Respiration Physiology (1981). 44. 61-86
Eiscvicr/Norih-Hoiiand Biomedical Presi
DESIGN OF THE MAMMALIAN RESPIRATORY SYSTEM.
V. SCALING MORPHOMETRIC PULMONARY DIFFUSING CAPACITY
TO BODY MASS: WILD AND DOMESTIC MAMMALS*
PETER GEHR1, DETER K. MWANGI2, ALEX AMMANN,
GEOFFREY M.O. MAI.OIY1, C. RICHARD TAYLOR4
and EWALD R. WEIBEL
Deportment of Anatomy. University of Heme. Berne. Switzerland
Abstract.Thii papa utilizes a comparative approach 10 establish the rcl
diffusing capacity for oxygen (Dio,) and maxii
i on the lame 21 individuals in African mammals spanning a range in body mass from
_ Ve confirmed earlier findings that Dto, was proportional lo Mb°" while V0llluI was
proportional lo Mj*. Thus, the ratio of DlOi/V0i„„, is approximately proportional to M(,"M. We
conclude that large animals require a larger pulmonary diffusing capacity to transfer oxygen at the
same rate from air to blood.
Lung morphology
Oxygen consumption
Pulmonary diffusing capacity
The pulmonary diffusing capacity Tor 02, Di.0, is the conductance for O, flow
from air to blood in the lung, driven by the partial pressure difference between
alveolar air and capillary blood (fig. I). Il is determined, in part, by some
;il Science Foundation (3.394.74 and
rd School of Public Health, 665 I luntington Avenue.
Boston, MA 02115. U.S.A.
'Present address: ILRAD, P.O. Box 30709, Nairobi. Kenya.
" dicine. University of Nairobi, P.O. Box 29053, Kabelc,
Kenya.
' Present address: Museum of Comparative Zoology. Harvard University, Cambridge, MA 02138. U.S.A.
0034-5687/81,00O0-O0O0/S02.50 © Elscvier/North-Holland Biomedical Press
SCALING
OF
Dl0i
TO
BODY
MASS
63
DESIGN OF THE MAMMALIAN RESPIRATORY SYSTEM
0, FLOW _ PRESSLNE , nMUClMICS
RA1E _ GRADIENT
;;fe (A) = (Pl-P^Oi^fl?,
\L (Si* <Fa-P»W.;VB-/JB •
we believe that marine mammals should be considered separately for reasons given
in the discussion.
Consequently, the two approaches proposed to test whether Dl0, was matched
10 vo, 6>ve paradoxical results: whereas Dl0i is closely proportional to V„, within
a size class, V0l and Dl,0j scale differently to body mass over a large size range.
It seemed possible that this paradox resulted from the fact that in the comparative
studies the measurement of V0j and Dl„, have not been done on the same animals,
or not even on a homogeneous and comparable population of animals. In order
to remove this the present study combines Dt^,. studied by morphometry in the
lungs of the same specimens of African bovids and vivcrrids on which Taylor cl al.
(1981) had obtained measurements of V0imlI. The inclusion of wild and domesticated
bovids in that study also allowed us lo compare Dl.0) with V„JlnjI for animals of
similar size but different metabolic needs.
,ided into three compartments with 02 flow_ra.es "function
MATERIALS AND METHODS
r r° T"p„ i i I o. b.« to «m»' —" " ",e r"!'
size ran? of nammab (2 s <*fc,"<T.,8'u0v°';'simitar «b,i„„ is ro„„<l f«-
mrfta on >h= m»n,m„l,.„ lung m found 1tot t.,, », 1)r„p„„io„al
t:l«^U—.s „,.« J— -U-* I*. SW »nd bod, m
This study was performed on 27 African mammals (15 species) ranging in body
mass (M,,) from 0.42 lo 251 kg as specified in table 1. The animals were recruited
from vivcrrids (dwarf mongoose, banded mongoose, genet cat), wild bovids (stint,
dik-dik, Grant's gazelle, Thomson's gazelle, wildebeest or gnu, waterbuck, eland,
giraffe) and domestic ruminants (Masai goat, Masai sheep, zebu cattle, camel).
Combined estimates of maximal oxygen consumption, V0imai, and morphomctric
diffusing capacity for oxygen, DL,,,, were obtained on 22 of these animals. V0m„
measurements were obtained while the animals were running on a treadmill by the
method described by Sccherman el al. (1981). The detailed data of this part of the
study arc presented in the companion paper by Taylor et al. (1981).
