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Histochennical properties of some jaw muscles of the lizard Tupinambis nigropunctatus (teiidae).

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THE ANATOMICAL RECORD 203:345-352 (1982)
Histochemical Properties of Some Jaw Muscles
of the Lizard Tupinambis nigropunctatus (Teiidae)
GAYLORD S. THROCKMORTON ANI) CARL W. SAUBERT I V
Department of Cell Biology, The University of Texas Health Science Center at
Dallas, Dallas, T X 75235
ABSTRACT
In many vertebrate limb and jaw muscles constituent fibers with
differing contractile and metabolic properties are distributed so as to produce distinct intramuscular oxidative and glycolytic regions. The purpose of this investigation was to determine if similar compartmentalization exists in jaw muscles of
the teiid lizard Tupinambis nigropunctatus. Nine jaw muscles from two adults and
one juvenile were examined, and serial sections from each muscle were analyzed
using histochemical techniques to indicate relative contractile, oxidative, and glycolytic capacities of the fibers and their patterns of distribution. Three distinct
fiber types were observed. The histochemical profile of type 1 fibers most closely
resembled that of tonic muscle fibers, while profiles of type 2 and type 3 fibers
corresponded to those of fast-twitch glycolytic (FG)and fast-twitch oxidative (FO)
fibers, respectively. Three muscles contained only type 2 (FG)fibers, and two muscles contained a noncompartmentalized mixture of all three fiber types. The remaining four muscles were distinctly compartmentalized, having a small, inner
oxidative region containing primarily type 1 (tonic)and type 3 (FO)fibers and a
larger, outer region consisting entirely of type 2 (FG)fibers. The possible relationships between fiber types, compartmentalization, and jaw function are discussed.
Comparison among many mammalian skeletal muscles shows a variable distribution of
fiber types, which differ in their contractile and
metabolic properties (Guth and Samaha, 1969;
Yellin, 1969; Baldwin et al., 1972; Peter et al.,
1972; Ariano et al., 1973; Collatos et al., 1977;
Gunn, 1978; Armstrong, 1980; English, 1980).
In general deep muscles within muscle groups
are composed mainly of high-oxidative fastand slow-twitch fibers, while more superficial
muscles of the group have high proportions of
low-oxidative fast-twitch fibers, and this type
of stratification is more prominent in antigravity muscle groups than in their antagonists
(Ariano et al., 1973; Collatos et al., 1977; Armstrong, 1980; Armstrong et al., 1982). These
differing properties among muscles are reflected in different patterns of muscle utilization
during locomotion (Armstrong et al., 1977;
Smith et al., 1977; Sullivan and Armstrong,
1978; Walmsley et al., 1978). A similar stratified distribution of fibers also exists within
mammalian muscles, giving rise to specialized
regions or compartments (Guth and Samaha,
1969; Yellin, 1969; Baldwin et al., 1972;
0003-276x18212033-0345102.50
C
1982 ALAN R. LISS. INC.
Gonyea and Ericson, 1977; Gunn, 1978; Armstrong, 1980;English, 1980)that may function
differentially (English, 1980).
Numerous nonmammalian vertebrates show
similar muscle compartmentalization. The iliofibularis muscle of the toad (Liinnergren and
Smith, 1966), frog (Engel and Irwin, 1967;
Smith and Ovale, 19731, and desert iguana
(Gleeson et al., 1980)have a deep (medial)oxidative compartment containing both twitch
and tonic fibers (Liinnergren and Smith, 1966;
Luff and Proske, 1979; Gleeson et al., 1980)
and a superficial glycolytic region. Most other
hindlimb muscles of the desert iguana exhibit
similar compartmentalization (Putnam et al.,
1980).
There have been few comparable studies on
vertebrate jaw muscles. Several investigators,
using various histochemical procedures, have
observed regional differences in the fiber composition of several mammalian jaw muscles
(Hiiemae, 1971; Suzuki, 1977; Maxwell et al.,
.
~~
~~
Received Septemher 18. 1981. accepted March 15. 1982
346
G.S. THROCKMOKTON AND C.W. SAUUERT IV
1979;Throckmorton and Saubert, unpublished
observations). Using morphological, histochemical, and electrophysiological techniques,
Herring et al. (1979)demonstrated that muscular activity within different histochemical portions of the pig masseter was related to specific
phases of the masticatory cycle. Similar histochemical and physiological studies have not
been conducted on jaw muscles of lower vertebrates.
