Structure and Functions of Fish Muscle

Symp. zaal. Sac. Land. (1981) No.48.
71-113
Structure and Function of Fish Muscles
IAN A. JOHNSTON
Department of Physiology, University of St Andrews,
St Andrews, Fife, Scotland
SYNOPSIS
Fish swim using a combination of paired and unpaired fins and undulations of
the segmental myotomal muscles. Although there is a simple anatomical separ-
ation of fibre types within the myotome, the myoseptal organization and orien-
tation of fibres is complex. The number of distinct fibre types described varies
from two to five depending on species. Slow ~ed fibres form either a thin super-
ficial or an internalized strip which constitutes between 0.5% and 29% of the
total muscle. Red fibres are multiterminally innervated, being activated by local
junction potentials. Characteristically, the fraction of red fibre volume occupied
by mitochondria (25-38%) is comparable to mammalian heart muscle. The bulk
of locomotory muscle consists of larger diameter fast fibres which have a highly
developed glycogenolytic capacity. In elasmobranchs,holosteans, chondrosteans
and some primitive teleosts fast fibres are innervated by a single basket-like end-
plate formation at one myoseptal end. The available electromyographical evi-
dence suggeststhat in such casesred fibres alone support sustained activity and
the fast muscle is reserved exclusively for short periods of burst swimming. In
contrast, most teleosts recruit fast fibres for higher sustainable as well as burst
swimming speeds. Fast muscles in such fish are unusual among vertebrates in
having extensive polyneuronal innervation. Isolated polyneuronally innervated
fast fibres require much higher stimulation frequencies (200-300 Hz) to elicit
maximum tensions than fibres with single end-plates (15-20 Hz). Full activation
of polyneuronally innervated muscles probably requires simultaneous and per-
haps asynchronous activity of a number of different motor neurones. This may
give additional flexibility to polyneuronally innervated fast muscles allowing
their recruitment at a wider range of swimming speeds than fibres with single
end-plates. Finally, special features of the regulation of contractility and energy
metabolism in fish muscles are discussedin relation to locomotion.
INTRODUCTION
Adaptations for aquatic locomotion account for many of the special-

ized features of fish muscle. The energy expenditure of locomotion
in water is not linearly related to speed as it is for many terrestrial
72 Ian A. Johnston
vertebrates (see Bennett, 1978). In general, the power requirements

of swimming are thought to rise as a function of body size and vel-
ocityJ. This reflects the way drag-forces on the body increase with
speed (see Webb, 1975). Thus burst speeds require proportionally
more effort than sustained swimming. This explains the predominance
of fibre types that can develop power rapidly and essentially inde-
pendently of the circulation. Typically, 90% of fish skeletal muscle
is composed of anaerobic white fibres giving the flesh both its charac-
teristic white colour and culinary importance. The possession of a
large muscle mass reserved for burst activity does not constitute a
serious weight penalty, as it would in a terrestrial animal since most
fish preserve neu tral buoyancy.
In the older fish groups (elasmobranchs, dipnoans, primitive tele-
osts) the different energetic requirements of sustained and burst
swimming have led to a complete anatomical and functional division
between fast and slow motor systems (Bone, 1966). Indeed the
physical separation of red and white fibres in the swimming muscles
of Torpedo led to one of the earliest descriptions of fibre types in
vertebrates (Lorenzini, 1678). Thus, in dogfish, sustained swimming
is entirely supported by slow red fibres which account for only 5-
10% of the myotomal musculature. In contrast, the fast motor system
which consists of phasically active white fibres is reserved for burst
activity (Bone, 1966). The red and white muscles of elasmobranchs
have somewhat similar innervation and physiological properties to,
respectively, the slow tonic and fast twitch muscles of other ver-
tebrate groups (Bone, 1964,1966, 1978a).
However, in most teleosts there is not a simple division of labour
between red and white muscles and both fibre types are recruited at
sustainable swimming speeds (Hudson, 1973; Johnston, Davison &
Goldspink, 1977; Bone, Kicznuik &Jones, 1978). The fast muscles of
advanced teleost groups are unusual among vertebrates in having
multiple innervation. For example, each fast fibre in the scorpaeni-
form fish, Myoxocephalus scorpius, is innervated by two to five
separate axons from each of four spinal nerves (Hudson, 1969).
Characteristically isolated polyneuronally innervated fast muscles
!
require much higher stimulation frequencies to elicit maximum ten-
sions than fibres with single end-plates (Flitney & Johnston, 1979;
Johnston, 1981). It seems likely that full activation ofpolyneuronally
innervated muscles requires simultaneous and perhaps asynchronous
activity of a number of different motor neurones. This may well give
additional flexibility to power development by the musculature over
and above that offered by the hierarchical recruitment of motor units
of different sizes. The control of contractility and the regulation of
Structure and Function of Fish Muscles 73
metabolism in multiply innervated fast muscles remains one of the

outstanding problems for physiologists and biochemists interested in
fish muscle.
LOCOMOTORY MUSCLES
A wide variety of body forms and modes of swimming have been

described among the fishes (see Webb, 1975; Lindsey, 1978). For-
ward swimming is usually achieved by lateral undulations of the seg-
mental myotomal muscles passing backwards along the trunk. How-
ever, a large number of fish rely to some degree on the paired and
unpaired fins to provide forward motion ( e.g. rays, trigger fish, etc. ).
In many cases, for example the surf perch Cymatogaster aggregata,
as swimming speed increases the main prop\1lsive thrust switches
from the enlarged pectoral fins to oscillations of the trunk and
caudal fin (Webb, 1973). The box fish Ostracion provides an extreme
example of the use of fins for locomotion in that the trunk is totally
inflexible and the fish swims by fan-like oscillations of the caudal fin.
The overwhelming majority of papers published on fi&h muscle
have dealt exclusively with the segmental myotomal musculature. In
teleosts and elasmobranchs the myotomes have a complex W-shape
and form a series of overlapping cones. The muscle fibres in each
myotome insert into a connective tissue sheath or myocommata.
Functional aspects of the shape and arrangement of the myotomes
have recently been reviewed both in different groups of fishes and in
development (Bone, 1978a). The orientation of fibres within the
myotome is complex and varies both along the body and with dis-
tance from the vertebral column (see Alexander, 1969). In general,
superficial fibres run parallel to the surface whereas deeper fibres
make angles of up to 40 with the long axis of the body (Alexander,
1969). The significance of this arrangement is thought to be to allow
similar degrees of sarcomere shortening at different body flexures.
Thus optimal overlap between thick and thin filaments and hence
maximum tension generation is achieved at all depths within the
myotome.
FIBRE TYPES
Nomenclature
Although classifications based on muscle colour have lost favour with
workers on other vertebrate groups, they are still widely applied to
, , L---' L--J L--J L..J
IW, OW IR.OR.S
- -
w D
I 'L-JL..J
c W PR
- ~~
w DR SR
u
FIG. 1. A diagrammatic representation of the distribution of fibre types in fish segmental
myotomal muscle. (A) Dogfish (Scytiorhinus canicuta) after Bone & Chubb (1978). S,
superficial; OR, outer red; IR, inner red; OW, outer white; and IW, inner white muscle
fibres. (B) Brook trout (Satvetinus fontinatis Mitchill) after Johnston & Moon (1980b).
R, red; and W, white muscle fibres. (C) Common carp (Cyprinus carpio L.) after Johnston,
Davison et at. (1977). R, red; P, pink; and W, white muscle fibres. (D) Skipjack tuna (Kats-
uwonus petamis L.) after Rayner & Keenan (1967) and Bone (1978b). SR, superficial red;
DR, deep red; and W, white muscle fibres. The intensity of shading represents the relative
histochemical stainin~ reactions for succinic dehvdro2Cnase. a mitochondrial marker enzyme.
fish muscle. In other vertebrates, locomotory muscles contain a

