| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 Department of Medicine, University of California, San Diego, La Jolla, California 92093-0623; and 2 Department of Biology, University of Joensuu, 80101 Joensuu, Finland
 |
ABSTRACT |
|---|
 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
The objective was to examine fiber
capillarization in relation to fiber mitochondrial volume in the highly
aerobic diaphragm of the shrew, the smallest mammal. The
diaphragms of four common shrews [Sorex araneus; body mass,
8.2 ± 1.3 (SE) g] and four lesser shrews (Sorex
minutus, 2.6 ± 0.1 g) were perfusion fixed in
situ, processed for electron microscopy, and analyzed by morphometry. Capillary length per fiber volume was extremely high, at values of
8,008 ± 1,054 and 12,332 ± 625 mm
2 in
S. araneus and S. minutus, respectively (P
= 0.012), with no difference in capillary geometry between the two
species. Fiber mitochondrial volume density was 28.5 ± 2.3%
(S. araneus) and 36.5 ± 1.4% (S. minutus;
P = 0.025), yielding capillary length per milliliter
mitochondria values (S. araneus, 27.8 ± 1.5 km; S. minutus, 33.9 ± 2.2 km; P = 0.06)
as high as in the flight muscle of the hummingbird and small bats. The
size of the capillary-fiber interface (i.e., capillary surface per
fiber surface ratio) per fiber mitochondrial volume in shrew diaphragm
was also as high as in bird and bat flight muscles, and it was about
two times greater than in rat hindlimb muscle. Thus, whereas fiber
capillary and mitochondrial volume densities decreased with increased
body mass in S. araneus compared with S. minutus
Soricinae shrews, fiber capillarization per milliliter mitochondria in
both species was much higher than previously reported for shrew
diaphragm, and it matched that of the intensely aerobic flight muscles
of birds and mammals.
capillary-fiber interface; capillary anisotropy; capillary shape; ultrastructure; morphometry
| |
INTRODUCTION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
SMALL FIBER SIZE, EXTREMELY dense capillary network, and high mitochondrial volume density are well-known structural characteristics for high O2 flux in intensely aerobic muscles. Studies of ultimate cases of extremely high O2 demand, such as the flight muscles of the hummingbird (20) and small bats (15, 21), provided insights into structural designs for high O2 flux rates in muscles in relation to their O2 demand. They revealed extremely high values of capillary length per milliliter fiber mitochondria in flight muscles (studies above and Ref. 17) at values two to three times greater than previously estimated for mammalian muscles, based on studies of various muscles, including the intensely aerobic diaphragm of the Etruscan shrew, the smallest mammal (10). Interestingly, the higher capillary length per fiber mitochondrial volume in the flight muscles was achieved via different capillary geometries in bird vs. bat. Yet capillary surface per fiber surface [SS(c,f)], i.e., the size of the capillary-fiber interface per fiber mitochondrial volume was similar in avian and mammalian flight muscles, and it was about two times greater than that in rat hindlimb. The greater SS(c,f) in flight muscle supported the notion pioneered by Gayeski and Honig (6) that capillary surface area rather than diffusion distance plays a major role in determining maximal O2 flux in muscles. It suggested that the small fiber size in these muscles may be important, not so much to reduce diffusion distances to the center of the muscle fibers, but instead to maximize the size of the capillary-fiber interface relative to the volume of mitochondria to be supplied in the muscle fibers.
The lower capillary length per fiber mitochondrial volume previously reported in the intensely aerobic shrew diaphragm (10) suggested a different structural design for high O2 flux compared with that in flight muscles of small birds and mammals. Interestingly, both mammalian heart and tuna red muscle, i.e., two muscles that contract continuously throughout an animal's lifespan, showed lower capillary length per fiber mitochondrial volume than did skeletal muscles of birds and mammals (18). Thus the lower value also reported in shrew diaphragm (10) could represent differences in structural design for high O2 flux, resulting in an apparent excess of mitochondrial volume for the size of the capillary network or reduced capillary surface area for the volume of fiber mitochondria in continuously contracting diaphragm compared with flight muscles at similar mitochondrial volume densities. To our knowledge, SS(c,f) and its relationship to fiber mitochondrial volume in shrew diaphragm have never been investigated.