After completion of the physiological studies the animals were sacrificed and
their lungs fixed by tracheal instillation of a 2.5% potassium-phosphate buffered
glutaraldehydc solution at a head pressure of 25 cm above the chest with the animals
in supine position. The lungs were removed from the chest in tow, their volume
estimated by a water displacement method, following which we proceeded lo tissue
sampling and morphometric analysis as described in detail by Weibcl el al. (1981a).
The sampling procedure adopted for this study deviated somehow from that used
on the older material introduced here for comparison, but it has been shown that
the new method only affects the errors and not the estimates, so that the results of
the new and of the older studies remain comparable (Weibcl cl at., 1981a).
The following physical coefficients were used together with the estimates of
morphometric parameters to calculate Dl„, after the model of Wcibel (1970/71):
K, = K„ =4.1 .i0",0cm2-sec-' -mbar"1,
0Ol = 1.87 I0-' mlO, ml-' sec-' mbar-'
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£06
0056 0'0£9I
OO'tf
(IPHI1 mb PBfV)
wva
(miupttm sn2"J ot*N)
mns
tptdt PH* - "V
o
.tg ■<1"!>J
(aiySii vhm'O)
1K> 13U'D
(oStmUl soSunjl)
MOo8aoai papucg
(DjruJtd 3]v2o\>n)
ssooSuoui Jicwrj
zQ ,uij) V (;0 !"■) I
. nana, ■(iki) ;o U JOJMJ. *M P*""1
^v^^^j^sX'St. '''!'
UOJj d|da:« psynciu 91-8 »»» 4UU
SCALING OP Dl0, TO BODY MASS
• for restricted population of African
, ill 2.7 animals, (B) and (C) only those
a • Mk* (Mb in kg) for (A) and (II) and y •
ell as correlation coefficient r, are reported
for (C). 95% confiden
»L
«*)
ml
m>
66.13
3.577
58.27 . 7504
soar. 4.255
0986
0.918
5(0
V(c)
ml
2.988
4 190
2.488 . J.S8S
3.231. 5.432
0.400. 0.494
0.924
0.971
0874.
0900.
0028
0.950
0.053
-0001 .
0889.
m' ■
«K0
urn
DlO,
V(c)/(SA)
ml 0,/sec • mbar
IB)
SlM-Mb
ml/mi
0 44J
0.055
1 171
Dl-Oi/Mb
m'/kg
ml Qjltec -kR-mbar
*Oi««/Mb
nilO,/s«kg
3.474
0.051
1.71
S(A)
0)1
ml 0,/sec mbar
1.879
0.027
to
D<-0l
0.044. 0 0 6 9
0936 . 1.465
2MS0. 4.189
0.043. 0.063
1.43 , 1.976
-0.066
1.455. 2.428
0.020. 0.037
1.188
1.265
-0.003
-0.221
0.951.
0171 .
-0.009.
1.020
i' tM
0.966
0.974
1042
0.99]
0.057
1.012
0.114
-0.120. -0013
-0057.
0.052
- 0 . 2 6 2 . -0.179
1.107.
1.168 .
1.268
1.363
RHi^^"W^|
.^:m
B00Y MASS (kg)
, nowcr electron micrograph or wildebeest lung showing dense packing of capillaries <Q
r;ot^
with fibroblast processes. Magmficalion: 9000 x.
Pig. 6. Allometric plot of lung volume. African mammals. Symbols sec fig. 4.
0.991
0.9S5
0.364
0.911
0.333
-0510
-0.022
-0932
0.990
0.987
SCALING OP Dtn, TO BODY MASS
D E S I G N O P T H E M A M M A L I A N R E S P I R AT O R Y S Y S T E M
tlCHSOM G4ZEUE C*
jS SICtPt!)'
( fl A n r Vo M c u E
'9LA
(
•' SUNK?) ' V0j>na>
/
slc««:07S
CAHJI A ,'
p • qanoed Hoeoosr.
BOOY MASS (kg)
BOOY MASS (kg)
. ....r,,.-, .-..ca. African mammals. Symbols sec fig. 4.
was that found for the harmonic mean thickness of the tissue barrier (r,„) whose
mean was of the order of 0.5 pm with a range from 0.37 lo 0.65 urn (table 2).
Prom these data the morphometric pulmonary diffusing capacity for oxygen,
Dl.0l, was calculated and found to vary between 0.017 and 11.1 mlO.-s"1 -mbar"';
it scaled linearly with M„ (b = 0.95), as shown in fig. 9. It is noteworthy that the
slopes for diffusing capacity, alveolar and capillary surface areas, and capillary
volume were close to I, and that they were all significantly different from the slope
of 0.78 obtained on the same animals by Taylor et al. (1981) for V0ima, (table 2b).