heterogeneous mixture of different fibre types. However, in fish,
fibre types are largely present in different positions within the myo-
tome (Fig. 1). Thus problems of classification which arise due to the
presence of both fast and slow red fibres are not as serious in fish as
in other animals. In addition, the complex orientation of myotomal
fibres has made it technically difficult to obtain information about
relative contraction speeds. The similar innervation of fast and slow
muscles in most teleosts also makes this an inappropriate way of
distinguishing between fibre types. Since most studies are based
entirely on histochemical or ultrastructural criteria it is often safer
to retain the rather unsatisfactory nomenclature based on colour
than to adopt unsubstantiated physiological criteria such as fast or
slow, tonic or phasic. Thus in this review the terms red and white
have been used except where data exist to allow classification accord-
ing to physiological properties.
Histologyand Histochemistry
Most investigations have concerned the segmental myotomal muscu-
lature, although there have been a few studies of the paired and
unpaired fins (Bergman, 1964; Kryvi & Totland, 1978; Nishihara,
1967; Walesby & Johnston, 1980a). In a survey 'of 84 species of
marine fish Greer-Walker & Pull (1975) reported that red fibres
constituted between 0.5 and 29% of the myotomal muscle mass.
The proportion of red fibres is highest in active pelagic families
such as Scombridae and Clupeidae and lowest in bottom dwelling
predators, deep-sea fishes and those species which use their fins as
a primary means of locomotion.
Cartilaginous fishes which have been studied include Chimaera
monstrosa (Kryvi & Totland, 1978), dogfish Scyliorhinus canicula
L. (Bone, 1966, 1978a) and the sharks Etmopterus spinax and
Galeus melastomus (Kryvi, 1977). Bone (1978a) has described five
fibre types in the dogfish on the basis of differences in innervation,
ultrastructure and histochemical staining characteristics (Fig. 1A). In 1
dogfish, the outer border of the myotome consists of a single inter-
rupted layer of large diameter superficial fibres which show negative
histochemical staining for succinic dehydrogenase (SDHase) and Ca2+-
activated myofibrillar ATPase activity (Bone & Chubb, 1978). Super-
ficial fibres are characterized by an intense staining for glucose-
phosphate-isomerase. The functional significance of these fibres is
unclear. They are unlikely to represent growth stages of the under-
lying red fibres since they appear relatively late during post-embryonic
76 IanA. Johnston
development (Bone, 1978a). Two types of red fibre can be dis-
tinguished on the basis of size, aerobic capacity and myofibrillar
ATPase activity (Bone & Chubb, 1978). Outer red fibres have a
higher SDHase and lower myofibrillar ATPase activity than the some-
what larger diameter red fibres adjacent to the white muscle. The
outer few layers of white fibres are differentiated from deep white
fibres by having a higher proportion of mitochondria, more abundant
capillary supply, and a somewhat different myofibrillar ATPase
activity (Fig. 1A) (Bone, 1978a; Bone & Johnston, in press). Bio-
chemical measurements of myofibrillar ATPase of the five fibre types
of dogfish are presented in Table I and correlated with the histo-
chemical observations.
TABLEI
Mg2+- Ca2+-stimulated myofibrillar A TPase activities of fish skeletal muscle fibre
types. Activities expressed as Jlmol P'Pi released, mg myofibrillar protein-1
min-i
Outer red 0.06 0.51

0.25 0.25
Inner red 0.18 } 0.50
Pink 0.62
Outer white 0.55

0.73 1.09 0.99
Inner white 0.40 }
Data from Bone &Johnston (in press)a, Johnston & Moon (1980b)b,Johnston, Davison
& Goldspink (1977)C and Johnston & Tota (1974)d. Numbers of fish used and standard
errors of the mean are given in the original publications. Assay temperatures are shown in
brackets.
The arrangement of fibre types of some representative teleosts is

shown in Fig. 1B-D. The simplest case is exemplified by species such
as brook trout (Salvelinus fontinalis Mitchill) (J ohnston & Moon,
1980b: fig. 2) and the Atlantic mackerel (Scomber scombrus) (Bone,
1978b ). In these fish the myotome is differentiated into two distinct
fibre types on the basis of histochemical staining for aerobic enzymes
and myofibrillar ATPase (Fig. 1B; Johnston & Moon, 1980b). Bio-
chemically the myofibrillar ATPase activity of the white fibres is
around three times that of the red (J ohnston, Frearson & Goldspink,
1972: table 2). White fibres are SDHase negative and form a hetero-
Q:eneousg:roup with respect to fibre size. In the case of rainbow
trout there is a continuous distribution of white muscle fibre diam-

eter between 15 and 90.urn, overlapping that of red fibres, 5-40.urn
Oohnston, Ward & Goldspink, 1975). Most workers have considered
the range of fibre size in teleost white muscle to represent different
stages in growth rather than distinct fibre types Oohnston, Ward
et al., 1975; Korneliussen, Dahl & Paulsen, 1978; Johnston & Moon,
1980b). Greer-Walker (1970) has shown that fibre number continues
to increase throughout life in many species of fish. This contrasts
with the situation found in most other vertebrates where fibre
number is fixed at or shortly after birth.
There have been relativ~ly few studies of capillary supply and
blood flow to fish red and white muscle fibres (Boddeke, Slijper &
van der Stelt, 1959; Bone, 1978b; Stevens, 1968; Mosse, 1978).
Capillary density is related to the aerobic capacity of the muscle. In
a study of three teleost species Mosse (1978) found a mean capillary
fibre ratio of 0.2-0.9 for white and 1.9-2.5 for red muscle. In
Platycephalus bassensis 49% of white fibres have no peripheral
capillaries (Fig. 2). Interestingly, the capillarization of white muscles
in certain pelagic species is more highly developed. The white fibres
of yellow tail scad (Trachurus maccullochi), pilchard (Sardinops
neopilchardus) and mackerel (Scomber australasicus) have fewer
fibres with no peripheral capillaries (17.8%, 16.5% and 23% respec-
tively} (Mosse, 1979}.
~n
an
30
Percent.
Fibres ?n
10
0 1 2 3 4 5 6 7 8 9 10 11
Number Capillaries
FIG. 2. Percentage of red and white muscle fibres surrounded by a given number of capil-
laries. The data is for the flathead (Platycephalus bassensis) and counts were made by direct
visualization of capillaries in semi-thin (1 JJ.m) durcupan sections. From Mosse (1978: table
31.
78 Ian A. Johnston
In some species another type of fibre occurs in an intermediate