The purpose of this study was to examine capillary-fiber structure, i.e., the size of the capillary-fiber interface in relation to fiber mitochondrial volume, in the intensely aerobic shrew diaphragm. Specifically, we tested the hypothesis that the structural design for high O2 flux differs in continuously contracting and intensely aerobic shrew diaphragm compared with mammalian and avian flight muscles at similar mitochondrial volume densities. The Soricinae subfamily of the insectivores shrews Soricidae were of particular interest for this study, because these shrews have distinctively high-mass-specific metabolic rates, with basal values two to three times greater than predicted from their body mass (23). We examined capillary-to-fiber geometry and relationships between fiber capillarization and mitochondrial volume in the diaphragm of the common shrew (Sorex araneus, body mass 7-12 g) and the lesser shrew (Sorex minutus, 2-3 g), i.e., two species with different body mass and, therefore, different metabolic rates and muscle aerobic capacity. We report a similar structural design for high O2 flux, i.e., as high SS(c,f) per milliliter fiber mitochondria, as in flight muscles in both species.
| |
MATERIALS AND METHODS |
|---|
|
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
Four common shrews [Sorex araneus, body mass 8.2 ± 1.3 (SE) g] and four lesser shrews (Sorex minutus, 2.6 ± 0.1 g) were used. They were captured alive with fall traps in September near the city of Joensuu in eastern Finland (latitude 62°30'N). The capture of the shrews and all of the experiments were conducted with the permission of the local committee for animal experimentation at the University of Joensuu. The shrews were anesthetized by intraperitoneal injection of pentobarbital sodium (30 mg/kg), and vascular perfusion was performed as described previously (14, 34). Briefly, the chest was cut open, and the entire vasculature was perfused via a cannula inserted directly into the left ventricle, whereas the right atrium was cut open to secure outflow. Perfusion with Ca-free saline (11.06 g/l NaCl; 4,000 USP heparin) followed by a 6.25% solution of glutaraldehyde in 0.1 M sodium cacodylate buffer (pH 7.4) was carried out at a nonpulsatile pressure of 100-120 mmHg. The diaphragms were cut into thin longitudinal strips, stored in the glutaraldehyde fixative, and processed for electron microscopy, as described previously (14).
From each diaphragm, four to eight blocks were cut into 1-µm-thick sections (four transverse and four longitudinal) with an LKB Ultrotome III. They were stained with 0.1% aqueous toluidine blue solution, and sarcomere length (lo) was measured in each longitudinal section (14). One-micrometer-thick transverse sections from three animals in the S. araneus group were used in the previous light microscopy study by Savolainen and Vornanen (34) of fiber size and capillarization in transverse sections of hindlimb muscles compared with diaphragm. Ultrathin sections (50-70 nm) were cut transversely to the muscle fiber axis from four blocks in each sample. They were contrasted with uranyl acetate and bismuth subnitrate (29), and electron micrographs for morphometry were taken on 70-mm films with a Zeiss 10 electron microscope.
