Professional Documents
Culture Documents
Relative Size of Hearts and Lungs of Small Bats
Relative Size of Hearts and Lungs of Small Bats
net/publication/232661948
CITATIONS READS
31 1,349
4 authors, including:
Jose Iriarte-Diaz
University of the South
71 PUBLICATIONS 1,894 CITATIONS
SEE PROFILE
Some of the authors of this publication are also working on these related projects:
comparing the energetic cost of increasing aerodynamic force through different kinematic mechanisms (robotic bat) View project
All content following this page was uploaded by Jose Iriarte-Diaz on 30 May 2014.
We estimated the heart and lung size of several species of small bats (Tadarida brasiliensis, Mormopterus
kalinowski, Myotis chiloensis, Histiotus macrotus, H. montanus, Lasiurus borealis and L. cinereus) and
compared these values to those of bats of larger size and other mammals. Our results confirmed that bats have
the largest relative heart and lung size of all mammals. This is associated with the high energetic costs of flight.
As expected, the mass-specific lung and heart sizes of small bats were larger than those of large bats. However,
although relative heart mass decreased according to body mass, Mb-0.21, lung volume was nearly isometric with
body mass (exponent = 0.90). This exponent was close to unity, and between exponents reported previously
(0.77 and 1.06). This suggests that small bats compensate the energetic cost of flight mainly by changes in
cardiovascular morphology. The relative heart mass of both H. macrotus and H. montanus was particularly
large, representing 1.71 and 2.18% of total body mass, respectively. These values correspond to 121.3 and
162.7%, respectively, of the expected values from allometric relationships. In these big-eared bats, the large
hearts could be attributed to the energetic costs induced by the ears’ drag.
that these factors also affect differential- The lung volume was estimated from radio-
ly key organs of the cardiovascular and graphs with a previously developed method (Canals
respiratory systems. For example, Jurgens et al., 2005). On the images of the lungs, a straight
line (RL) between both costophrenic recesses was
et al. (1981) showed different lung volume-
traced, and several measurements were made: i) the
body mass and heart size-body mass allo- width of RL (W) as a lateral measurement; ii) the
metric relationships between bats and height between RL and the top of the left (H1) and the
other mammals (see also Maina, 2000a, right (H2) lung; and iii) left (w1) and right (w2) lung
2000b). width at the middle point of diaphragm domes (Fig.
The allometric relationships between 1). Considering the average between w1 and w2 as
lung and heart size with body size have an estimator of the dorso-ventral diameter of the
been estimated mostly for species of bats lungs (i.e., in lungs with nearly circular basal sec-
tions) a box containing the lungs and mediastinum
with body mass above 20 g (see Maina,
organs was built. Canals et al. (2005) showed that
2000b); the inclusion of more bats outside lungs filled 49.6% of the volume of this box and
this range could significantly vary these re- therefore:
lationship. Furthermore, bats are the second
VL = 0.496 × VRX ≈1/2 × VRX
most diverse order of mammals, and this di-
versity is associated with variable sources,
such as diet (from frugivores to sanguiv-
ores), life history, wing morphology, and
habitat. If these factors impose energetic
constraints on bats, we could expect differ-
ences in key organs of the cardiovascular
and respiratory systems.
The aim of this study is to estimate the
heart and lung size of small bats, comparing
them to those of bats of larger size and oth-
er mammals.
was a good estimator of the lung volume, where: unbalanced nested ANOVA, considering taxa (i.e.,
families: molossids vs. vespertilionids) and species as
H1 + H2 w +w
VRX = W × (
2
) × ( 1 2 2) factors.
represented the volume of the box containing the
lungs. RESULTS
Heart mass and lung volume were compared with
the expected values from the allometric relationships Heart masses (MH) of the studied spe-
0.0883
MH = 0.01471 × Mb cies were larger than expected from the al-
for heart mass (Jurgens et al., 1981) and: lometric relationship for bats:
VL = 0.16 × Mb
0.7731 MH = 0.01471 × Mb0.0883
for lung volume of bats (Maina et al., 1991). Also, where Mb is body mass. When MH was di-
lung volume was compared with values predicted for vided by the expected values derived from
all mammals by: the allometric relationship of Jurgens et al.