position between the red and white muscle layers (Bokdawala &
George, 1967; Johnston, Patterson, Ward & Goldspink, 1974;Mosse
& Hudson, 1977). These so-called pink fibres can be di'stinguished
histochemically from other fibre types on the basis of their stability
to alkaline (pH 10.3-10.4) preincubation prior to staining for myo-
fibrillar ATPase activity (Johnston, Patterson et at., 1974). In carp
(Cyprinus carpio ), pink fibres constitute a larger proportion of the
myotome than red fibres (-10%) (Fig. 1C) (Davison, Johnston &
Goldspink, 1976). Biochemical studies of the fibre types in carp have
shown pink fibres to ,have intermediate aerobic enzyme and Mg2+
Ca2+ myofibrillar ATPase activities between red and white fibres
(Johnston, Davison et at., 1977). The light chain compositions of
vertebrate myosins have been shown to be characteristic of fibre
phenotype (Lowey & Risby, 1971). Carp red fibres have two, and
pink and white fibres, three species of light chain, characteristic of
slow and fast muscle myosins respectively (Focant, Huriaux &
Johnston, 1976;Johnston, Davison et at., 1977).
Some fishes of the family Scombridae have internalized red
muscle masses (Fig. 1D). This feature is associated with a counter-
current vascular heat-exchanger which enables elevated red muscle
and brain temperatures to be maintained over a wide range of am-
bient temperatures. The extent to which capacities for regulating
body temperature have developed within the tunas varies consider-
ably between species (see Sharp & Pirages, 1978). In the skipjack
tuna (Katsuwonus petamis) the superficial wedge of red muscle is
differentiated from the internalized red muscle by a larger fibre size
and a significantly lower histochemical staining for SDHase activity
(Bone, 1978b ). Indeed, quantitative ultrastructural studies by Bone
(1978b) have shown ten times as many mitochondria in deep red
fibres (Table II) and a more highly developed capillary bed (-4.7
capillaries/fibre). Mitochondria in superficial red and white muscle
differ from those of the deep red fibres in showing a reduction of
cristae development and the presence of lamellar figures interrupting
the cristae array (Bone, 1978b). Mg2+ Ca2+ myofibrillar ATPase
activities of Atlantic bluefin tuna (Thunnus thynnus) red muscles .
are twice that of white muscle and somewhat higher than analogous
red muscles of less active species (Table I) (Johnston & Tota, 1974).
In tuna muscular effort associated with ventilation has been trans-
ferred from the buccal to myotomal muscles (ram ventilation)
(Dizon, Brill & Yuen, 1978). This feature is associated with contin-
uous high-speed swimming. Significantly it has been suggested that
both tuna red and white muscles have a significant capacity of
aerobic glucose utilization (Guppy, Hulbert & Hochachka, 1979).
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80 Ian A. Johnston
ULTRASTRUCTURE
There have been a number of recent quantitative studies of the fine

structure of fish myotomal (Patterson & Goldspink, 1972, 1973;
Kryvi, 1977; Kryvi & Totland, 1978; Bone, 1978b; Walesby &John-
ston, 1980a; Johnston & Maitland, 1980) and pectoral muscles
(Kryvi & Totland, 1978; Walesby &Johnston, 1980a).
The striking feature of fish red muscle is the high mitochondrial
density, which often exceeds that found in the most active mam-
malian muscles. For example, the fractional volume occupied by
mitochondria in red myotomal muscles of various cold-water species
is comparable to their volume in the ventricular muscle of the mouse
l
FIG. 3. (A) Brook trout (Salvelinus !ontinalis) red muscle fibres. Transverse frozen section
(10 Jlm) stained for succinic dehydrogenase as a mitochondrial marker enzyme. Note lipid
droplets between red fibres (R) and the higher SDHase staining in red than in white fibres
(W) (bottom left). (B) Brook trout red fibres, semi-thin (I Jlm) araldite embedded section
stained with p"p~5=nylene diamine (PPDA). Note the abundant capillary supply (C) and the
high proportion of fibre volume occupied by mitochondria (M) and lipid (L). (C) Longitudi-
nal section of plaice red fibre from a four-month-starved fish. Note loss of cristae from mito-
chondria (C) also the presence of a distinct M line (ML) and capillary (CL) containing a
nucleated red blood corpuscle (RBC). (D) Plaice (Pleuronectes platessa L.) red fibre. Elec-
tronmicrograph showing high mitochondrial density (M) and numerous lipid droplets (L).
This fish has been food deprived for several weeks. Note the depletion of lipid deposits (DL).
(34%) and finch (37%) (Bossen, Sommer & Waugh, 1978) (Table II;
Fig. 3). In contrast, approximately 0.5-8% of white fibre volume is
occupied by mitochondria, depending on position within the myo-
tome and species (Table II). An interesting exception to this corre-
lation between muscle pigmentation and respiratory capacity occurs
in ice fishes of the family Channichthyidae. In this group all muscles
are pure white in colour owing to the absence of both haemoglobin
(Rudd, 1954) and myoglobin (Hamoir, 1978; Walesby, Nicol &
Johnston, in press). The superficial myotomal fibres in the pelagic
ice fish Champsocephalus gunnarii have a mitochondrial density of
around 45% and are almost entirely surrounded by capillaries
(Walesby, Flitney &Johnston, unpublished results).
Another characteristic of fish red or slow fibres concerns the
highly developed sarcoplasmic reticulum (SR) and T-tubule system.
The fractional volume occupied by SR in red muscle is greater than
for tonic and slow twitch muscles in other vertebrates and approaches
that of fast twitch fibres U ohnston, 1980b ). Quantitative data from
studies of fish sarcotubular systems are summarized in Table III. In
most myotomal muscles studied T -tubules are located at the junction
TABLE III
Fractional volume (%) occupied by sarcoplasmic reticulum and T-system in some

representative vertebrate muscles
Sarcoplasmic reticulum T -system
Species Muscle Type

- - -
Red White Red White
ELASMOBRANCHS
Etmopterus spinaxG 4.9 6.0 0.33 0.55
Ga/eus me/astomusG 4.6 6.8 0.57 0.89
TELEOSTS
Salmo gairdnerib 5.1 13.7 0.10
Tonic Twitch Ton.ic Twitch

AMPHIBIANS
Rana pipiensc 4-5' 9.1 O.18g
Slow Fast Slow Fast
Twitch Twitch Twitch Twitch
MAMMALS
Guinea pigd,e 3.2 4.6 0.14 0.27
Data is taken from the following: aKryvi (1977); bNag (1972); CMobley & Eisenberg (1975);
dEisenberg & Kuda (1975); eEisenberg, Kuda & Peter (1974); fpeachey (1965); gFlitney
(1971) (Rana temtJoraria).
82 Ian A. Johnston
of the Z disc (Franzini-Armstrong & Porter, 1964; Kilarski, 1966;

Nag, 1972; Patterson & Goldspink, 1972; Kryvi, 1977). A similar
location of the tubular system is found among the locomotory muscles
of lampreys (Teravainen, 1971), urodeles (Totland, 1976) and
anurans (Peachey, 1965). In fish extraocular (Kilarski, 1966) swim
bladder and drum muscles (Eichelberg, 1976) and in hagfish (Kom-
eliussen & Nicolaysen, 1973) and mammalian muscles the T-tubules
are situated at the A-1 boundary. The functional significance of these
different positions is unknown.
The fractional volume occupied by myofibrils varies from 80-96%
in white muscles to 40-60% in red muscles (see Johnston, 1980b,
for a review). Myofibrillar packing is more regular in white muscles.
White fibres of teleosts are characterized by elongated peripheral myo-
fibrils (Fig. 4). In small fibres the arrangement of fibrils resembles
FIG. 4. (A) Transverse section of a pink fibre from the myotomal muscle of the crucian carp
(Carassius carassius L.). Note intermediate mitochondrial density (M) and irregular myo-
fibrillar packing (My). In this species lipid droplets are not common in any fibre type; the
principal stored fuel is glycogen. (B) Brook trout white fibres. Transverse frozen section
(10 !lm) stained for succinic dehydrogenase. Dark spots within the fibres correspond to
lipid and mitochondrial accumulations. Note the wide range of fibre size. (C) Brook trout
white fibres. Semi-thin (I !lm) araldite embedded section stained with p-phenylene diamine
(PPDA). Note the peripheral ribbon-like myofibrils (PM), the dense myofibrillar packing
(My) and the accumulations of mitochondria (M) and lipid (L). (D) Longitudinal section
of crucian carp white fibre. Note distinctive M-Iine (ML), mitochondria (M) with highly
developed cristae array and glycogen rosettes (G).
a cart-wheel with spokes radiating to a small central hub of sarco-