Capillary numbers per fiber cross-sectional area and longitudinal
section area [QA(0) and
QA(
/2), respectively] were measured by point
counting with a 100-point eyepiece square-grid test system on
1-µm-thick sections examined at a magnification of ×400 with a light
microscope. On average, 9.0 ± 0.4 (SE) fields were examined per
sample on transverse sections, yielding ~1,200 fiber profiles for
each sample. The number of fields examined per sample in longitudinal sections averaged 18 ± 1, yielding ~220 portions of fiber
profiles in longitudinal sections from each sample. As in previous
studies (14), capillary density estimates were related to
the muscle fibers as a reference space (rather than to muscle volume)
in all samples to avoid variations due to the unreliable preservation of the intercellular spaces by the preparation procedures. In tissues
similarly prepared, our laboratory (20) has previously shown that fiber cross-sectional area [
Capillary geometry, i.e., the anisotropy coefficient
[c(K,0)], and capillary length per volume of
muscle fiber [JV(c,f)], i.e., the product of
c(K,0) and
QA(0), were estimated via a
model-based method, as described previously (13), by using
the ratio between QA(0) and
QA(/2). Capillary luminal diameter
[
Capillary-to-fiber number ratio [NN(c,f)] was
computed as the product of QA(0)
and ×
Two independent estimates of capillary perimeter in transverse section,
× [c(K,0)/c'(K',0)] ×
The volume density of mitochondria, myofibrils, and lipid droplets per
volume of muscle fiber was estimated by point counting at a final
magnification of ×30,000 on 20 fields obtained by systematic random
sampling on one ultrathin transverse section from each block (total 80 fields/sample). Mitochondrial volume per micrometer fiber length
[VN(mt,f)] was calculated as the product of
mitochondrial volume per volume of fiber [VV(mt,f)] and
Statistical analyses.
Data are expressed as means ± SE. Group means were compared by
unpaired Student's t-test and ANOVA. Estimates of
SV(c,f) and
| |
RESULTS |
|---|
|
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
The small fiber size and high capillary density in shrew diaphragm
are illustrated in Fig. 1. For
comparison, micrographs of transverse and longitudinal sections of rat
diaphragm and soleus muscles at the same magnification are also shown
in Fig. 1. Morphometric data on fiber size, capillarization, and
ultrastructure in the diaphragm of S. araneus and S. minutus are given in Table 1. The
lo ranged from 2.04 to 2.53 µm in the samples
and did not differ between S. araneus (group mean, 2.22 ± 0.10 µm) and S. minutus (2.40 ± 0.07;
P = 0.18). Capillary densities, i.e.,
QA(0), JV(c,f), and SV(c,f),
were, respectively 40, 54, and 60% greater in S. minutus
than in S. araneus, whereas differences in fiber size,
capillary number, and SS(c,f) were not
significant (Table 1).
|
|
The c(K,0) averaged 1.22 ± 0.04 and
1.24 ± 0.03 in the two groups, indicating that
JV(c,f) was, on average, 22-24% greater than a simple count of QA(0) would
indicate (see MATERIALS AND METHODS). The plot of the ratio
of QA(0) and
QA(/2) [R = QA(0)/QA(/2), used to estimate capillary geometry] and lo in
each sample are shown in Fig. 2.
Comparison with previous data in rat revealed no difference in
capillary geometry between shrew diaphragm and rat muscles (hindlimb,
diaphragm) at similar lo (Fig. 2).
|
The
Consistent with the findings on capillary cross-sectional shape,
SV(c,f)3 [calculated from
The volume density of mitochondria per volume of muscle fiber was 28% greater in S. minutus than S. araneus, with no significant difference in the volume density of subsarcolemmal mitochondria between the two groups (Table 1). The volume density of lipid droplets per volume of fiber was markedly greater in S. araneus than in S. minutus, and there was no difference in the volume density of myofibrils per volume of fiber or in VN(mt,f) between the two groups (Table 1). Whereas the reason for the greater volume density of lipid droplets in S. araneus is not clear, large differences were found between individuals in each species (range: 5.0 ± 0.3 to 15.8 ± 1.3% in S. araneus, 0.6 ± 0.1 to 4.2 ± 0.3% in S. minutus). This could be due to differences in diet, environmental temperature, and time between capture and tissue perfusion. Examination of records ruled out a seasonal effect or sex differences in lipid content in the muscle fibers in both species.