VL = 0.046 × Mb
1.06
(1981) ratios were larger than unity in most
(Gher et al., 1981). To test differences between ob- cases, 1.235 ± 0.235 (t = 7.06, n = 49, P <
served and expected values, the observed/expected ra- 0.001 — Table 1).
tio (R) was computed and the hypothesis H0: R ≤ 1 vs. When we used both Jurgens’ and our
H1: R > 1 was tested with Student’s t-tests. species we obtained the following relation-
Regression analyses (potential model) were per-
ship:
formed using our data and values from the literature
(Jurgens et al., 1981; Maina et al., 1991) to estimate MH = 0.02273 × Mb0.791±0.058
new allometric relationships between heart mass and (both variables in grams and the exponent
lung volume with body mass.
expressed as 0 ± SE; F1, 10 = 188.1, P <
To compare mass-specific heart masses (relative
heart mass, RHM) and mass-specific lung size (rela- 0.001, r2 = 0.949 — see Fig. 2).
tive lung volume, RLV) between the species of We found significant differences in the
this study, one-way ANOVA analyses or Kruskal- relative heart mass (RHM) of different
Wallis tests were used when appropriate. Multiple species (Kruskal-Wallis: H = 10.75, P <
comparisons with the Tukey test or its non-parametric 0.05). RHM of M. kalinowski was larger
equivalent were also performed. To study possible
phylogenetic effects on heart mass, independent of than that of T. brasiliensis and M. chiloen-
body mass, the ratio between the observed and ex- sis, and the RHM of H. macrotus was larg-
pected values from allometry was analyzed with an er than T. brasiliensis (P < 0.05 in multiple
TABLE 1. Heart size (0 ± SD) of bats. MH is the heart mass, RHM is the relative heart size (MH/Mb, in %),
and R is the observed/expected ratio of heart mass as derived from the allometric relationship:
MH = 0.02273 × Mb0.791±0.058 (this study)
Species n Mb (g) MH (g) RHM R
Tadarida brasiliensis 15 11.25 ± 1.13 0.145 ± 0.033 1.29 ± 0.23 0.943 ± 0.176
Mormopterus kalinowski 2 3.10 ± 1.13 0.057 ± 0.018 1.88 ± 0.10 1.041 ± 0.022
Myotis chiloensis 21 6.88 ± 0.47 0.096 ± 0.015 1.40 ± 0.20 0.921 ± 0.137
Histiotus macrotus 4 9.65 ± 0.61 0.166 ± 0.035 1.71 ± 0.03 1.213 ± 0.237
H. montanus 1 12.50 0.272 2.18 1.627
Lasiurus borealis 5 7.87 ± 1.10 0.120 ± 0.020 1.55 ± 0.27 1.046 ± 0.169
L. cinereus 5 12.76 ± 2.74 0.173 ± 0.042 1.40 ± 0.04 1.042 ± 0.279
Pipistrellus pipistrellus* 2 4.85 ± 0.18 – 1.26 ± 0.24 –
Myotis myotis* 4 20.60 ± 0.90 – 0.98 ± 0.08 –
Molossus ater* 4 38.20 ± 1.40 – 0.97 ± 0.01 –
Phyllostomus discolor* 4 45.20 ± 1.34 – 0.94 ± 0.09 –
Rousettus aegyptiacus* 3 146.00 ± 7.50 – 0.84 ± 0.08 –
* — data from Jurgens et al. (1981)
68 M. Canals, C. Atala, B. Grossi, and J. Iriarte-Díaz
FIG. 3. Observed/expected ratios for the heart mass of Tadarida brasiliensis (T brasil), Mormopterus kalinowski
(M kalino), Myotis chiloensis (M chilo), Histiotus macrotus (H macro), H. montanus (H mont), Lasiurus
borealis (L boreal) and L. cinereus (L ciner). Species differences are indicated by different letters above the bars.
Histiotus montanus was not used in the analysis (n = 1)
Heart and lung size of bats 69
TABLE 2. Body mass (Mb) and lung volume (V*L) of several bats. RVL is the relative lung size (VL/Mb)
Species n Mb (g) V*L (cm3) RVL (cm3/g)
Tadarida brasiliensis 4 11.95 ± 1.36 0.654 ± 0.091 0.055 ± 0.011
Mormopterus kalinowski 2 3.10 ± 1.13 0.162 ± 0.024 0.054 ± 0.021
Myotis chiloensis 8 6.95 ± 0.54 0.406 ± 0.071 0.058 ± 0.009
Histiotus macrotus 3 9.80 ± 0.666 0.602 ± 0.094 0.061 ± 0.005
H. montanus 1 12.50 0.696 0.056
Lasiurus borealis 2 6.80 ± 2.05 0.455 0.064 ± 0.004
L. cinereus 3 16.06 ± 7.62 1.025 ± 0.389 0.066 ± 0.010
Phyllostomus hastatus* 4 97.8 ± 2.56 4.95 ± 0.26 0.051 ± 0.007
Pteropus lylei* 7 456.0 ± 20.87 15.37 ± 1.93 0.034 ± 0.011
P. alecto* 1 667.0 22.20 0.033
P. poliocephalus* 1 928.0 39.24 0.042
* — data from Maina et al. (1991); lung volume measured by means of water displacement method
and the molossids, T. brasiliensis (11.3) estimations for WLs and ARs are 7.0 N/m2
with Molossus ater (38.2) and M. kalinows- and AR = 6.8, and 7.167 N/m2 and AR = 6.6
ki (3.1) did not show differences other than for H. macrotus and H. montanus, respec-
those expected from differences in body tively (M. Canals, unpubl. data). For L. bo-
size. Our phylogenetic analysis did not de- realis WL = 7.4 N/m2 and AR = 6.6 (Pat-
tect differences between molossids and terson and Hardin, 1969) and for M.