plasm. This feature is not observed in elasmobranchs, holocephali or
higher vertebrates and may be related to the pattern of fibre growth
in teleosts.
In contrast to higher vertebrates, both red and white fibres have a
distinctive M-line (Figs 3 & 4). Other ultrastructural criteria for dis-
tinguishing between fibre types include a somewhat thicker Z-line in
white than in red fibres (Patterson & Goldspink, 1972) and differ-
ences in the deposition of stored metabolites (Bone, 1978a). Glycogen
particles are present either as rosettes or small chains in all fibre
types but are particularly abundant in red fibres. With the exception
of tuna Euthynnus petamis which has higher glycogen stores in white
fibres (Guppy et at., 1979) this is a reversal of the typical vertebrate
pattern (1ohnston, 1980b ). Biochemical determinations of gly-
cogen concentrations vary from 350-3600 mg/l 00 gin red to 9-
1440mg/100g in white fibres depending on activity level, nutritional
status, and species (Love, 1970). Lipid droplets are usually more
abundant in red than white fibres constituting 11% of fibre volume
in brook trout (Satvetinus fontinatis Mitchill) and plaice (pteuronectes
ptatessa) Oohnston & Moon, 1980b; Johnston, 1981) (Fig. 3).
In fatty fish such as arichovy Oohnston, unpublished) a layer of fat
cells occurs between the skin and red muscle layer, while in other
species, for example mackerel (Bone, 1978b) and eel, adipocytes are
widely distributed among the white muscle fibres. The extent to
which the muscle lipid reserves of such fish represent metabolic
stores, or function as part of a buoyancy mechanism, is unknown.
There have been relatively few ultrastructural investigations of the
fibre types other than red or white. Intermediate/pink fibres of the
carp Oohnston & Maitland, 1980) and sharks (Gateus metastomus
and Etmopterus spinax) (Kryvi, 1977) have an intermediate mito-
chondrial density and myofibrillar packing to red and white fibres.
The dogfish superficial fibres described by Bone (1978a) are distinct
from either red or white fibres in containing an inconspicuous M-
line, virtually no lipid, simple mitochondria, and a relatively poorly
developed T -system and SR.
INNERVATION AND ElECTROPHYSIOlOGICAl PROPERTIES
In dogfish, red fibres receive a number of terminations of the en-

grappe type derived from two separate axons. The motor axons
either pass into the fibre from the myosepta! ends or run across the
surface of the muscle innervating a number of different fibres (Fig. 5 ).
84
/\.
I
*-
B
-~
c ~
FIG. 5. A diagrammatic representation of the different patterns of motor innervation (left)

and modes of activation (right) of fish muscle fibres. Traces of electrical activity show
stylised responses to depolarizing pulses or nerve stimulation. Vertical calibration bars
represent 20 mV, and horizontal bars 5 ms. Zero potential is indicated with a horizontal
line. (A) All fish red fibres examined are multiply innervated and are activated by junction
potentials (see Barets, 1961). (B) White fibres in elasmobranchs,dipnoans and certain tele-
osts (see Fig. 6) are focally innervated at one myoseptal end. Motor terminations are of the
en-grappe type. Focally innervated fibres show a propagating action potential overshooting
zero potential by around 20 mV (seeHagiwara & Takahashi, 1967). (C) Multiply innervated
white fibres are found in all acanthopterygians and certain other fish groups (see Fig. 6).
Each muscle fibre is innervated by several different motor axons. Stimulation of the nerve
supply results in two distinct kinds of electrical response: (1) junction potentials; and (2)
spike potentials (seeHudson, 1969).
From electrophysiological measurements of membrane space con-

stants Stanfield (1972) concluded that motor terminals were around
150-200.um apart. Subjunctional folds are present on terminals of
both superficial and outer and inner red fibres of Scyliorhtnus (Bone,
1972). Typically, red fibres do not produce action potentials in
response to depolarizing pulses (Stanfield, 1972). Thus in this respect
and in relation to their innervation dogfish red fibres resemble the
true slow or tonic fibres of amphibians. However, Stanfield (1972)
found that eight out of 27 red fibres examined showed a significantly
large inward sodium current on depolarization to suggest they were
capable of propagating an action potential. Of the remaining fibres six
showed no inward Na current and the others only a small inward
Na current. Thus althoug:h it is likelv that red fibres are normally
activated by junction potentials the electrophysiology of fish slow

