ruddy duck (Oxyura j. ferruginea), Speckled teal (Anas oxyptera), Puna teal (Anas puna), Andean goose (Chloephaga melanoptera). HAM: Bar-
headed goose (Anser indicus). Data are taken from Maina (2002) and Maina et al. (2017). Data from birds in the present study are shown in
red. The ‘e’ and ‘o’ beside the data for the flightless birds indicate data from the emu and the ostrich
F I G U R E 9 Comparison of percentage
of exchange tissue, percentage of
pulmonary O2 extraction, and percentage
of ventilation increase. (a) Percentage of
the lung composed of exchange tissue. (b)
Percentage of O2 extracted from inspired
air while breathing a hypoxic gas mixture
(5% O2). (c) Percentage of increase in
ventilation in birds breathing the same
hypoxic gas mixture (100% is normal
level). Data sources for (b) and (c) are Scott
et al. (2015), Lague et al. (2017) and Ivy
et al. (2019)
larger in the lungs of high-altitude birds. The pulmonary speciali- falls between those of low-altitude species and the high-altitude
zations previously reported for the Andean goose, however, con- residents reported here, but a mass-specific volume of exchange
tinue to be exceptional in this regard, even among high-altitude tissue that is not significantly lower than that of the high-altitude
residents (Maina et al., 2017). The bar-headed goose that migrates residents. The data also suggest the mass-specific volume of the
at altitude twice each year has a mass-specific lung volume that lung may increase with time spent at altitude. The ruddy duck, the
|
196 BAKKEREN et al.
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DATA AVA I L A B I L I T Y S TAT E M E N T

The data that support the findings of this study are available from How to cite this article: Bakkeren C, Smith E, York JM, Chua
the corresponding author upon reasonable request. B, McCracken KG, Milsom WK. A morphometric analysis of
the lungs of high-altitude ducks and geese. J. Anat.
ORCID 2020;237:188–196. https://doi.org/10.1111/joa.13180
Ciska Bakkeren https://orcid.org/0000-0002-1485-2728
William K. Milsom https://orcid.org/0000-0002-0866-7489

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ORIG INAL PAPER

A morphometric analysis of the lungs of high-altitude ducks

Ciska Bakkeren1 | Emily Smith1 | Julia M. York2 | Beverly Chua1 |

altitude, birds, hypoxia, lungs, morphometry, pulmonary exchange tissue, pulmonary O2

1 | I NTRO D U C TI O N was hypothesized that transient high-altitude performance favoured

F I G U R E 1 Sample haematoxylin and

Species n BM (kg) VL (cm3) IPB (cm3) Pb (cm3) BV (cm3) ET (cm3)

The volumes of the main structural components of the lungs 4 | D I S CU S S I O N

F I G U R E 3 Sample haematoxylin and

F I G U R E 7 Comparison of the bird lung volumes in the present

TA B L E 3 Mass-specific volume (cm3/kg) of intrapulmonary

F I G U R E 6 Mean volume densities of the secondary bronchi,

DATA AVA I L A B I L I T Y S TAT E M E N T

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