The purpose of this study was to characterize the composition and compartmentalization
of nine jaw muscles of the lizard Tupinambis
nigropunctatus using standard histochemical
procedures. We observed three types of fibers
in these muscles. Four of the jaw muscles were
very distinctly compartmentalized with an inner oxidative region surrounded by a glycolytic region. The other muscles showed no compartmentalization and were composed of either
pure glycolytic fibers (two muscles) or a mixture of all fiber types (three muscles).
MATERIALS AND METHODS
The species chosen for study was the teiid
lizard Tupinambis nigropunctatus (Peters and
Donoso-Barros, 1970).Tupinambis is an omnivorous lizard which will feed on a variety of
foods including plant material, raw egg, and
small mammals, and thus exhibits a variety of
feeding behaviors and serves as a general model for lizard jaw musculature.
Three specimens of Tupinambis were used in
the study; two adults (1.16 and 8.5 kg body
weight) and one juvenile (0.60kg body weight).
The specimens were purchased from animal
dealers and were housed in wooden cages with
sun and heat lamps available and were fed raw
egg and baby mice. One animal was purchased
in September and maintained in captivity for
10 months, and the other two were purchased
in July and were sacrificed within 1 month of
arrival. There were no noticeable differences in
the muscles among the three specimens except
that the muscle fibers of the juvenile were of
much smaller diameter than those of the
adults.
Nine muscles were examined in this study:
m. depressor mandibulae, m. levator anguli
oris, m. adductor externus superficialis, m. adductor externus medius, m. pterygoideus superficialis, m. pterygoideus profundus, m.
pseudotemporalis superficialis, m. pseudotemporalis profundus, and m. adductor posterior
(Rieppel, 1980).The muscles were removed bilaterally one at a time, weighed, and then, if it
was a large muscle, it was divided into smaller
portions for ease of sectioning (See Table 1).In
addition, the plantaris and soleus muscles of
rats were used as control tissue. Muscles were
prepared as described below (see also Table 1).
In all instances where sampling occurred the
entire thickness of the muscle was retained in
the sample for analysis.
1) Depressor mandibulae: In one adult the
muscle was cut transversely across the belly to
produce origin and insertion portions. In the
other adult a sample was taken from the middle of the muscle belly. No specimen was collected from the juvenile.
2) Levator anguli oris: In both adults the entire muscle was used, and no specimen was collected from the juvenile.
3) Adductor externus superficialis: In both
adults the muscle was divided into four portions, two at the origin end and two at the insertion end. In the juvenile the entire muscle
was used.
4) Adductor externus medius: In both adults
a sample was taken from the middle of the
muscle belly and divided into anterior and
posterior portions. In the juvenile the muscle
on the right side was prepared as in the adults
and the muscle on the left side was used whole.
5) Pterygoideus superficialis: After removal,
the muscle was spread out flat. In the adults
the muscle was divided into four parts, producing medial and lateral origin and insertion portions. In the juvenile the muscle was left intact.
6) Pterygoideus profundus: In the adults a
sample was taken from the middle of the muscle belly. No specimen was collected from the
juvenile.
7) Pseudotemporalis superficialis and pseudotemporalis profundus: In the adult animals,
samples were taken from the middle of each
muscle belly, while in the juvenile both muscles were used whole.
8) Adductor posterior: In one adult a sample
was taken from the middle of the muscle belly; in
the other adult the entire muscle was used, and
no specimen was collected from the juvenile.