fibres warrants further investigation. The pattern of innervation of
red muscles in other elasmobranchs and indeed in dipnoans, holo-
steans, chondrosteans and teleosts would appear to be broadly similar
to that described from dogfish~Bone, 1964).
r White muscle fibres in dogfish are innervated by large diameter
axons which run in the myosepta and give rise to basket-Iike en-
plaque end-formations at one end of the fibre (Bone, 1964, 1966).
Each muscle fibre is innervated by two separate axons which fuse to
form a single end-plate (Bone, 1964, 1972). In dogfish, the two
motor terminals contaiQ vesicles of different size ranges, 50 nm and
100 nm (Best & Bone, 1973). The significance of this dual innervation
is unknown since only acetyl cholinesterase has been demonstrated
in sub-synaptic folds (Pecot-Dechavassine, 1961). Bone (1978a) has
calculated that each motor unit in dogfish white muscle contains
around 50-100 fibres. In a study of several species of tropical sting-
ray Hagiwara & Takahashi (1967) found that white fibres showed
typical over-shooting spike-potentials on depolarization. Thus white
fibres of elasmobranchs resemble frog fast twitch fibres. In some
elasmobranchs, for example Torpedo, the more superficial white
fibres receive basket-Iike endings to the mid-region rather than the
ends of the fibre (Bone, 1964).
The innervation of white muscles in chondrosteans, holosteans and
dipnoans has been less studied but appears to resemble that of elas-
mobranchs (Fig. 6) (Bone, 1964). However, among teleosts another
type of innervation occurs and focally innervated white muscles are
only found among the more taxonomically primitive groups (Fig. 6).
Indeed, Bone (1970) has suggested that the type of innervation may
even serve as a taxonomic character. No acanthopterygians have
focal innervation and of the orders which are considered to be
primitive on other grounds, for example the Salmoniformes, only the
Salmonidae are multiterminally innervated (Bone, 1970). Interest-
ingly, orders such ,as the Osteoglossiformes and Ostariophysi also
contain families with both types of innervation. For example within
the Osteoglossiformes which comprise freshwater butterfly fish
(Pantodontidae), feather backs (Notopteridae) and mooneyes (Hi-
odontidae), only Hz.odon has terminal innervation (Bone, 1978a).
Thus in the majority of the 20,000 teleosts, including the Perci-
formes and Cypriniformes which together account for around four-
fifths of all the species, the white fibres are multiply innervated.
Branches of the spinal nerves run in the myosepta and fan out
across the surface of the myotome to form a diffuse network such
that each fibre receives numerous nerve terminals (Barets, 1961 ;
~
MAMMALS
BIRDS
REPTILES
AMPHIBIANS
-=:.I'
y ~
~ ~~
--,
..a~
.Rhl.' ~
_tiM C,
~ ,o,
~~
..W- --~ ~ "!00-'
"--I~~
CHONDROSTE' HOLOSTI' TILEOSTE'
, , , I' I'
~I~
OSTEICHTHYES
.CHONDRICHTHYES-
r;:;;;;L-
~l
AGNATHA
FIG. 6. Distribution of focal and multiterminal innervation among fast muscles of verte-
brates. Only representatives of the teleosts have multiterminal innervation. Taxonomically
primitive teleosts (lower box) have focal innervation. The middle box contains orders such
as the Osteoglossiformesand Salmoniformes containing families with both focal and multi-
ply innervated white fibres. This list is not intended to be comprehensive.SeeBone (1964,
1970). Teleost orders with taxonomically advancedfeatures have exclusively multiple inner-
vation (upper box). Land vertebrates have single end-plates as do dipnoans, elasmobranchs,
chondrosteans,holosteans, lampreys and hagfish.
Bone, 1~64) (Fig. 5). The end-plate formations have been variously
described as consisting of small rings or loops as in the tench (Barets,
1961) or as being multiple and made up of numerous separate neuro-
fibrillar annuli, e.g. Myoxocephalus scorpius (Hudson, 1969). Nerve
terminals are usually embedded in the sarcolemma and subjunctional
folds are absent (Nishihara, 1967). In Myoxocephalus, the short-
homed sculpin, Hudson (1969) found that each fibre receives inner-
vation from as many as five axons from each of four spinal nerves.
The number of terminals on each fibre ranges from eight to 22 with
an average of 14 about 0.7 mm apart. Hudson considered that each
end-plate is derived from a separate axon while others have con-
sidered that fibres are also multiply innervated by the same axon as
is the case with red fibres (Barets, 1961). Hudson (1969) calculated
that each abdominal myotome in the sculpin consists of 12 motor
units all of a considerable size.
There have been relatively few studies of the electrophysiological
properties of multiply innervated fast muscles (Barets, 1961; Hidaka
& Toida, 1969; Hudson, 1969). Hudson (1969) found that electrical
stimulation of spinal nerves elicits two kinds of electrical response,
namely spike potentials resulting in a fast twitch, or junction poten-
tials leading to a graded local contraction by the muscle. The typical
response to supramaximal nerve stimulation is an all-or-none spike
potential overshooting zero-potential by as much as 20 m V. Depolar-
ization of the membrane occurs in two phases. Duration of the fast
phase of the spike potential is of the order of 1.5-2.5 m S-I at 12C
(Hudson, 1969). Variation in stimulus intensity below maximal
results in junction potentials the amplitude of which can be quan-
titized in discrete steps providing evidence for innervation by several
different motor axons. Generally, Hudson found that junction poten-
tials did not exceed 35 m V and that in fresh preparations spike po-
tentials often arose from a single junction potential. However, in a
proportion of cases, particularly in older preparations, only junction
potentials could be elicited. At present, it is not possible to conclude
whether white fibres can be activated .n vivo in the absence of spike
potentials. Clearly, the electrophysiological properties ofpolyneuron-
ally innervated myotomal_muscles are worthy of further study.
The few multi terminally innervated fin muscles that have been
investigated appear to be similar to myotomal muscles (Bergman,
1964; Nishihara, 1967). Fin muscles may well provide a convenient
nerve-muscle preparation for investigating the combined electrical
and mechanical responses of polyneuronally innervated fibres.
88 Ian A. Johnston
MECHANICAL PROPERTIES
In spite of the separation of fish fibre types into different positions

within the myotome there have been very few studies of their con-
tractile properties. The complex fibre orientation and myoseptal
insertion of fish trunk muscles make such studies technically difficult.
In order to obtain preparations in which the fibres run parallel it is
necessary to utilize either single or small bundles of fibres. Fin, jaw
and sound-producing muscles provide more suitable whole muscle
preparations and have been the subject of a limited number of studies
(Bergman, 1964; Hidaka & Toida, 1969; Vamamoto, 1972).
Bone & Johnston (in press) have compared the properties of
bundles of red and white fibres from the dogfish myotome. Both
fibres respond to a single supramaximal stimulus; white fibres giving
a fast twitch (half-time peak tension: t, "" 20 ms) and red fibres a
slow contraction (t, "" 100 ms). On multiple stimulation, fused
tetani are produced at frequencies above 8 Hz. Twitch-tetanus ratios
of around 0.5 occur at 5 Hz and 10 Hz for red and white fibres respec-
tively. Very different stimulation characteristics have 'been reported
for multiply innervated teleost muscle. Flitney & Johnston (1979)
studied red and white fibre bundles isolated from adductor operculi
muscles of Tilapia massambica. Red fibres from Tilapia only respond
at stimulation frequencies in excess of 5-10 Hz. Both fibre types
produce graded, fused tetani, reaching a maximum at 250-300 Hz.
Unloaded speeds of shortening are 2.6 L s-I for white and 1.5 L S-I
for red fibres at 18C (Flitney & Johnston, 1979). However, rate of
rise of tension during supramaximal stimulation at 200 Hz was 6.5
times greater for white than for red fibres.
The responses of fibre bundles to different stimulation frequencies
for (a) the focally innervated white fibres of the cuckoo ray Raja
naevus and by (b) the polyneuronally innervated myotomal fibres of
the cod Gadus marhua L. are shown in Fig. 7. Typical tetanic fusion
frequencies on multiple stimulation are 5-10Hz for skate and 40-
50 Hz for cod. Maximal tensions require stimulation in excess of
200 Hz for cod and only 20 Hz for skate. The rate of tension devel-
opment is also frequency-dependent. Alexander ( 1969) has calculated
that the complex geometry of white fibres results in very little short-
ening ( "" 3% Lo) , even at maximum body flexure. I t seems likely that
the rate of tension development for multiply innervated fibres in viva
may be limited as much by the muscles membrane properties as by
its maximum speed of shortening.
Structureand Functionof Fish Muscles 89
,
J ""--
2Hz 5 Hz 10 Hz
\
, \
--
20Hz TWITC H
CUCKOO RAY
COD
FIG. 7. Isometric contraction of bundles of white muscle fibres at different stimulation
frequencies. (Top) Cuckoo ray Raja naevus (Muller & Henle) pectoral muscle. (Bottom) Cod
Gadus morhua dorsal myotomal muscle. Stimulation voltage 6V I ms pulse width. Vertical
scalebar representstension 3kgfm2 .Horizontal scalebars represent 2s (cuckoo ray), 500 ms
(cod) (multiple stimulation) and for twitches 100 ms. Temperature 18C. Note the lower
tetanic fusion frequency and lower stimulation frequency required to elicit maximum ten-
sion in ray compared to cod muscle. Mter Johnston (I980a).
1
A full understanding of these differences in the modes of activation
of fast fibres from different groups of fishes must await mechanical
studies with innervated single fibre preparations.
REGULATION OF MUSCLE CONTRACTILITY
Some features of the regulation of contractility in fish skeletal muscle