Figure 3 shows the plot of
JV(c,f) against total VV(mt,f) in
each sample. For comparison, the linear relationship and group mean
values in bat pectoralis and hindlimb and rat soleus are also shown in
Fig. 3. Comparison with previously published data in flight muscles
revealed no significant difference between capillary length per unit
volume of mitochondria, i.e., the ratio of
JV(c,f) and VV(mt,f), in S. minutus (33.9 ± 2.2 km capillary/ml mitochondria) and
S. araneus (27.8 ± 1.5 km capillary/ml mitochondria)
diaphragm, compared with bat and hummingbird flight muscles (15,
20, 21).
|
Because the capillary orientation coefficient
c(K,0) was <1.53 in all samples, the anisotropy
coefficient of capillary surface, c'(K',0), was
1, and BB(0) in transverse sections
was a direct estimate of SS(c,f) in each sample
(see Ref. 19). Figure 4
shows the plot of SS(c,f) against
VN(mt,f) in each sample. For comparison, the
linear relationships between SS(c,f) and
VN(mt,f) in flight muscle of bird and mammal and
in rat hindlimb are also shown in Fig. 4. The ratios of
SS(c,f) and VN(mt,f) did not differ among S. araneus (0.0040 ± 0.0008),
S. minutus (0.0056 ± 0.0006), and mammalian or avian
flight muscles (data not shown). SS(c,f) was 83 and 141% greater than in rat hindlimb muscle at similar
VN(mt,f) values of 89 µm3
(S. araneus) and 77 µm3 (S. minutus), respectively.
|
| |
DISCUSSION |
|---|
|
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
We found that capillary length per milliliter mitochondria was as high in the diaphragm of the Soricinae shrew as in the flight muscle of the hummingbird and small bats. Consistent with the requirements for high O2 flux rates in the muscles, SS(c,f), i.e., the size of the capillary-fiber interface, relative to fiber mitochondrial volume was also as high in the shrew diaphragm as in bird and bat flight muscles, and it was about two times greater than in rat hindlimb muscles. Whereas fiber capillary and mitochondrial densities decreased with increased body mass in S. araneus (7-12 g) compared with S. minutus (2-3 g), the ratio of the two quantities was much higher than previously reported for shrew diaphragm, and it matched that of the intensely aerobic flight muscles of birds and small bats in both species.
Fiber size. Previous studies have shown that skeletal muscles of the common shrew, S. araneus, lack slow myosin heavy chains and consist exclusively of fast motor units (32, 33), as also found in the extremely fast-contracting flight muscles of the hummingbird and small bats (1, 31). Maximum heart rates of 1,043 ± 66 (SD) beats/min (S. minutus) and 938 ± 29 beats/min (S. araneus), and respiratory rates as high as 660-800 breaths/min (resting) and 760-1,080 breaths/min (maximal) have been reported in 2- to 4-g Etruscan and Soricinae shrews (12, 22, 37). Fiber type IID (or IIX), i.e., fibers with intermediate- to high-aerobic enzyme activity, and fiber size and shortening velocity characteristics intermediate between IIA and IIB fibers were found to be particularly abundant in diaphragm (7). Consistent with its requirements of high-ATP turnover and sustained high contraction rates, the shrew diaphragm is exclusively composed of small, highly aerobic, fatigue-resistant, and fast-contracting type IID fibers (24, 33).
Our finding of extremely small fibers in S. araneus and S. minutus confirmed previous data in shrew muscles (25). Group meanFiber capillarization and mitochondrial volume.
To our knowledge, the only other reports of fiber capillary density in
relation to fiber mitochondrial volume in shrew diaphragm are from
Hoppeler and colleagues (10, 11), who reported capillary length densities of 4,000-5,500 mm2 and
mitochondrial volume densities of 28-35% in the diaphragm of a
3-g Etruscan shrew. The greater capillary densities in S. araneus
and S. minutus are partly due to methodological
differences between the two studies, i.e., the use of immersion-fixed
tissue in the Etruscan shrew study vs. perfusion-fixed material in the present study. Assuming a lo range of
1.6-2.3 µm in immersion-fixed muscle (4),
we calculate capillary length densities in the Etruscan shrew
(3,900-8,500 mm2), which largely overlap our data in
S. araneus (Fig. 3). Whereas the high metabolic and
respiratory rates in Soricinae (12) could explain their
high capillary length per milliliter mitochondria, further studies are
needed to determine whether values in the Etruscan shrew differ from
those in S. minutus and/or S. araneus. However,
the similar capillary-to-fiber ratio in the Etruscan shrew diaphragm
(2.2; H. Hoppeler, personal communication) and in S. araneus
and S. minutus (Table 1) suggests that the difference in
capillary density with our data relates to a difference in fiber size,
which is likely related largely to lo and not to
capillary number.