Each muscle sample was embedded in tragacanth gum, quick frozen in liquid freon, and
then stored at - 70°C until sectioning, when
10-mmserial sections were cut on a microtome
cryostat at - 20°C. One section was incubated
for myofibrillar adenosine triphosphatase (ATPase) activity following preincubation at pH
10.3 (Guth and Samaha, 1970). Intense staining under these assay conditions indicates
fast-twitch contractile properties (Burke et al.,
1967; Gleeson et al., 1980). Other serial sections were incubated for reduced diphosphopy-
347
HISTOCHEMICAL PHOPEKTIES OF LIZARD JAW MUSCLES
TABLE 1. Locations of muscle repions examined
Animal number
~~
Muscle
~~
~
Depressor
Mandihulae
Levator
Anguli oris
~~
~~
Middle
Whole muscle
Whole muscle
Anterior near origin
Posterior near origin
Anterior near insertion
Posterior near insertion
Adductor
Externus
Medius
Anterior middle
Posterior middle
Pterygoideus
Superficialis
Medial near origin
Lateral near origin
Medial near insertion
Lateral near insertion
Middle
Adductor
Posterior
T-11
~
Near origin
Near insertion
Adductor
Externus
Superficialis
Pterygoideus
Profundus
Pseudotemporalis
Superficialis
Pseudotemporalis
Profundus
~
T-6
(Juvenile)
-
Whole muscle
Left side
Whole muscle
Right side
Anterior middle
Posterior middle
Whole muscle
Anterior near origin
Posterior near origin
Anterior near insertion
Posterior near insertion
Anterior middle
Posterior middle
Medial near origin
Lateral near origin
Medial near insertion
Lateral near insertion
Middle
Middle
Whole muscle
Middle
Middle
Whole muscle
Middle
Middle
ridine nucleotide diaphorase (DPNH) (Novikoff et al., 1961) and alpha-glycerophosphate
dehydrogenase (a-GPDH) (Wattenberg and
Leong, 1960) activities to indicate the relative
oxidative and glycolytic capacities of the
fibers, respectively. Using light microscopy,
fibers were classified as either type 1, 2, or 3,
depending on the histochemical profile they
presented for these three assays.
RESULTS
Fiber types
Based on the histochemical analyses used we
have identified three major muscle fiber types
in the jaw muscles of Tupinambis (Figs. 1,2,3).
Because the histochemical properties of these
fibers differ somewhat from those of mammals
(Peter et al., 1972)and also from those of lizard
limb muscle fibers (Gleeson et al., 1980), we
have simply referred to these fibers as types 1,
2, and 3. The possible relationship of these designations to more standard nomenclature for
vertebrate muscle fibers types is indicated in
Table 2 and will be discussed below.
Type 1 fibers stained lightly for ATPase,
DPNH, and a-GPDH activities (Table 2, Figs.
~~
Whole muscle
1,2,3)and were found only in muscles with mixed fiber populations or in the oxidative regions
of compartmentalized muscles. Type 2 fibers
stained darkly for ATPase and a-GPDH activities and lightly for DPNH activity (Table 2,
Figs. 1,2,3)and were ubiquitous to all muscles
and muscle regions studied. Type 3 fibers
stained darkly for ATPase and DPNH activities and lightly for a-GPDH activity (Table 2,
Figs. 1,2,3). Like type 1 fibers, type 3 fibers
were found only in muscles with mixed fiber
populations or in the oxidative regions of compartmentalized muscles.
Muscles
The jaw muscles of Tupinambis fall into
three groups in terms of distribution of fiber
types (Table 3);homogeneous, mixed, and compartmentalized. Three muscles, the pterygoideus profundus, adductor posterior, and pseudotemporalis superficialis, consisted entirely
of type 2 fibers.
Two muscles, the depressor mandibulae and
levator anguli oris, contained a mixture of
three fiber types, and although there was some
regional variation in fiber distribution, there
348
G.S. THROCKMOKTON AND C.W. SAUBEKT 1V
T A B L E 2. Chmparison of histochemical properties
Alkaline
ATPase
IY-GPIIH
DPHN
Light
Dark
Light
Dark
Light
Light
Dark
Very
dark
Very
light
Hattus noruegicus
so
Light
Intermediate
to dark
Light
Dark
FG
Very
dark
.
..
FOG
Light
Dark
Dark
Dark
~
~~
SDH
ATPase
-.
(Y
GPUlI
~
Dipw\uurus d o r s d i s (Gleeson et a1 , 1980)
Dark
Dark
Light
FG
FOG
Tonic
TABLE 3. Muscle characteristics
Pure type 2:
Pterygoideus profundus
Adductor posterior
Pseudotemporalis superficialis
Completely mixed
Depressor mandibulae
Levator anguli oris
Compartmentalized:
Adductor externus superficialis
Adductor externus medius
Pseudotemporalis profundus
Pterveoideus suuerficialis'
'See results on p. 350
was no clear-cut compartmentalization. In the
depressor mandibulae approximately half of
the fibers were type 1 and they appeared to be
evenly distributed throughout the muscle.