are ilIu!ltr3ted in FiQ". R. Ten!lion develonment. ri!le!l 3!1 3 f1lnction of
~
tJZ:::
CNS
FIG. 8. The control of contractility in fish muscle. Abbreviation: CNS, central nervous
system; SR, sarcoplasmic reticulum; CBP, cytoplasmic calcium binding proteins; CT, cal-
cium transient; PK, Ca2+-dependentprotein kinase. Factors modulating force production
include: (I) The number and frequency of motor units activated. (2) Neurotransmission.
(3) The muscle action potential (or distributed depolarization) is t.ransmitted to the SR via
the T-tubule system causing releaseof bound calcium. (4) This results in a transient increase
in free calcium from 0.1 to 10JlM. (5) The duration of the calcium transient is thought to
be reduced in fast muscles by the presence of high concentrations of cytoplasmic calcium
binding proteins (parvalbumins), see Fig. 9. (6) Calcium ions activate (a) muscle contraction
and (b) glycogen breakdown by direct binding effects to troponin C and phosphorylase
kinase respectively. There is also evidence that force production can be modulated by myo-
sin phosphorylation through a specific Ca2+-activatedmyosin light-chain kinase. (7) In slow
mammalian muscles calcium uptake into the SR is modulated by a cytoplasmic factor
thought to be a Ca2+-dependentprotein kinase. Slow muscles of salmonid fishes do not
appear to have such a mechanism (McArdle & Johnston, in press). The extent to which this
is true of other speciesis unknown. Incubation of Tilapia red and white musclesin ringers
containing zero calcium or veraparnil (5 X 10~5) leads to a rapid and reversible loss of
tension (Flitney & Johnston, 1979). It appears, therefore, that fish muscleshave a require-
ment for extracellular calcium. Whether Ca2+crossesthe sarcolemma or remains bound to
sites on the outside is unknown.
myoplasmic free calcium concentration within the range 0.1 to

10 .uM. In multiply innervated fibres the release of calcium from the
SR is dependent on the degree of depolarization of the muscle mem-
brane which is in turn determined by the number of motor neurones
activated and their firing frequency. In fish white but not red fibres
cytoplasmic calcium binding proteins (parvalbumins) play an import-
ant role in regulating free calcium concentrations (Gerday & Gillis,
1976; Pechere, Derancourt & Harech, 1977).
Parvalbumins are found in all vertebrate fast muscles but occur in
particularly high concentrations in fish white fibres (-15% soluble
proteins) (Le Peuch, Demaille & Pechere, 1978). Characteristically
they are acidic proteins of low molecular weigh t ( 11 ,000-12,000
daltons) which can bind 2-g atoms Ca2+/mole (Pechere, Capony &
Demaille, 1973). Sequence studies have shown strict conservation of
the amino acid residues at the Ca2+-binding sites and a high degree
of homology with other muscle calcium binding proteins, troponin
C, myosin P light chain and calmodulin (Collins, 1976; Perry, 1979).
In the metal-free form parvalbumins are able to inhibit Mg2+ Ca2+
myofibrillar ATPase activity by chelating Ca2+ ions bound to trop-
onin C (Pechere, Derancourt et at., 1977). Calcium bound to parval-
bumins can be exchanged and accumulated by SR vesicles (Gerday
& Gillis, 1976). The relative binding constants of Ca2+ for troponin
C and parvalbumins are Kd 's 10-6 M and 10-7 M respectively (Ben-
zonana, Capony & Pechere, 1972; Potter & Gergely, 1975). The
current view is that parvalbumins function in aiding rapid relaxation
(Gerday & Gillis, 1976; Pechere, Derancourt et at., 1977). Since
parvalbumins occur in molar excess over TNC in fish muscles Ca2+-
released by the SR causes only a transient activation of crossbridges
as Ca2+rapidly becomes bound within the cytoplasm. Thus relaxation
occurs before all the Ca2+is resequestered within the SR (see Fig. 9).
In some fish the sarcoplasmic reticulum occupies a somewhat
similar proportion of fibre volume in both fast and slow fibres (e.g.
Patterson & Goldspirik, 1972; see also Table III).
Evidence has been obtained that Ca2+-uptake in mammalian slow
but not fast muscles is regulated by a Ca2+-dependent protein kinase 1
which phosphorylates components of the pump necessary for trans-
port. Although sarcoplasmic reticulum isolated from red and white
muscles of rainbow trout has a somewhat different protein compo-
sition and it does not appear to require protein kinases or cAMP for
full activation (McArdle & Johnston, in press). The extent to which
this is true for other species and represents a phylogenetic difference
between fishes and mammal~ i~ 1Inknn~-
92 Ian A. Johnston
FIG. 9. Diagrammatic representation of the role of parvalbumins in Ca2+ movements in fish

fast muscle fibres. The width of the lines represents the relative magnitude of the Ca2+
fluxes. After Pechere, Derancourt et at. (1977).
Activation of myosin crossbridges in fish muscle is achieved

through direct effects of Ca2+-binding to troponin C as in other
vertebrates (Lehman & Szent-Gyorgyi, 1975). In addition, phos-
phorylation of myosin through a specific Ca2+-activated myosin light-
chain kinase may lead to a modulation of force production (see
Perry, 1979).
FIBRE RECRUITMENT DURING SWIMMING

l
The recruitment of different fibre types with increasing speed has
been studied in dogfish (Bone, 1966), rainbow trout (Hudson, 1973),
carp Uohnston, Davison et at., 1977), herring (Bone et at., 1978),
skipjack tuna (Rayner & Keenan, 1967; Brill & Dizon, 1979), bass
(Freadman, 1979, saithe Uohnston & Moon, 1980a) and brook trout
(J ohnston & Moon, 1980b ). This represents only a small proportion
of the 20,500 species of living fishes. However, at present the results

are consistent with a division in the pattern of fibre recruitment be-
tween different groups of fishes according to the type of innervation
of the fast motor system. Focally innervated fast fibres appear only
to be recruited for burst activity. For example, electromyographical
studies in the Pacific herring show that only red fibres are recruited
at speeds that can be sustained for several hours. Higher speeds ( 5
body lengths/s) result in the recruitment of white fibres and fatigue
of the fish within a further 1-2min swimming (Bone et at., 1978).
Qualitatively similar results have been obtained for the dogfish
(Scyliorhinus canicula) .which also has focally innervated white
fibres (Bone, 1966). In contrast a number of studies have shown
that both red and white fibres are recruited at sustainable swimming
speeds in species with multiply innervated fast muscles (Fig. 10)
(Hudson, 1973}; Johnston, Davison et at., 1977; Bone et at., 1978).
.~- ..~-
-#'~ ; ~ .~ ~ ~ ~ ~
-~ ~ ~w
A
""'-"'-
-
-w ~~- .}- , ,.. w
FIG. 10. Recruitment of fibre types of the brook trout (Salllelinus fontinalis Mitchill)
during steady swimming. (Top) Shows insertion of EMG electrodes in red (r) and white
(w) muscles. (Bottom A) Top two traces, EMGs recorded from red and white muscle regions
during steady swimming at 1 lengthfs. Note potentials are only recorded from the red
muscle layer. Lower trace, a burst of electrical activity in white muscle associated with a
change of position in the swimming chamber during the same experiment. (Bottom B)
Recordings of EMGs from red and white musclesat a steady swimming speedof 3 lengthsfs.
Brook trout are able to maintain this speedindefinitely. Horizontal scalerepresents 500 rns.
V~ti,..aI scalereDresents1 mv. {From Johnston & Moon, 1980b.)
94 Ian A. Johnston
For example the threshold speed for recruitment of white fibres is