vespertilionids, but it showed specific dif- chiloensis WL = 6.8 N/m2 and AR = 5.76,
ferences sustained by extreme values. have been reported (Canals et al., 2002;
Histiotus species seem to have larger hearts Iriarte-Díaz et al., 2002). The ears of
than expected from the allometric relation- H. macrotus are about 3 cm long, and those
ship (Fig. 3), which could be a consequence of H. montanus about 2 cm long, represent-
of their phylogenetic position and similar ing 29–42.8% and 22–33% of the total body
morphology and life style. The RHM of length, respectively (Mann, 1978). During
both H. macrotus and H. montanus were flight these bats can afford to have large,
particularly large, 1.71 and 2.18% of body drag-producing ears, like Plecotus auritus
mass, which correspond to 121.3 and (Norberg, 1987). Field observations suggest
162.7% of the values expected from allo- that both species have a low flight speed
metric relationships, respectively. (Mann, 1978) as expected from the allomet-
Although the sample size was small, one ric relationship:
specimen of H. montanus and four speci-
mens of H. macrotus, the relative heart size v = 2.9 × WL0.44
of both species was consistently high. These where v = flight speed (Norberg, 1987).
species are commonly known as big-eared This, added to the drag-producing ears,
bats. Both species can live in dense wood- makes locomotion among shrubs energeti-
lands, but also inhabit areas with few trees. cally expensive. Their large heart could be
In Chile, they are commonly present in sa- a cardiovascular response to this life style.
vannas and zones with shrubs and wood- The heart and lung are key organs in
lands. They are generally found in small the strategy for specialization for flight in
colonies in mines, caves, roofs and tree bats. Within the mammalian scheme, the
holes (Mann, 1978; Redford and Eisen- heart and lung are remarkably refined and
berg, 1992). They have wing loadings (WL) operating close to their maximal perform-
and aspect ratios (AR) similar to those of ance (narrow-based and high-keyed strate-
M. chiloensis and L. borealis. Preliminary gy — Maina, 1998). The most important
Heart and lung size of bats 71
specializations are: large hearts (Snyder (F. BOZINOVIC, ed.). Ediciones Universidad Ca-
1976; Jurgens et al., 1981), high hematocrit, tólica de Chile, Santiago, 531 pp.
GEHR, P., D. K. MWANGI, A. AMMANN, G. M. O. MA-
hemoglobin concentration, erythrocyte LOIY, C. R. TAYLOR, and E. R. WEIBEL. 1981. De-
count and blood oxygen capacity (Wolk and sign of the mammalian respiratory system. V.
Bogdanowicz, 1987) and thin blood-gas Scaling morphometric pulmonary diffusing ca-
barrier and large lungs (Maina and King, pacity to body mass: wild and domestic mam-
1984; Maina, 1998, 2000b). Moreover, all mals. Respiration Physiology, 44: 61–86.
IRIARTE-DÍAZ J., F. F. NOVOA, and M. CANALS. 2002.
anatomical and physiological specializa-
Biomechanic consequences of differences in
tions enhance the oxygen uptake capacity of wing morphology between Tadarida brasiliensis
bats in flight to levels similar to those of and Myotis chiloensis. Acta Theriologica, 47:
birds (Thomas, 1987). Most likely, the main 193–200.
factor determining the size of these organs JURGENS, J. D., H. BARTELS, and R. BARTELS. 1981.
is related to oxygen requirements, which are Blood oxygen transport and organ weight of
small bats and small non-flying mammals. Res-
allometrically correlated with body size, piration Physiology, 45: 243–60.
and only secondarily modulated by resource MAINA, J. N. 1998. The lungs of the flying vertebrates
abundance, foraging behavior, life style and — birds and bats: is their structure optimized for
phylogeny. this elite mode of locomotion? Pp. 177–185, in
Principles of animal design: the optimization and
symmorphosis debate (E. R. WEIBEL, C. R. TAY-
ACKNOWLEDGMENTS LOR, and L. BOLIS, eds.). Cambridge University
Press, Cambridge, 314 pp.