Type 2 fibers were the least numerous. Although no direct measurements of fiber diameter were made, type 3 fibers appeared to be
Fig. 1. Serial section ( x 45) through the m. levator
anguli oris of Tupinambis nigropunctatus (specimen T-5)
showing ATPase activity following preincubation at pH
10.3. Fiber number 1 represents a lightly stained type 1
(tonic) fiber. Fiber number 2 represents a darkly stained
type 2 (FG) fiber. Fiber number 3 represents a darkly
stained type 3 (FO)fiber.
Fig.2. Serial section as in Figure 1 showing DPNH activity. Fibers 1 and 2 represent lightly stained type 1 (tonic)
and type 2 (FG)fibers, respectively. Fiber number 3 represents a darkly stained type 3 (FO)fiber.
Light
Dark
Intermediate
to dark
Dark
Dark
Intermediate
to dark
smaller in diameter than the other types and
tended to be found in groups of three or more
surrounded by type 1 fibers. In the levator anguli oris type 3 fibers were located primarily
around the lateral surface of the muscle where
they formed a layer several fibers thick.
Deeper in the muscle type 1 fibers predominated, though some type 2 and a few type 3
fibers were also present. Type 2 fibers were
most numerous in the deepest portions of the
muscle. As in the depressor mandibulae, the
type 1 and type 2 fibers tended to be larger
than the type 3 fibers.
The remaining four muscles were distinctly
compartmentalized (Fig. 4). They contained a
single, usually small, inner or medial area of
mixed fiber population and a larger, outer or
more superficial region containing only type 2
fibers. In all samples the boundaries between
these two compartments were clear cut with
little, if any, intermingling of fiber popula-
Fig. 3. Serial section as in Figure 1 showing a-GPDH activity. Fibers 1 and 3 represent lightly stained type 1 (tonic)
and type 3 (FO) fibers, respectively. Fiber number 2 represents a darkly stained type 2 (FG)fiber.
Fig. 4. A section (16 x ) from the m. pseudotemporalis
profundus of Tupinambis nigropunctatus (specimen T-5)
showing ATPase activity following preincubation a t pH
10.3. 0 - t h e oxidative region. G - the glycotic region.
HISTOCHEMICAL PROPERTIES OF LIZARD JAW MUSCLES
349
350
G.S. THROCKMORTON A N D C.W. SAUHER'I' I V
tions. We have termed the outer compartment
the glycolytic region because it is composed
exclusively of type 2 fibers that exhibit highglycolytic and low-oxidative metabolic potentials. We have termed the inner compartment
the oxidative region because this was the only
area in these compartmentalized muscles
where fibers possessing notable oxidative
metabolic capacity (type 3) were found. This
fiber organization and regional terminology
corresponds to those of compartmentalized
lizard hindlimb muscles (Putnam et al., 1980).
Of the eighteen samples of the adductor externus superficialis, nine showed a distinctive
oxidative region containing all three fiber
types; three, all in the anterior region of the
muscle from animal T-5, contained only type 2
fibers; the remaining six samples consisted of
primarily type 2 fibers with some type 1 fibers
found near one edge of the sample. When present, the oxidative region accounted for 25% or
less of the total number of fibers in these
samples and was located next to the major tendon running through the muscle. The oxidative region contained approximately 60% type
1, 20-3070 type 2, and 10-20% type 3 fibers.
The type 3 fibers were located along the medial
surface of the oxidative region.
Of the eight samples of the adductor externus medius, four contained a distinctive oxidative region located near the main tendon of
the muscle. Two oxidative regions had a few
type 3 fibers along one edge and the other two
consisted entirely of type 1 and type 2 fibers.
The type 1 fibers accounted for 60% or more of
the fibers in these regions. Again, the oxidative compartment accounted for 25% or less of
the muscle fibers present.
Of the six samples of the pseudotemporalis
profundus, only one, the left side of animal
T-11, lacked an oxidative compartment. In the
other samples, the oxidative region was relatively large, accounting for 25-30% of the
fibers in the sample. Type 1 fibers accounted
for 30-4070 of the fibers in the oxidative region
and type 3 fibers accounted for 50% or more.
