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1 Department of Medicine, An increased ratio of muscle capillary to
fiber number (capillary/fiber number) at altitude has been found in
only a few investigations. The highly aerobic pectoralis
muscle of finches living at 4,000-m altitude
(Leucosticte arctoa; A) was recently
shown to have a larger capillary/fiber number and greater contribution
of tortuosity and branching to total capillary length than sea-level
finches (Carpodacus mexicanus; SL) of
the same subfamily (O. Mathieu-Costello, P. J. Agey, L. Wu, J. M. Szewczak, and R. E. MacMillen. Respir. Physiol. 111: 189-199, 1998). To evaluate the role
of muscle aerobic capacity on this trait, we examined the less-aerobic
leg muscle (deep portion of anterior thigh) in the same birds. We found
that, similar to pectoralis, the leg muscle in A finches had a greater capillary/fiber number (1.42 ± 0.06) than that in SL
finches (0.77 ± 0.05; P < 0.01),
but capillary tortuosity and branching were not different. As also
found in pectoralis, the resulting larger capillary/fiber surface in A
finches was proportional to a greater mitochondrial volume per
micrometer of fiber length compared with that in SL finches. These
observations, in conjunction with a trend to a greater (rather than
smaller) fiber cross-sectional area in A than in SL finches (A: 484 ± 42, SL: 390 ± 26 µm2,
both values at 2.5-µm sarcomere length;
P = 0.093), support the notion that
chronic hypoxia is also a condition in which capillary-to-fiber structure is organized to match the size of the muscle
capillary-to-fiber interface to fiber mitochondrial volume rather than
to minimize intercapillary O2
diffusion distances.
capillary anisotropy; mitochondria; hypoxia; capillarization; bird
AN INCREASE IN THE SIZE of the muscle
capillary-to-fiber interface is thought to increase the
O2 conductance into muscle fibers (10), an adaptation that would be favorable for
O2 transport in hypoxia. Previous
work has shown that chronic hypoxic exposure alone does not result in a
change in either capillary-per-fiber number (28) or capillary geometry
(15, 26) in limb muscles of mammals. However, there have been so far
three reports of increased muscle capillary-per-fiber number in birds
at altitude. Léon-Velarde et al. (12) found a greater
capillary-per-fiber number in pectoralis and some limb muscles of
Andean coots living at 4,200 m than in birds of the same species
nesting at sea level. A greater capillary-per-fiber number and altered
geometry have recently been found in the flight muscle of both lowland
pigeons kept at 3,800 m for 5 mo (18) and finches living and flying at
4,000-m altitude (Leucosticte arctoa;
A) than in sea-level finches (Carpodacus
mexicanus; SL) (20). One possible explanation for the
changes in both capillary number and geometry in bird flight muscle was
its high aerobic capacity, suggesting that capillary neogenesis at
altitude may require a high O2
demand. The primary objective of this investigation was to determine
whether less aerobic leg muscle in the A finches demonstrated similar
adaptations in fiber capillarization as the highly aerobic flight
muscle (20), compared with the same leg muscles in SL
finches. Specifically, we examined whether the size of the
capillary-to-fiber interface was increased in leg muscle of A finches
and, if so, what was the role of changes in capillary-per-fiber number,
capillary geometry, and fiber size in this response. Furthermore, we
wanted to determine whether the relationship between capillary-to-fiber surface and fiber mitochondrial volume in leg muscle would be altered
at altitude.
We have recently published data on the capillary-to-fiber geometry of
the pectoralis muscle in SL and A finches (20). In this paper, we
present data for capillary-to-fiber geometry and fiber ultrastructure
of the leg muscle (deep portion of anterior thigh) of the same animals.
The materials and methods are the same as those described in the
previous paper, except for the muscle sampling of the leg, and are
briefly described below.
Five house finches, C. mexicanus (2 adult females, body mass 18.2 and 21.8 g; and 3 subadults, body mass
18.3-22 g), and five gray-crowned rosy finches,
L. arctoa (4 subadults, body mass
21.6-24.0 g; and 1 adult female, body mass 24.5 g), were used,
with adult and subadult birds identified as described elsewhere (20).