Figure 10 finally plots diffusing capacity against maximal oxygen consumption
for the 21 animals on which both measurements had been obtained; Dl0, increases
with the power 1.27 of maximal oxygen consumption (tabic 2c). Thus, as shown
in fig. II, the flow of oxygen across the unit alveolar surface area or the unit
diffusing capacity is smaller in large than in small animals.
Finally, comparing the wild and domestic bovids comprised in this study for
which both V0)-M and Dl„, estimates were available (fig. 12) it is clear that the
large domestic animals had consistently a lower mass-specific V0 „,, and also a
lower mass-specific DLq,. It was surprising that goats and sheep did not show a
reduced V0lin„/Mb and Dl^,,/Mb compared to gazelles.
SHEEJM2) * /
IHOMSON GAZEUC Jr^,,,,
y gemEI CAT<2)
/ • BANDED MONGOOSE
/* DWARf MONGOOSCU)
aSooi
ooi
oi
«
*
™
Pig. 9. Allometric plot of pulmonary diffusing capacity. African mammals. Symbols see fig. 4.
100°
BODY MASS (kg)
Fig. 8. Allometric plot of capillary volume. African mammals. Symbols see fig. 4.
SCALING OF Di0, TO BODY MASS
DESIGN OP THE MAMMALIAN RESPIRATORY SYSTEM
2EBUU)
WA
R
tlSJCK/■
/ • BANDED MO«00SE
,* DWARF MONGOOSE (2)
: VfhjH, and specific Dl
3. COMPARATIVE MORPHOMETRY OF MAMMALIAN LUNGS
pu.monary diffusing capacity
against
%,„, for
African
mammal, on which V„
..j :-j:..:a....ii..
rrav|or
el al..
1981).
An important question to answer is whether the group of Kenyan mammals con
sidered in this study is representative of a broader population of mammalian lungs.
For this purpose we have compared the present data with those obtained on other
mammalian species using the same basic method. Rather than presenting individual
animal data table 3 and figs. 13-16 report average values for species estimates.
The species considered range in body weight from 2 g in the Etruscan shrew to
500 kg in tlie horse and 700 kg in a Swiss cow. Of the 32 species 15 represent
those investigated in the present study. It is clearly seen from figs. 13-16 that
the data obtained on the African ruminants and vivcrrids fit well into the general
population, and that the allometric regressions Tor all parameters are identical for
the Kenyan mammals and the overall population (tables 2 and 4). In addition
the broader population reveals that the slight increase in thickness of the air-blood
barrier with body mass is significant; it should be noted that the allometric
regression coefficient for t,,, found in the Kenyan animals is the same as that for
the overall population. Also the capillary loading of the alveolar surface area,
estimated by the ratio V(c)/S(A), is significantly increasing with body mass.
1
' 10
*
| 02
i? 01
- sloe*: - 015
LUNG FINE STRUCTURE AND BODY SIZE
L
00DY MASS (kg)
Rg. II. Plot of maximal O, flow per unit alveolar su.fac
ass for African mammals on which V0jnul was m.
unit diffusing cap"
vidually (Taylor ■■
Allhough the animals investigated span a body size range of almost three orders
nf Magnitude, there were no striking size-dependent differences in the fine structure
e.crs of pulmonary gas exchange apparatus for mammalian specie
,ed are marked by asterisk (cf. Taylor el a,.. 1981). Because of the
-lively, on the basis of M*. The two groups for the rats were.
. for *c dogs were: mean 5.4 kg. range 2.6-8.2; men U.6 kg.