Of nine samples of the pterygoideus superficialis examined, only one, the medial portion
on the right side of animal T-5, contained fibers
other than type 2. In this one sample there
were a few type 1 and type 3 fibers along one
edge of the sample. Because we did not section
the entire length of this large muscle, it seems
likely that somewhere within the muscle there
is an oxidative region, and a more complete examination of this muscle will be needed to determine the size and location of such an area.
DISCUSSION
At present most investigators use one of
three systems for classifying skeletal muscle
fiber types (Brooke and Kaiser, 1970; Burke et
al., 1967; Peter et al., 1972).We have used the
system proposed by Peter et al. (1972)in which
classification is based on three criteria- relative contractile speed, relative oxidative capacity, and relative glycolytic capacity-all of
which can be demonstrated either histochemically or biochemically. In addition, two recent
studies on lizard hindlimb muscle fiber populations (Gleesonet al., 1980; Putnam et al., 1980)
employed the system of Peter et al. (1972),and
our use of the same system simplifies comparison of results.
We have identified three major muscle fiber
types in the jaw muscles of Tupinambis and
labeled them as types 1, 2, and 3 because their
histochemical profiles are not completely compatible with those reported for mammalian and
lizard muscle fiber types. We have employed
these labels for discussion purposes only and
do not propose their adoption as standard
nomenclature.
Our type 1 fibers are the most difficult to interpret. Without direct experimental evidence
we have identified them as tonic fibers for several reasons. First, their histochemical profile
is the same as that for tonic muscle fibers in
toad (LBnnergren and Smith, 1966) and frog
(Engel and Irwin, 1967; Smith and Ovale,
1973) skeletal muscle, and no twitch fibers in
vertebrate skeletal muscle show such a profile.
Second, in the compartmentalized jaw muscles
of Tupinambis, type 1 fibers are found only in
the oxidative region, and an identical pattern
of restricted tonic fiber distribution occurs in
compartmentalized muscles of frogs (Engel
and Irwin, 1967; Smith and Ovale, 1973),toads
(Lhnergren and Smith, 1966), and lizards
(Putnam et al., 1980). Third, tonic fibers are
commonly found in a wide variety of nonmammalian skeletal muscles (see Putnam et al.,
1980). The confusing factor is that our type 1
fibers do not have the oxidative capacity of
limb tonic fibers in Dipsosaurus (Gleesonet al.,
1980), but this may reflect specialization of
fiber function, either between lizard limb versus lizard jaw muscles, between lizard species,
or between lizard limb versus other vertebrate
limb tonic fibers. In addition to their presence
in oxidative regions of compartmentalized
muscles, type 1 fibers were also present in
significant numbers in the two mixed muscles.
Our type 2 fibers clearly appear to be fast-
IIIS'I'OCHEMICAI, P w P E w I E s OF LIZARD JAW MUSCIXS
twitch glycolytic (FG) fibers, as their profiles
are identical to those of fibers classified as FG
in mammalian (Peter et al., 1972) and lizard
(Gleeson et al., 1980)hindlimb muscles. These
type 2 (FG) fibers were present in all muscles
examined and they represent the dominant
jaw muscle fiber population, as they also do in
most mammalian (Ariano et al., 1973; Collatos
e t al., 1977) and lizard (Putnam et al., 1980)
limb muscles. Three jaw muscles and the glycolytic regions of the four compartmentalized
muscles were composed entirely of type 2 (FG)
fibers, conferring on these muscles and muscle
regions the ability to contract rapidly, forcefully, and anaerobically, but limiting their ability
to provide high tension levels for prolonged periods of time. Type 2 (FG)fibers were also present in the oxidative regions of compartmentalized muscles but were less numerous than type
1 and type 3 fibers.
Our type 3 fibers have histochemical profiles
and sizes most closely resembling those of
mammalian fast-twitch oxidative (FO) fibers
(Nemeth et al., 1979).They lack the glycolytic
capacity of fast-twitch oxidative glycolytic
(FOG) fibers found in lizard (Putnam et al.,
1980)and mammalian (Peter et al., 1972)hindlimb muscles, suggesting that they may be
more specialized than similar fibers in locomotory muscles.