Both species belong to the same subfamily (Passeriformes: Fringillidae: Carduelinae) and demonstrate similar size and morphology as well as
similar respiratory and metabolic responses to altitude or low
temperature at rest, despite the large difference in altitude of their
habitats (4).
Tissue preparation.
All birds were collected in September, under scientific collector's
permits issued by the US Forest Service, the US Fish and & Wildlife
Service, and the California Department of Fish and Game. House finches
were caught by bait trap in Orange County, CA. Rosy finches were caught
via mist nets in permanent snow fields at an elevation of 4,000 m in
the White Mountains of Eastern California (Inyo County). All birds were
anesthetized via intravenous injection of pentobarbital sodium
(1-4 mg/100 g) within 24 h of capture, and the muscles were
perfusion fixed in situ at a nonpulsatile pressure of 150-170 mmHg
at the University of California, San Diego (house finches) and the
Barcroft Laboratory of the University of California White Mountain
Research Station (rosy finches), as detailed elsewhere (20). As in
other studies of birds (18), this perfusion pressure is higher than
that used in mammals (80-100 mmHg; Ref. 14) to match the higher
blood pressure found in birds (30). Muscle samples (~7 × 4 × 1 mm) were obtained from the midbelly of the deep portion of
the anterior thigh [femorotibialis medius muscle, which is of
mixed fiber-type composition in other birds (31)]. All muscle
samples were cut into thin longitudinal strips, stored in
glutaraldehyde fixative (total osmolarity: 1,100 mosM; pH 7.4), and
processed for electron microscopy, as described previously (14).
ABSTRACT
Top
Abstract
Introduction
Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References
METHODS
Top
Abstract
Introduction
Methods
Results
Discussion
References
Morphometry.
Capillary counts per fiber sectional area (i.e., capillary densities)
were obtained by morphometry on transverse
[QA(0)] and longitudinal
[QA(
/2)] sections
by using a 100-point eyepiece square-grid test at a magnification of
×400 on a light microscope, with muscle fibers as the reference
space to avoid errors introduced by unreliable preservation of the
intercellular spaces (14). An average of 13 ± 2 (SE)
fields/sample in transverse sections and 38 ± 7 fields/sample in
longitudinal sections were measured.
(c)], number of
capillaries around a fiber
(NCAF), fiber
cross-sectional area
[
(f)], and fiber
cross-sectional perimeter
[ 
(f)] were
measured by using an image analyzer (Videometric 150, American
Innovision) on the same transverse sections used to estimate
QA(0). An average of 171 ± 23 fibers, randomly selected by systematic sampling, were measured per
sample. The (c) was determined as the shorter axis of capillary sections that were close to circular (<20% difference between shorter and longer diameters), which assumes capillary cross-sectional circularity, as suggested previously in bird (16) and rat muscles (14). An average of 165 ± 11 capillary
profiles/sample were measured.
Capillary density and (f) were
normalized to a
lo of 2.5 µm,
because this value fell within the range found in this investigation
(2.31-2.61 µm). Capillary-per-fiber number ratio [NN(c,f)]
was calculated as the product of
QA(0) and
(f). Capillary-to-fiber perimeter
ratio [BB(0)] was
estimated in transverse sections at a magnification of ×1,000 by
using a 100-point square-grid test eyepiece system. On average, 24 ± 2 fields/sample were examined. Because
c(K,0) was <1.53 for all muscles,
BB(0) was a direct estimate of
capillary surface per fiber surface
[SS(c,f)]
(21). Capillary surface per fiber volume
[SV(c,f)1]
was estimated by using an O (6 × 6) cycloid eyepiece test system
(Cruz-Orive, Univ. of Bern, Switzerland) on vertical (i.e.,
longitudinal) sections, with the use of the same longitudinal sections
used to estimate QA(/2). An
average of 76 ± 1 fields/sample was measured at ×1,000
magnification. To test for internal consistency of the measurements,
SV(c,f) was also
calculated from BB(0), i.e.,
SV(c,f)2 = BB(0) · [(f)/(f)], and JV(c,f),
i.e.,
SV(c,f)3 = · (c) · JV(c,f).
Mean capillary perimeter in muscle transverse sections
[(c)] was estimated
by two independent methods: one making no assumptions about capillary
shape, i.e.,
(c)1 = BB(0) · (f)/NN(c,f), and one assuming circular capillary cross sections, i.e.,
(c)2 = [c(K,0)/c'(K',0)] · (c).