55%
of values measured in rat diaphragm similarly prepared at similar
lo. The smaller 2, P <0.015) with similar mitochondrial
densities (15). In contrast, capillary length density in
S. araneus diaphragm was about two-thirds that of S. minutus (Table 1), and it did not differ from the flight muscles.
Mitochondrial volume density was smaller in the diaphragm of S. araneus than in both S. minutus diaphragm and flight
muscles of the hummingbird and bat (P < 0.004),
whereas it did not differ between flight muscles and S. minutus diaphragm. Yet SS(c,f), i.e., the
size of the capillary-fiber interface, per fiber mitochondrial volume
was similar in S. araneus and S. minutus
diaphragm and bird and bat flight muscles, and it was about two times
greater than that in rat hindlimb. We are not aware of comparable data
on SS(c,f) relative to fiber mitochondrial volume in diaphragm of rat or other species.
As reported previously for hummingbird and bat flight muscles
(20, 21), the high SS(c,f) relative
to fiber mitochondrial volume in shrew diaphragm supported the notion
pioneered by Gayeski and Honig (6) that capillary number,
rather than intrafiber diffusion distance, plays a major role in
determining maximal O2 flux in muscle. Specifically,
measurements of uniformly low intrafiber PO2 in
muscle at maximal exercise indicated that a major resistance to
O2 flux occurs at the capillary-to-fiber interface, i.e.,
the carrier-free region from red blood cells in the capillaries into
subjacent muscle fiber sarcoplasm (6). Examination of myoglobin desaturation in human muscle via noninvasive proton magnetic
resonance spectroscopy (28) and functional measurement of
O2 diffusion capacity in isolated dog gastrocnemius muscle in situ (3, 9) also supported the notion of a major
functional barrier to O2 diffusion at the capillary-fiber
interface. The high SS(c,f) per milliliter
mitochondria in shrew diaphragm suggests a greater capacity for
O2 extraction from capillary to the muscle fibers, as seen
in flight muscle where the twofold greater capillary-to-fiber interface
per fiber mitochondrial volume matched the twofold higher mitochondrial
respiration rates measured in flying hummingbirds compared with limb
muscles of mammals running at maximal O2 consumption (36). No comparable data are available on maximal
mitochondrial respiration rates in shrew diaphragm.
Muscle O2 extraction depends on the interaction between
muscle O2 diffusive and convective characteristics,
according to the equation %O2 extraction = 1 
e
O2/
,
where O2 is muscle O2
diffusive capacity, 
is the slope of the O2 dissociation
curve in the physiological range, and is muscle blood flow
(30). In other words, muscle O2 extraction depends on the interaction between muscle structural capacity for
O2 flux [determined by SS(c,f)]
and functional properties of blood O2 transport, including
red blood cell flux and blood O2-carrying properties. As in
the hummingbird (20), blood capillary transit time in the
shrew is extremely short, with whole body circulation time possibly as
short as 1 s during maximal activity (35). The small
red blood cell size in shrew mentioned earlier may allow for faster
O2 uptake in the lung and faster unloading to the tissues
(2). In addition, the characteristically high-hemoglobin concentration and hematocrit of S. araneus and S. minutus blood (38) provide a high
O2-carrying capacity. Furthermore, data available in other
species of shrew suggest an increased capacity for O2
unloading to tissues, via the combined effect of low O2 affinity and large Bohr effect in shrew blood (2). Thus
hematological data point to an enhanced functional capacity for
O2 unloading in shrew diaphragm, in addition to the
increased structural capacity for O2 flux provided by the
greater capillary-to-fiber interface. It remains to be determined
whether these traits lead to altered percent O2 extraction,
compared with other muscles or species, at the enormous circulatory
rates in shrew compared with rat and larger mammals.