0.8-1.9 lengths's in saithe Oohnston & Moon, 1980a), and 2.0
lengths's in carp Oohnston, Davison et al., 1977). Somewhat higher
speeds for recruitment of white fibres have been reported in striped
bass (Morone saxatilis), 3.2 lengths's, and bluefish (Pomatomus
sultatrix), 4.5 lengths's (Freadman, 1979). Thus in some species with
multiply innervated fast muscles there may be a secondary reversion
to the more primitive pattern of fibre recruitment such as is found in
the dogfish. Recent studies have shown a wide range of aerobic ca-
pacities for teleost white muscles between species, presumably reflec-
ting different degree& of involvement of this fibre type in sustained
swimming Oohnston & Moon, 1980b).
Only in carp have electromyographs (EMGs) been recorded from
the pink muscle layers. In this study it was shown that the order of
recruitment of fibre types with increasing speed is red muscle > pink
muscle > white muscle Oohnston, Davison et al., 1977).
METABOLISM
EnzymeActivities of Redand White MuscleFibres

Detemlinations of maximal in vitro activities of enzymes can be used
to assessthe metabolic capacities of different muscles. In the case of
non-equilibrium enzymes such information gives a useful semi-
quantitative estimate of maximal metabolic flux (see Newsholme &
Start, 1973; Newsholme, Zammit & Crabtree, 1978). Enzymes
catalysing non-equilibrium reactions can be identified by measure-
ments of mass action ratios and they usually have among the lowest
activities in the pathway, being regulatory steps in metabolism.
Enzymes catalysing equilibrium reactions only provide qualitative
infomlation about the relative importance of particular metabolite
pathways and the principal fuels supporting activity. Enzyme studies
of fish muscle have recently been reviewed (Zammit & Newsholme,
1979;Johnston, 1980b). Table IV gives the maximaltn vitro activities
of some enzymes of energy metabolism from the fast and slow
muscles of the brook trout measured under optimal conditions of
pH, substrates and co-ions U ohnston & Moon, 1980b ). Typically
white muscles have a higher glycolytic potential (phosphorylase,
PFK activities) and lower oxidative capacity (citrate synthetase) than
red muscles.
Barany (1967) has demonstrated for a wide range of vertebrate
muscles that mvofibrillar ATPase activities parallel the unloaded
TABLE IV
Activities of some key enzymes of energy metf,lbolism and metabolite concen-
trations in the red and white muscles of brook trout (Salvelinus fontinalis
Mitchill). Data from Johnston & Moon (198Ob) and Walesby & Johnston
(198Gb)
Enzyme Activities
(j.lmol substrate/g dry wt./min)
Mg2+ Ca2+ myofibrillar ATPase+
Creatine kinase
Adenylate kinase
5' AMP aminohydrolase
Glycogen phosphorylase
Hexokinase
Phosphofructokinase
Pyruvate kinase
Lactate dehydrogenase
Cytochrome oxidase
Citrate synthetase
3-0H Acyl coA dehydrogenase
Metabolite concentrations
(J1mol/gdry wt.)
ATP 2.9 6.1
ADP 0.4 0.6
AMP 0.2 0.2
Pi 3.8 7.1
Phosphoryl Creatine 9.3 25.7
Activity expressed as IJ.mol Pi releasedfmg myofibrillar proteinfmin.
speeds of shortening. On this basis, white muscles of the trout and

other species studied (see Table I) are around two to five times as
fast as red muscle. Activities of enzymes responsible for maintaining
ATP supply during contraction such as creatine kinase, adenylate
kinase and 5' AMP amino-hydrolase parallel those of myofibrillar
A TPase. 5' AMP amino-hydrolase is particularly important in fast
muscles since it catalyses the deamination of AMP to IMP thus
shifting the equilibrium of adenylate kinase in favour of ATP pro-
duction. It has been calculated that in fatigued muscles up to half of
the ATP for contraction is supplied by this pathway.
In a study of a large number of invertebrate and vertebrate species
Beis & Newsholme (1975) found that muscles with the lowest ATPI
AMP ratios usually have the lowest rate of ATP utilization and the
least variation in energy requirement. The ATP/AMP ratios in the red
96 Ian A. Johnston
and white muscles of brook trout (R, 18.6; W, 38.3} and tuna (R,
26.3; W, 61.1} reflect the relative activity levels of these muscles and
lend support to this concept (Table IV}.
Both metabolite concentrations (Freed, 1971; Walesby & John-
ston, 1980b} and enzyme activities can be modified by environ-
mental factors such as temperature, activity and nutritional status
(seeJohnston, 1980b }.
BurstSwimming
The type of locomotory activity best understood is burst swimming.
Maximum swimming' sp~eds can only be maintained for relatively
few tail-beat cycles and are approximately 26 lengths/s for 10 cm fish
and 4 lengths/s for 1 m fish (Wardle, 1975). Burst swimming is
accompanied by an extremely rapid activation of glycolysis in white
muscle. In trout this results in the utilization of around 50% of muscle
glycogen stores in 15 s which is equivalent to a flux of 40.umol
glycogen derived glucose/kg/s (Stevens & Black, 1966). There is near-
quantitative conversion of muscle glycogen to lactate which may be
retained in the muscle for several hours following the cessation of
exercise (Wardle, 1978). Lactate levels of 59 (trout) and 69 mmol/kg
(skipjack tuna) have been recorded in white muscles following 1-2
min burst swimming (Black, Robertson & Parker, 1961; Guppy et
at., 1979). Recovery of white muscle lactate to pre-activity states
may require up to 18 h in some species (Black, Robertson et at.,
1961) bu tis usually complete wi thin 30-60 min in red muscle
(Johnston & Goldspink, 1973a).
Changes in metabolite concentrations between rest and maximal
activity in tuna white muscle are illustrated in Fig. 11. Burst swim-
ming is associated with a large decrease in phosphoryl creatine (90%)
and ATP (53%) and a small increase in AMP concentrations (22%)
(Guppy et at., 1979: table 2).
In the carp Driedzic & Hochachka (1976) observed a 48% decrease
in the total adenylate pool and an essentially 1 : 1 increase in IMP
and NH4 due to the deamination of AMP by 5' amino-hydrolase (see
above). it is possible that this is one source of the anaerobic NH4
production which has been frequently observed following enforced
exercise in fish (Kutty, 1972).
The regulation of glycogenolysis in fish white muscle is illustrated
in Fig. 12. N on-equilibrium or regulatory steps in anaerobic glycolysis
include phosphorylase, phosphofructokinase and pyruvate kinase
(Newsholme & Start, 1973). There is an interesting phylogenetic
difference in the control of glycogen breakdown between fish and
Gly 100 -
PCr
50 - 10
REST G6P ATP
Glu
F6P FDP Pyr lac
BURST 50 -
3-
I 100 -
FIG. 11. Metabolite concentrations in freeze-clamped white muscles of skipjack tuna
Euthynnus pelamis during rest and burst swimming activity (data from Guppy et at.,
1979: table 2). Abbreviations: Gly, glycogen; Glu, glucose; G6P, glucose-6-phosphate;
F6P, fructose-6-phosphate; FDP, fructose 1, 6-diphosphate; Pyr, pyruvate; Lac, lactate;
PC, phosphoryl creatine; ATP, adenosine 5'-triphosphate. Units of concentration IJmolg
wet weight muscle-l. Dark shading represents data from resting fish and light shading
burst swimmin~.
mammalian muscles (Fischer, Blum et at., 1975). While rabbit muscle