A significant difference between
(c)1
and
(c)2
would indicate noncircularity of the capillary cross sections (20).
The volume density of mitochondria, myofibrils, and lipid droplets per
volume of muscle fiber was estimated by point-counting on 40 fields/sample (20 fields on each of 2 blocks/sample) by using electron
micrographs of ultrathin transverse sections projected on a 144-point
square-grid test of a microfilm reader (Documator DL 2, Jenoptic, Jena,
Germany). Mitochondrial volume per micrometer of fiber length
[VN(mt,f)] was
calculated as the product of mitochondrial volume density
[VV(mt,f)] and
(f).
Statistics.
Data are means ± SE. Group means were compared by unpaired
Student's t-test. Repeated-measures
ANOVA and paired Student's t-test
were used to compare estimates of
SV(c,f) and
(c), respectively, obtained in
the same samples via different methods. Body mass was compared between
groups by using a two-way ANOVA to account for the effects of
maturational level (i.e., subadult or adult) on this variable.
Linear-regression analysis was used to interpolate
JV(c,f) at a
similar VV(mt,f) (i.e., 8%) in
each group. A two-way ANOVA was subsequently used to compare
JV(c,f) between A
and SL finches as a function of sampling site [i.e., leg muscle
(this study) and data in pectoralis muscle of the same birds
(20)].
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Body mass and fiber size.
As previously reported, body mass was significantly greater in A (23.1 ± 0.5 g) than in SL birds (20.0 ± 0.8 g;
P < 0.05), with no systematic
difference between subadult and adult in either group
(P = 0.50). Whereas
(f) in transverse sections normalized to 2.5-µm
lo was
significantly larger in A (97 ± 4 µm) than in SL birds (85 ± 3 µm; P < 0.05), muscle
(f) at 2.5-µm
lo only
demonstrated a trend to being larger in A finches (P = 0.09). Fiber shape factor, i.e.,
shape factor = 4 · · (f)/ (f)2,
was not different between A (0.64 ± 0.02) and SL birds (0.68 ± 0.01; P = 0.14).
Capillary number, surface, and geometry.
Figure 1 shows light micrographs of
transverse and longitudinal sections obtained from the leg in A and SL
finches. QA(0) normalized to
2.5-µm lo
(Table 1) was significantly greater in A
(2,990 ± 208 capillaries/mm2) than in SL
finches (1,989 ± 121 capillaries/mm2;
P < 0.01). This was because of the
greater number of capillaries per fiber, i.e., 56% greater
NCAF in A (4.2 ± 0.1) than in SL finches (2.7 ± 0.1;
P < 0.01), and 84% greater
NN(c,f) in A
(1.42 ± 0.06) than in SL birds (0.77 ± 0.05;
P < 0.01). The greater increase in
NN(c,f) in A
finches resulted in a 15% reduction of the capillary sharing factor,
i.e., number of fibers sharing a capillary = NCAF/NN(c,f)
(24). This corresponds to a greater proportion of capillaries being
shared by three rather than four fibers. There was no difference in
lo between the
muscles examined, nor was there a difference in
c(K,0) between A and SL birds (Fig. 2). For comparison, the relationships
between c(K,0) and
lo in leg of
mammal (rat soleus) and pectoralis of bird (pigeon) are also shown in
Fig. 2. The 55% greater
JV(c,f) in A
finches (P < 0.01) was due
entirely to the greater QA(0),
with no difference in the contribution of capillary tortuosity and
branching to capillary length.
SV(c,f)1
measured with a cycloid grid was 32% larger in A than in SL finches,
but the difference did not reach significance (P = 0.073).
SS(c,f) was 41%
greater in A than in SL finches (P < 0.01). The (c) was not different
between groups (P = 0.27). As found in
other birds (18, 22), (c) was smaller (range: 2.9-4.3 µm) than in mammals [e.g., rat,
range: 4.3-6.1 µm (14)], consistent with the smaller short
axis of red blood cells (RBC) in small birds (2, 8). Although RBC dimensions were not measured in this study, the RBC long axis averaged
11.5 ± 0.2 µm and the short axis 6.1 ± 0.2 µm in blood smears from house finches (4 females: 2 adults and 2 subadults) found
in the same area as the birds used in this study (unpublished observations).