in 46.1. range 36.0-57.0)
9.11
0.61
0.10
0.024
0.104
0.017
0.22
0.39
0.49
(0.00181
0.031
0.062
0.067
1.13
(Ciocubaa fffarii)
2.7
t.45
0.156
0.25
0.125
10.006)
0.571
0.063
(O.oos)
6.34
0.388
(0.054)
0.017
0077
0.013
0.004)
0.023
0.042
0.050
0.123
0.202
0.011
0.060
0.0116
(0.OO4)
0.018
0.034
0.043
0.135
0.245
0.26
0.29
0.27
(0.04)
0.37
0.36"
0.42
0.38
0.35
0.113
f"0.<WU
0.147
(0.007)
0.29
(0.012)
(ami
0.054
0.065
(0.017)
0.26
(0.005)
0.407
(0056)
0.816
(0.019)
o.4So
(0.063)
1.48
(0.0431
0.37
(0.039)
0.40
(0.021)
0.91
0.11)
0.74
(0.09)
1.46
(0.32)
5.86
1114)
4.70
(OutS)
7.15
(1*8)
Family LrporiJae
R*bbit
Dog
(Canisfamilujru)
18.2
(13.5)
43.2
tt-9)
82.7
(20J)
76.9
(45.6)
illy Glraffulce
Giraffe
:lopardalis) I
14.1
(U.l)
35.5
(8.8)
65.5
115.2)
131.9
(37J)
26.0
124.9)
55.8
(21.1)
110.0
(33.0)
233.7
(68.7)
0 43
(0.02)
0.47
(003)
0.50
I0O1)
0.53
(0.03)
(2) awmOA 9Nm
(in)
|1W
0-9SK
O'Mf
W"
(,uj) aawans avioBATv
SCALING OF Din, TO BODY MASS
DESIGN OP THE MAMMALIAN RESPIRATORY SYSTEM
Allometric regression for morphoincti ic rcspualoiy variables l<It extended |]H»pul;itimi based on species data
(table 3). Reported as in table 2
Parameter
Units
Coefficicnl a
Eipone 1 1
lean (95% eort/UaKt
inltrval)
b
(
(95% confUcnce
rMOMSOti GAZIUE7/000
COAI
/
DOGO/
GRAMS GAZEUE <
3.342
7.727
3.198
0.416
0.049
2.97/ ,
2.456.
2 JOS.
0J96.
3.759
3.027
4437
0.437
0055
1.059
0.949
0.952
1.000
0.050
1.031 . 1087
0 917.0 980
0 924.0.980
0.912.1.037
0.037.0064
0.997
0.996
0.996
0.970
0.796
OWARf MONGOOSE •/• BANDED MONGOOSE
GUrCA PO CO RAI
BOOY MASS (kg)
Fig. 15. Allometric plot of capillary volume for all species. Sec fig. 13.
*is' y i'&lu
ofthe lung parenchyma. The main difference lies perhaps in the number of alveolar
pores which arc sparse in bovids but very dense and conspicuous in the viverrid
lungs; the latter resemble shrew or dog lungs with their notoriously large number
of pores, occupying nearly every capillary loop (Gchr et at., 1980a,b). There
were also considerable differences in the dimensions of terminal airways and of
alveoli, but these did not show any obvious rclalion with body size.
This was confirmed by the morphometric analysis which revealed a great variation
in the volume density of tissue and capillaries, as well as in the alveolar surface
density, the largest and smallest values differing by 2-3 times. But with the sole
exception ofthe capillary volume density which was slightly larger in bigger animals,
these morphomclric variables were not correlated with body size. It is interesting
to note, however, that some of these variables arc significantly different between
domesticated and wild animals, so that Ihcy may be related to differences in the
level of 02 consumption.
noo a/
GRANIS OAZEIlE •
ik-d* .V**-
MONKI.Y °sl__
/ o riAUOil
•KMir CAT
/• IWNOID MONGOOSI
»«tw »° H005£
BODY MASS (kg) |
Fig. 16. Allometric plot of pulmonary diffusing cap..
SCALING OF MORPHOMETRIC VARIABLES
The present study was undertaken to compare the scaling of maximal metabolic
rate with that of the major morphometric determinants of pulmonary diffusing
capacity. The study was done on a group of mammals ranging in body mass from
400 g to 250 kg. The first uuestion to answer is whether the morphometric data
thus obtained are representative of the data obtained on a more extended population
ranging from 2 g to 700 kg and derived from 34 different species (Weibcl, 1972, 1973,
1979).
The morphometric method used in this present study was slightly modified as
compared to that used in previous studies, particularly with respect to the sampling
protocol. In a companion paper (Weibcl ci at., 1981a) we have shown that the
DESIGN OF THE MAMMALIAN RESPIRATORY SYSTEM
new and the old method yield comparable results. The two data sets can therefore
be considered jointly. ^ ^^.^ dcrJvcd for ,hc rcslrictcd and
extended populations respectively; none of the correlations ***»*"*
between restricted and extended population. We can there ore «***"»
range of African mammals considered in the present study ,s rcprcscn at.v of
he extended population. On the other hand, due to the limited weight angc
coifdenc/interva, for the regression coefficients for the Ker.ynn^annna
wider than those for the extended population; this had however no effect on the
tat stica significance of the correlations, with the exception of the scaling o
ZSSonSc mean barrier thickness, xh„ which is significant only for the extended
Telung volume, VL, corresponding to submaximal inflation was found to
sea e i X with body mass with a narrow confidence limit This IS . few*
', "videtL which also shows that lung we*ht and ^.^«g»£
linearly related to M„ (Brody, 1945; Tcnncy and Remmers 1963, Stahl, 1965, 1967,
Weibcl 1972; Barllctt and Areson, 1977; Gehr « at., 1980b).