The pterygoideus profundus, adductor posterior, pseudotemporalis superficialis, and
most of the pterygoideus superficialis of Tupinambis are composed entirely of type 2 (FG)fibers, and this may indicate a functional specialization in these jaw muscles. If type 2 fibers
behave as mammalian FG fibers do, then these
muscles would normally be recruited only
when high tension outputs or bursts of power
are required or when the more oxidative fibers
become fatigued (Armstrong et al., 1974; Gillespie et al., 1974; Armstrong et al., 1977;
Smith et al., 1977; Sullivan and Armstrong,
1978; Walmsley et al., 1978).
The levator anguli oris and depressor mandibulae muscles have mixed fiber populations
and lack definitive oxidative and glycolytic regions. The levator anguli oris retracts the skin
of the corner of the mouth during jaw closure
in lizards (Lakjar, 1926), and the presence of
both twitch and tonic fibers would ensure that
this happens quickly, as during prey capture,
while the tonic fibers may function to retract
the skin during chewing cycles. In other lizard
species electromyographic activity from the
depressor mandibulae was observed only during the fast part of jaw opening (Throckmor-
351
ton, 1978,1980).However, because tonic fibers
produce a very lowfrequency electromyographic signal, the tonic fibers of the depressor
mandibulae may have been active during slow
opening of the jaws.
The organization of four lizard jaw muscles
is similar to that of lizard limb muscles (Gleeson et al., 1980).These muscles contain a relatively small oxidative region containing primarily type 1 (tonic)and type 3 (FO)fibers surrounded by a large glycolytic region composed
of type 2 (FG) fibers. In these lizard jaw and
limb muscles the oxidative region is usually
located deep within the muscle and often is
near a major tendon. Similar compartmentalization has been reported in mammalian limb
(Guth and Samaha, 1969; Yellin, 1969; Baldwin et al., 1972; Gonyea and Ericson, 1977;
Gunn, 1978; Armstrong, 1980; English, 1980)
and jaw (Hiiemae, 1971; Suzuki, 1977; Herring
et al., 1979) muscles, though in these species
the boundaries between regions are not as
sharp as in lizard muscle.
The presence of anatomically different
regions in a muscle suggests functional differentiation within the muscle. In mammals
the oxidative fibers are utilized during postural support and low to moderate levels of muscular tension, but they may be recruited during
all types of activity (Armstrong et al., 1974;
Gillespie et al., 1974; Armstrong et al., 1977;
Smith et al., 1977; Sullivan and Armstrong,
1978; Walmsley et al., 1978). I t is not
unreasonable to propose that our type 3 (FO)
fibers are utilized in a similar fashion. We can
only speculate that the functional role of our
type 1(tonic)fibers is one of joint stabilization,
which has been suggested as one possible function of tonic fibers in limb muscles (Simpson,
1979; Putnam et al., 1980).Given this information, we postulate that the oxidative regions of
Tupinambis jaw muscles are used for manipulative or postural activities or for stabilizing
joints during movement, while the glycolytic
regions are used when rapid movement and
strong forces are needed, as in chewing or capturing prey. Electromyographic recordings
from the different regions of individual
muscles are needed to confirm this pattern of
differential function, as has been done in mammalian limb (English, 1980) and jaw (Herring
et al., 1979)muscles.
The presence of organizational specializations in lizard jaw muscles is consistent with
the variety of functions and behaviors observed in these animals. Tupinambis exhibits a
range of feeding behaviors that involve differ-
352
G.S. THROCKMORTON AND C.W. SAUBERT IV
ences in the degree and rate of jaw movement
(Throckmorton, unpublished observations).
Prey capture and inertial feeding, for example,
utilize rapid jaw movements with wide excursions. Killing of prey often involves hard bites
that crush the prey. During swallowing and
lapping there is minimal jaw movement and
rates of movement are low. Future studies
should correlate types of jaw movement with
regional differences in muscle morphology.
ACKNOWLEDGMENTS
We would like to thank Ms. Betsy Crom for
sectioning and staining the tissues. Funds for
this project were provided by National Science
Foundation grant DEB78-05330.
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tupinambis, teiidae, histochennical, muscle, properties, lizard, nigropunctatus, jaw
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