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Fiber ultrastructure.
Table 2 presents data for fiber
ultrastructure in the leg of A and SL finches. The 32% greater total
VV(mt,f) in A finches (P < 0.05) was proportionally
distributed between subsarcolemmal and intermyofibrillar populations
of mitochondria.
VN(mt,f)2.5, calculated as the product of
VV(mt,f) and
(f) normalized to 2.5-µm
lo, was
significantly greater in A (45.9 ± 5.8 µm3) than in SL birds (28.1 ± 3.4 µm3;
P < 0.05). To determine the
relationship between
SS(c,f) and fiber
mitochondrial volume, we examined the quotient of
SS(c,f) and
VN(mt,f). In this ratio,
VN(mt,f) was not normalized to
lo because both
SS(c,f) and
VN(mt,f) were measured at the same
lo in each
sampling site and, therefore, variability due to
lo canceled out.
The ratio
SS(c,f)/VN(mt,f)
was similar in A (0.0056 ± 0.0007) and SL finches (0.0064 ± 0.0010; P = 0.55), indicating that the slope of this relationship was maintained at altitude compared with at
sea level.
|
2 for the leg in A and SL
finches, respectively, at 8%
VV(mt,f).
|
Capillary shape.
Capillary perimeter estimated with no assumption of shape,
(c)1,
was significantly greater than
(c)2, which assumed circular capillary cross sections, in both A (16.8 ± 1.0 vs. 11.9 ± 0.6 µm; P < 0.05) and SL finches (19.2 ± 1.4 vs. 12.8 ± 0.6 µm;
P < 0.01), indicating that capillary
cross section was not circular in either group. Taking the quotient of
(c)1/[c(K,0)/c'(K',0)]
and · (c)
revealed that capillary cross-sectional perimeter was 42 ± 12 and
50 ± 6% greater than for circular capillary profiles in A and SL
birds, respectively. There was no difference in either estimate of
capillary cross-sectional perimeter between groups, consistent with the (c) measurements made in
transverse sections. Similarly, SV(c,f)1
and
SV(c,f)2,
measured without assumption of capillary shape, were not significantly
different, indicating internal consistency of the data. In contrast,
SV(c,f)3
[i.e., using (c)], was significantly smaller than both
SV(c,f)1
and
SV(c,f)2,
confirming the noncircularity of capillary cross sections in both groups.
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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We report here for the first time a greater
NN(c,f) and fiber
mitochondrial volume in the leg muscle of A compared with SL finches of
the same subfamily (Carduelinae). In contrast to pectoralis muscle in
the same birds (20), the greater
NN(c,f) in A
finches was not associated with a greater contribution of tortuosity
and branching to total capillary length at the
lo examined
(range: 2.31-2.61 µm). The greater
NN(c,f) resulted
in a larger
SS(c,f) (41%) in
leg muscle of the A finch. This was accompanied by 63% greater fiber
VN(mt,f), due to both a greater
VV(mt,f) (32%) and a trend to
larger muscle (f) (24%;
P = 0.09) in the A finch. As a result,
SS(c,f)/fiber
VN(mt,f) did not differ between A
and SL finches. These findings are consistent with those in pectoralis
muscle in the same birds (20) and support the notion that
capillary-to-fiber structure is organized to match the size of the
capillary-to-fiber interface to fiber mitochondrial volume rather than
to minimize intercapillary O2
diffusion distances in chronic hypoxia. Furthermore, the much lower
JV(c,f) (range: 1,703-3,584 mm2) and
VV(mt,f) (5.3-11.1%) in the
femorotibialis medius muscle compared with that in the pectoralis
muscle [range: 5,584-12,009 mm2 and 15.3-31.6%,
respectively (20)] suggests that high capillarization and
O2 demand are not the sole factors
determining capillary neogenesis at altitude.
Capillarization and muscle O2 demand. Studies of adaptation to chronic hypoxia alone in mammals, including humans, have found no increase in NN(c,f) (7, 15, 28). However, Léon-Velarde et al. (12) reported for the first time greater NN(c,f) in altitude birds (Andean coots) compared with that in the same species nesting at sea level. In that study, capillary geometry was not examined, and no difference was found in either glycolytic or oxidative enzyme activity between altitude and sea-level coots.