We thank Dr. Myriam Favi for donating the stud- MAINA, J. N. 2000a. Comparative respiratory mor-
ied bats and PhD. Lafayette Eaton for idiomatic cor- phology: themes and principles in the design and
rections. This work was supported by the FONDE- construction of the gas exchangers. The Ana-
CYT 1040649 grant to MCL. tomical Record, 261: 25–44.
MAINA, J. N. 2000b. What it takes to fly: the structur-
LITERATURE CITED al and functional respiratory refinements in birds
and bats. Journal of Experimental Biology, 203:
CANALS, M., J. IRIARTE-DÍAZ, R. OLIVARES, and F. F. 3045–64.
NOVOA. 2002. Comparación de la morfología alar MAINA, J. N., and A. S. KING. 1984. The structural
de Tadarida brasiliensis (Chiroptera: Molossi- functional correlation in the design of the bat
dae) y Myotis chiloensis (Chiroptera: Vespertilio- lung. A morphometric study. Journal of Exper-
nidae), representantes de dos patrones de vue- imental Biology, 111: 43–63.
lo. Revista Chilena de Historia Natural, 74: MAINA, J. N., S. P. THOMAS, and D. M. DALLS.
699–704. 1991. A morphometric study of bats of different
CANALS, M., F. F. NOVOA, and M. ROSENMANN. 2004. size: correlations between structure and function
A simple geometrical pattern for the branching of the chiropteran lung. Philosophical Trans-
distribution of the bronchial tree, useful to esti- actions of the Royal Society of London B, 333:
mate optimality departures. Acta Biotheoretica, 31–50.
52: 1–16. MANN, G. 1978. Los pequeños mamíferos de Chile:
CANALS, M., R. OLIVARES, and M. ROSENMANN. 2005. marsupiales, quirópteros, edentados y roedores.
A radiographic method to estimate lung volume Gayana Zoología, 40: 9–342.
and its use in small mammals. Biological Re- MATHIEU-COSTELLO, O., J. M. SZEWCSAK, R. B. LO-
search, 38: 41–47. GERMAN, and P. J. AGEY. 1992. Geometry of
CRUZ-NETO, A. P., T. GARLAND, and A. S. ABE. 2001. blood-tissue exchange in bat flight muscle com-
Diet, phylogeny and basal metabolic rate in phyl- pared with bat hindlimb and rat soleus muscle.
lostomid bats. Zoology — Analysis of Complex American Journal of Physiology, 262: 955–965.
Systems, 104: 49–58. NORBERG, U. M. 1987. Wing form and flight mode in
CRUZ-NETO, A. P., D. C. BRIANI, and F. BOZINO- bats. Pp. 43–56, in Recent advances in the study
VIC. 2003. La tasa metabólica basal: ¿una vari- of bats (M. B. FENTON, P. RACEY, and J. M. V.
able unificadora en energética animal? Pp. RAYNER, eds). Cambridge University Press, Cam-
379–395, in Fisiología Ecológica y Evolutiva bridge, 470 pp.
72 M. Canals, C. Atala, B. Grossi, and J. Iriarte-Díaz
PATTERSON, A., and J. HARDIN. 1969. Flight speed of physiology in the common short nosed fruit bat
five species of vespertilionid bats. Journal of Cynopterus brachyotis. Respiration Physiology,
Mammalogy, 50: 152–153. 28: 239–247.
REDFORD, K. H., and J. F. EISENBERG. 1992. Mammals THOMAS, S. P. 1987. The physiology of bat flight. Pp.
of the Neotropics. The southern cone. The Uni- 75–99, in Recent advances in the study of bats
versity Chicago Press, Chicago, 435 pp. (M. B. FENTON, P. RACEY, and J. M. V. RAYNER,
REZENDE, E. L., F. BOZINOVIC, and T. GARLAND, JR. eds.). Cambridge University Press, Cambridge,
2004. Climatic adaptation and the evolution of 470 pp.
basal and maximum rates of metabolism in ro- WOLK, E., and W. BOGDANOWICZ. 1987. Hematology
dents. Evolution, 58: 1361–1474. of the hibernating bat, Myotis daubentoni.
SNYDER, G. K. 1976. Respiratory characteristics of Comparative Biochemistry and Physiology, 88A:
whole blood and selected aspects of circulatory 637–39.