Similar to flight muscles, the impact of the small fiber size in the
shrew diaphragm may be to maximize the size of the capillary-fiber interface relative to fiber mitochondrial volume rather than to reduce
O2 diffusion distances to the center of the muscle fibers. Interestingly, similar SS(c,f) per milliliter
fiber mitochondria was found in shrew diaphragm as in flight
muscles with different capillary geometry and length density or fiber
mitochondrial volume. Thus, as is also found in rat (27)
and bird muscles (8, 17), the size of the capillary-fiber
interface appears to be regulated in direct proportion to fiber
mitochondrial volume or maximal O2 demand in skeletal
muscles, irrespective of their fiber-type composition, level of aerobic
capacity, degree of capillarization, or capillary geometry.
In conclusion, fiber capillarization per milliliter mitochondria
in shrew diaphragm was much higher than previously reported for that
muscle, and it matched values in the intensely aerobic flight muscles
of bird and mammals. A similar structural design for high
O2 flux, namely, as high SS(c,f) per
milliliter mitochondria as in flight muscles, was found in the
diaphragm of common (8.2 ± 1.3 g) and lesser shrews
(2.6 ± 0.1 g).
| |
ACKNOWLEDGEMENTS |
|---|
We thank Peter Agey and Larnelle Hazelwood for technical assistance with this study.
| |
FOOTNOTES |
|---|
This work was supported by National Institutes of Health Grants Minority Biomedical Research Support 2S06 GM-47165 and PO1 HL-17731 and by a grant from the Academy of Finland (project no. 7641).
Address for reprint requests and other correspondence: O. Mathieu-Costello, Dept. of Medicine, 0623A, Univ. of California, San Diego, La Jolla, CA 92093-0623 (E-mail: odile{at}ucsd.edu).
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. Section 1734 solely to indicate this fact.
First published March 29, 2002;10.1152/japplphysiol.00940.2001
Received 11 September 2001; accepted in final form 21 March 2002.
| |
REFERENCES |
|---|
|
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
|
|---|
1.
Armstrong, RB,
Ianuzzo CD,
and
Kunz TH.
Histochemical and biochemical properties of flight muscle fibers in the little brown bat, Myotis lucifugus.
J Comp Physiol [B]
119:
141-154,
1977.
2.
Bartels, H,
Bartels R,
Baumann R,
Fons R,
Jurgens KD,
and
Wright P.
Blood oxygen transport and organ weights of two shrew species (S.
etruscus and C russula). Am J Physiol Regulatory Integrative Comp Physiol
236:
R221-R224,
1979.
3.
Bebout, DE,
Hogan MC,
Hempleman SC,
and
Wagner PD.
Effects of training and immobilization on 
O2 and O2 in dog gastrocnemius muscle in situ.
J Appl Physiol
74:
1697-1703,
1993
4.
Conley, KE,
Kayar SR,
Rösler K,
Hoppeler H,
Weibel ER,
and
Taylor CR.
Adaptive variation in the mammalian respiratory system in relation to energetic demand. IV. Capillaries and their relationship to oxidative capacity.
Respir Physiol
69:
47-64,
1987.
5.
Cruz-Orive, LM,
Hoppeler H,
Mathieu O,
and
Weibel ER.
Stereological analysis of anisotropic structures using directional statistics.
Appl Stat
34:
14-32,
1985.
6.
Gayeski, TEJ,
and
Honig CR.
O2 gradients from sarcolemma to cell interior in red muscle at maximal O2.
Am J Physiol Heart Circ Physiol
251:
H789-H799,
1986
7.
Gorza, L.
Identification of a novel type 2 fiber population in mammalian skeletal muscle by combined use of histochemical myosin ATPase and anti-myosin monoclonal antibodies.
J Histochem Cytochem
38:
257-265,
1990[Abstract].
8.