Recent investigations of flight muscle in birds showed increased NN(c,f) and altered capillary geometry both in sea-level pigeons kept at altitude (3,800 m, inspired PO2 = 91 Torr) for 5 mo (18) and in small birds (finches) living at 4,000 m (20). The much higher capillary density in flight muscle of pigeon (~3,000-6,000 mm2) and
finch (~5,000-11,000
mm2), compared with that in
limb muscle of mammals [e.g., rodents: ~1,400-3,000
mm2 (14, 15)] and coot
[500-1,700 mm2
(12)], suggested that a high
O2 demand may be required to
induce changes in capillary geometry at altitude. The results of this investigation confirmed this hypothesis. Whereas the increased NN(c,f) in leg
muscle of the A finch, as found earlier in some leg muscles of coot
(12), showed that the level of capillarization and
O2 demand are not the sole
determining factors for capillary neogenesis, there was no change in
capillary geometry in the leg (this study), unlike previous studies of
more aerobic flight muscle in pigeon (18) or the same finches used in
this study (20).
Effect of activity on capillarization. Previous investigations have shown that exercise training in hypoxia increases muscle NN(c,f) and mitochondrial enzyme activities in humans (5, 6) and rats (3). The A finches used in this study were observed to be flying uphill into strong descending head winds to reach permanent snow fields located in cirque basins on White Mountain, thus imposing high O2 demands on the flight muscle and likely accounting for the greater NN(c,f) and altered geometry compared with SL finches (20). Interestingly, the leg muscle of the A finch also shows greater NN(c,f) and fiber mitochondrial volume than SL finch leg muscle, but, in contrast to their own (A finch) flight muscle, no alteration of capillary geometry. The change in geometry in flight muscle, reflecting a greater contribution of venular capillary branches to total capillary length, was thought to be due to the lower PO2 (and thus greater stimulus for adaptation) in venular capillaries (20). Although the rosy (A) finches forage, while hopping, on insects thawing from snow fields in this cold microenvironment, the combined increased aerobic demands of hopping locomotion and elevated thermogenesis apparently are less than those imposed by flight in this hypoxic environment. These observations further suggest the existence of a rather remarkable degree of vascular plasticity that fits a given muscle system in a single individual to the aerobic requirements imposed on that system by the physical conditions of its environment. They also suggest that it is not the absolute O2 demand per se but rather the proportion of available muscle aerobic capacity which is utilized for activity at altitude that stimulates capillary proliferation.
Factors affecting capillary and mitochondrial adaptations at
altitude.
Within a muscle,
NN(c,f) is
closely related to fiber size (29). Similarly, an increased
NN(c,f)
accompanying the increased fiber size that occurs with maturational
growth (1, 28) or functional overload (25) has been well documented in
mammals. Whereas we found a 14% greater
(f) and a trend toward a greater
(f) (24%;
P = 0.093) in leg muscle of the A
finch, NN(c,f)
was 84% greater in A finches, strongly suggesting that the higher
NN(c,f) was not
simply a function of greater fiber size. Rather,
SS(c,f) and fiber
mitochondrial volume were proportionally greater in A finch leg muscle,
supporting the suggestion that, like exercise training (27) and
electrical stimulation (19), chronic hypoxia may be another condition
in which SS(c,f)
is regulated as a unique function of fiber mitochondrial volume or
muscle O2 demand (20).
(f) in leg of A
finches, the unchanged quotient of
SS(c,f) and
VN(mt,f) in leg supported findings
in pectoralis muscle (20) and supported the notion that
capillary-to-fiber structure is organized to match fiber mitochondrial
volume rather than to minimize intercapillary
O2 diffusion distance at altitude.
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ACKNOWLEDGEMENTS |
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This work was supported by National Heart, Lung, and Blood Institute Grant 5POHL-17731.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests: R. T. Hepple, Division of Physiology, 0623A, Dept. of Medicine, Univ. of California, San Diego, 9500 Gilman Dr., La Jolla, CA 92093-0623 (E-mail: rhepple{at}ucsd.edu).
Received 23 January 1998; accepted in final form 24 June 1998.
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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