h alveolar and capillary surface areas both scaled with a factor of 0.92 w
differed significantly from 1.0. In contrast the capillary blood volume scaled w„h
t or which was not significantly different from 1.0, and as a consequence
the capillary loading or the alveolar surface, estimated by the quotient V(c)/S(A)
how ". tendency .o increase slightly with body weight. The morphometry
puhnonary diffusing capacity, Dl0:, sca.ed linearly with Mb, the exponent 0.95
not beim; statistically different from 1.
The present study has thus, in essence, confirmed the previously estabhshed
findmg .1 a the main morphometric parameters of the pulmonary gas exchange
apparatus, namely alveolar surface area, capillary volume, and the compound
parameter DL,„. all scale about linearly with Mb.
RELATION OF MORPHOMETRIC VARIABLES TO V„!ln,j
The main purpose ofthe present study was to see how the morphometr. - >
dfile the 1 una as a gas exchanger related to maximal oxygen consumption. As
set o, it introduction two approaches are possible: (l)onc can compare
nim so comparable size but different oxygen requirements; (2) one car,.comp.™
Tiling of V, With that of morphometric variables over an extended range
of size classes. In our previous studies these two approaches had y.elded confi.cttng
-SXZSKZ* —«" size such as «^hor« JOehr and
Erni 1980) or normal and waltzing mice (Geelhaar and Weibcl. 1971, Hugon
n 111977) we had found that the morphometric variables *****ȣ
diffusing Capacity were closely related to the animals' oxygen requ.retnents. In the
SCALING OF Di.0,TO IIODY MASS
present study this finding was confirmed by comparing wild and domesticated
African bovids (fig. 12): the large domesticated bovids had a tendency to lower
oxygen needs and smaller pulmonary diffusing rapacity.
This study has however also confirmed the finding, that V0l„„ and the mor
phometric variables determining Dl.0l scale differently to body mass. Restricting
this analysis to the 12 species (21 animals) for which both estimates of V0inJ1 and
lung morphometry were available we find that V0;11I<„ scales with the power
b = 0.78 of body mass, with a 95% confidence interval for this slope of 0.72-0.83.
In contrast, alveolar surface area scales with b = 0.92 (confidence interval 0.87-0.97)
and DL0l with b = 0.95 (confidence interval 0.89-1.01). It is evident from this that
the slopes for S(A) and Dl.0l arc significantly different from the slope of V0im,,.
If we relate Dl0i directly lo V0imil wc find DLq, = 0.027 • V0jnm'".
It should be noted that the same general relationship also holds if wc compare
the scaling of morphometric variables in the extended population with the scaling
of vo.n»« f°r an extended population as presented by Taylor et at. (1981). These
two extended studies cover roughly the same size range, but were for the major
part done on different animals.
From these results wc conclude, that bigger animals require a larger pulmonary
diffusing capacity than smaller animals in order to admit the flow of oxygen
required by the organism during heavy work. For example, a wildebeest weighing
about 100 kg requires a diffusing capacity five times larger than a mongoose of
1 kg body weight to transfer the same amount of oxygen from air to blood
(see fig. 11).
COMPARISON WITH OTHER DATA
When comparing the results of the present study with those of other authors
wc first observe that physiological estimates of Dlco and Dl„, have repeatedly been
found to scale about linearly with Mh; Stahl (1967) obtained slopes of about
1.1 whereas O'Ncil and Lcith (1980) recently found a linear relation between Dlco
and Mb.
Our findings are in apparent conflict with those of Tcnney and Remmers (1963)
who had found the alveolar surface area lo be linearly related to V0l in a range
of mammals spanning six orders of magnitude from the bat to the whale, whereas
we find S(A) lo be related to V0j''. We have said before (Weibcl, 1973) that this
apparent conflict cannot result from differences in the morphometric estimates:
comparing those species that arc contained in both studies one finds good agreement
between the data; the fact that Tenncy and Remmers (1963) obtained their
measurements on air-dried lungs by light microscopy whereas we use electron
microscopy should have no effect on a comparative study of this kind. The
difference seems lo lie essentially in the selection of animals. Tcnncy and Remmers
(1963) included in their study terrestrial and marine mammals whereas our own
z i111 «
_
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