Hepple, RT,
Agey PJ,
Hazelwood L,
Szewczak JM,
MacMillen RE,
and
Mathieu-Costello O.
Increased capillarity in leg muscle of finches living at altitude.
J Appl Physiol
85:
1871-1876,
1998
9.
Hepple, RT,
Hogan MC,
Stary C,
Bebout DE,
Mathieu-Costello O,
and
Wagner PD.
Structural basis of muscle O2 diffusing capacity: evidence from muscle function in situ.
J Appl Physiol
88:
560-566,
2000
10.
Hoppeler, H,
and
Kayar SR.
Capillarity and oxidative capacity of muscles.
News Physiol Sci
3:
113-116,
1988
11.
Hoppeler, H,
Mathieu O,
Weibel ER,
Krauer R,
Lindstedt SL,
and
Taylor CR.
Design of the mammalian respiratory system. VIII. Capillaries in skeletal muscles.
Respir Physiol
44:
129-150,
1981[ISI][Medline].
12.
Jurgens, KD,
Fons R,
Peters T,
and
Sender S.
Heart and respiratory rates and their significance for convective oxygen transport rates in the smallest mammal, the Etruscan shrew Suncus etruscus.
J Exp Biol
199:
2579-2584,
1996
13.
Mathieu, O,
Cruz-Orive LM,
Hoppeler H,
and
Weibel ER.
Estimating length density and quantifying anisotropy in skeletal muscle capillaries.
J Microsc
131:
131-146,
1983[ISI][Medline].
14.
Mathieu-Costello, O.
Capillary tortuosity and degree of contraction or extension of skeletal muscles.
Microvasc Res
33:
98-117,
1987[ISI][Medline].
15.
Mathieu-Costello, O,
Agey PJ,
and
Szewczak JM.
Capillary-fiber geometry in pectoralis muscles of one of the smallest bats.
Respir Physiol
95:
155-169,
1994[ISI][Medline].
16.
Mathieu-Costello, O,
Agey PJ,
Wu L,
Hang J,
and
Adair TH.
Capillary-to-fiber surface ratio in rat fast-twitch hindlimb muscles after chronic electrical stimulation.
J Appl Physiol
80:
904-909,
1996
17.
Mathieu-Costello, O,
Agey PJ,
Wu L,
Szewczak JM,
and
MacMillen RE.
Increased fiber capillarization in flight muscle of finch at altitude.
Respir Physiol
111:
189-199,
1998[ISI][Medline].
18.
Mathieu-Costello, O,
Brill RW,
and
Hochachka PW.
Structural basis for oxygen delivery: muscle capillaries and manifolds in tuna red muscle.
Comp Biochem Physiol
113A:
25-31,
1996.
19.
Mathieu-Costello, O,
Ellis CG,
Potter RF,
MacDonald IC,
and
Groom AC.
Muscle capillary-to-fiber perimeter ratio: morphometry.
Am J Physiol Heart Circ Physiol
261:
H1617-H1625,
1991
20.
Mathieu-Costello, O,
Suarez RK,
and
Hochachka PW.
Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle.
Respir Physiol
89:
113-132,
1992[ISI][Medline].
21.
Mathieu-Costello, O,
Szewczak JM,
Logemann RB,
and
Agey PJ.
Geometry of blood-tissue exchange in bat flight muscle compared with bat hindlimb and rat soleus muscle.
Am J Physiol Regulatory Integrative Comp Physiol
262:
R955-R965,
1992
22.
Morrison, P,
Ryser FA,
and
Dawe AR.
Studies on the physiology of the masked shrew Sorex cinereus.
Physiol Zool
32:
256-271,
1959.
23.
Nagel, A.
Metabolic rates and regulation of cardiac and respiratory function in European shrews.
In: Advances in the Biology of Shrews, edited by Merritt JF,
Kirkland GL,
and Rose RK.. Pittsburgh, PA: Carnegie Museum of Natural History, 1994, no. 18, p. 421-434.
24.
Peters, T,
Kubis HP,
Wetzel P,
Sender S,
Asmussen G,
Fons R,
and
Jurgens KD.
Contraction parameters, myosin composition and metabolic enzymes of the skeletal muscles of the etruscan shrew Suncus etruscus and of the common European white-toothed shrew Crocidura russula (Insectivora: soricidae).
J Exp Biol
202:
2461-2473,
1999[Abstract].
25.
Pietschmann, M,
Bartels H,
and
Fons R.
Capillary supply of heart and skeletal muscle of small bats and non-flying mammals.
Respir Physiol
50:
267-282,
1982[ISI][Medline].
26.
Poole, DC,
and
Mathieu-Costello O.
Capillary and fiber geometry in rat diaphragm perfusion-fixed in situ at different sarcomere lengths.
J Appl Physiol
73:
151-159,
1992
27.
Poole, DC,
and
Mathieu-Costello O.
Relationship between fiber capillarization and mitochondrial volume density in control and trained rat soleus and plantaris muscles.
Microcirculation
3:
175-186,
1996[Medline].
28.
Richardson, RS,
Noyszewski EA,
Kendrick KF,
Leigh JS,
and
Wagner PD.
Myoglobin O2 desaturation during exercise. Evidence of limited O2 transport.
J Clin Invest
96:
1916-1926,
1995[ISI][Medline].
29.
Riva, A.
A simple and rapid staining method for enhancing the contrast of tissues previously treated with uranyl acetate.
J Microsc (Paris)
19:
105-108,
1974.
30.
Roca, J,
Agusti AGN,
Alonso A,
Poole DC,
Viegas C,
Barbera JA,
Rodriguez-Roisin R,
Ferrer A,
and
Wagner PD.
Effects of training on muscle O2 transport at O2 max.
J Appl Physiol
73:
1067-1076,
1992
31.
Rosser, BWC,
and
George JC.
The avian pectoralis: histochemical characterization and distribution of muscle fiber types.
Can J Zool
64:
1174-1185,
1986.
32.
Savolainen, J,
and
Vornanen M.
Fiber types and myosin heavy chain composition in muscles of common shrew (Sorex araneus).
J Exp Zool
271:
27-35,
1995[ISI][Medline].
33.
Savolainen, J,
and
Vornanen M.
Myosin heavy chains in skeletal muscles of the common shrew (Sorex araneus): absence of a slow isoform and transitions of fast isoforms with ageing.
Acta Physiol Scand
155:
233-239,
1995[ISI][Medline].
34.
Savolainen, J,
and
Vornanen M.
Muscle capillary supply in hind limb and diaphragm of the common shrew (Sorex araneus).
J Comp Physiol [B]
168:
289-294,
1998[Medline].
35.
Schmidt-Nielsen, K.
Swimming and flying.
In: Scaling: Why Is Animal Size So Important? Cambridge, MA: Cambridge University Press, 1984, p. 182-196.
36.
Suarez, RK,
Lighton JRB,
Brown GS,
and
Mathieu-Costello O.
Mitochondrial respiration in hummingbird flight muscles.
Proc Natl Acad Sci USA
88:
4870-4873,
1991
37.
Vornanen, M.
Maximum heart rate of soricine shrews: correlation with contractile properties and myosin composition.
Am J Physiol Regulatory Integrative Comp Physiol
262:
R842-R851,
1992
38.
Wolk, E.
Variations in the hematological parameters of shrews.
Acta Theriol (Warsz)
19:
315-346,
1974.
This article has been cited by other articles:
|
|
 |
|
  O. Mathieu-Costello, Y. Ju, M. Trejo-Morales, and L. Cui Greater capillary-fiber interface per fiber mitochondrial volume in skeletal muscles of old rats J Appl Physiol, July 1, 2005; 99(1): 281 - 289. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. C. Frisbee Impaired skeletal muscle perfusion in obese Zucker rats Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2003; 285(5): R1124 - R1134. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
) and
S. minutus (
) diaphragm. Dotted line, linear
relationship R = (1.76 × sarcomere length) 