phosphorylase kinase is rapidly activated or inhibited by cAMP
dependent protein kinases or specific phosphatases, the dogfish
enzyme depends only on Ca2+ for its activity (Cohen, Duewer &
Fischer, 1971; Fischer, Blum etat., 1975; Fischer, Alabaetat., 1978).
Indeed, there is no production of cAMP in response to noradrenaline
in dogfish white muscle (Fischer, Blum et at., 1975). The lack of a
hormonal mechanism for activating glycogen breakdown in dogfish
white muscle may be related to the relatively poor circulation through
this tissue during maximal activity. In vitro phosphofructokinase is
known to be activated by substrates, AMP, ADP, Pi and NH4 and 1
inhibited by phosphoryl creatine, ATP and citrate (Mansour, 1972).
Substrate cycling between F -6-P and FDP by the coupling of the
PFK and FDPase reactions is thought to provide a mechanism for
increasing the sensitivity of F -6-P phosphorylation to changes in
AMP (Newsholme, 1976) (Fig. 12).
Increases in AMP concentration activate PFK and inhibit FDPase
resulting in a proportionally larger increase in glycolysis than is
possible in the absence of substrate cycling. According to this scheme
DEPOLARIZATION
J,
Ca-RELEASE
.1.
GLYCOGEN
~
A PhOS. a Phos b.
GIP /
1~
1~
F6P
B
PFK
AMP
-'r:Bp'.
1L
TP
1l r-- HAD ,
1.3DP~ HADH
FBP
1l
1~
1l
PEP
PYK
FIG. 12. Control of anaerobic glycogenolysis in fish white muscle. Regulatory steps include
(A) glycogen phosphorylase, (B) phosphofructokinase and (C) pyruvate kinase (seetext for
details). Abbreviations: Phos, phosphorylase; GIP, glucose-l-phosphate; PFK, phospho-
fructokinase; FBP, fructose 1, 6-biphosphate; AMP, adenosine5' monophosphate; TP, triose
phosphates; NAD, f3-nicotinamide adenine dinucleotide; NADH, tf-nicotinamide adenine
dinucleotide reduced form; 1, 3 DPG, 1, 3 diphosphoglyceric acid; PEP, phospho(enol)
nvnlv"t.. .PYK nvnlv"t.. kin,,",,- Oth"T ahhreviation" are 2iven in the le2end to Fi~. 11.
small changes in ATP lead to proportionately larger changes in AMP

through the adenylate kinase reaction. Thus, in general, the higher
the initial ATP :AMP ratio the greater the increase in AMP for a given
breakdown of ATP and the greater the stimulation of glycolysis
(Newsholme et at., 1978). An interesting feature of the control of
glycolysis in fish muscles is the presence of a regulatory pyruvate
kinase. In vitro pyruvate kinase is inhibited by ATP and alanine and
activated by substrates and FDP (Somero & Hochachka, 1968;
Johnston, 1975). Regulatory pyruvate kinases are associated with
muscles in which there is a rapid and dramatic increase in glycolysis
between standard and burst activity. For example modulator-sensitive
pyruvate kinase occurs in the locomotory muscles of diving mammals
such as whales but not the limb muscles of terrestrial mammals
(Hochachka & Storey, 1975). The observed changes in metabolites
and Ca2+ release from SR during burst swimming are sufficient to
cause a rapid activation of glycolysis through the known regulatory
mechanisms described above (Figs 11, 12).
SteadySwimming
The metabolism of muscles during steady swimming is much less well
understood. One recurring problem with studies of metabolism of
sustained swimming has been the failure of many investigators to
control the activity state of fish either before or during the exercise
period. It is essential to know the exact swimming speed in lengths/s
and to control as far as possible the condition of the fish prior to its
introduction to the swimming chamber (e.g. temperature, nutritional
status, level of stress etc.). In addition the adaptive variation observed
within fish populations and particularly between species means that
it is often impossible to reach general conclusions about metabolism.
In general, fish can increase their oxygen uptake by a factor of
10-15 times between rest and maximal activity (Bennett, 1978).
Values for maximum oxygen consumption are comparable to the
basal levels for birds and mammals and are in the range 190-644 ml
kg-1 h-1 (see Jones & Randall, 1978). Unfortunately, only frag-
mentary data are known for tuna which might be expected to have
aerobic activity levels more comparable to homeotherms. It seems
likely that red muscle receives a significant proportion of the cardiac
output during steady swimming. This is particularly true for species
in which red muscles alone support sustained activity (e:g. elasmo-
branchs, dipnoans, primitive teleosts). Since red fibres constitute a
small fraction of the trunk musculature (5-10%) they undoubtedly
possessa highly active aerobic metabolism. Indeed, the mitochondrial
densities of fish red fibres are greater than those of similar fibres in
100 Ian A. Johnston
TABLE V
Maximal activities of enzymes of fatty acid and ketone body oxidation in fish
red muscle. Activities expressed as p.mol substrate utilized, g wet weight muscle-1
min-I
- - -
<0.01 (),07 3.7
<0.01 (),75 1.8
<0.01 (),60 4.5
1.3 ),01 0.2
'0.37 ),01 0.54
0.64 ).01 0.1
Data from Zammit & Newsholme (1979).
mammalian limb muscles (see Table II). Little is known about the
regulation of the tricarboxylic acid cycle in fish ( for a review see
Driedzic & Hochachka, 1978). Lipid is known to be an important
fuef during steady swimming particularly in those species which
undertake a spawning migration (see Bilinski, 1974),. There are indi-
cations that both lipolysis and the transport of fat differ significantly
between fish and mammals (see Bilinski, 1974). For example, it has
been reported that the activation of lipolysis in fish does not proceed
via cAMP-dependent protein kinases (Farkas, 1969). There are also
differences in the sites of storage and metabolism of lipid between
different fish groups. In elasmobranchs triacyl glycerol is stored in
the liver, whereas in teleosts a significant proportion is deposited
either in discrete stores in the viscera or dispersed throughout the
muscle fibres in adipocytes. Red muscles of teleosts contain high
activities of camitine palmitoyl transferase and triacyl glycerol lipase
but not 3-hydroxybutyrate dehydrogenase. The opposite situation is
found in elasmobranchs which have high activities of enzymes of
ketone body but not fatty acid oxidation (Zammit & Newsholme,
1979) (see Table V). Triacyl glycerol and non-esterified fatty acids
also occur in much higher concentrations in the plasma of teleosts
than elasmobranchs (Zammit & Newsholme, 1979). These differences
are augmented during starvation. Thus it seems likely that the most
important fat fuels are ketone bodies in elasmobranchs and fatty
acids in teleosts. Red muscles in salmonids can oxidize long chain
saturated fatty acids to CO2 at around ten times the rate of that of
white muscles Oonas & Bilinski, 1964; Bilinski, 1974). Similarly,
camitine palmitoyl transferase activities of teleost white muscles
are generally only 5% of that of red muscles (Crabtree & Newsholme,
1972). Thus it seems likely that oxidation of fats as fuels is much

more important in red than in white muscles even when the latter
are recruited for sustained activity.
Numerous studies have shown glycogen depletion during sustained
swimming in both the red and white muscles of teleosts (Pritchard,
Hunter & Lasker, 1971; Johnston & Goldspink, 1973a,b). However,
the pathways of carbohydrate metabolism utilized by multiply inner-
vated white fibres at sustained speeds are not known for any species.
Two basic possibilities exist: ATP generation could be aerobic using
either local glycogen stores or blood glucose, or largely anaerobic
resulting in the productiQn of lactic acid. For the latter case, a num-
ber of schemes have been proposed involving lactate-exchange with
other tissues to keep the fish in overall aerobic balance.
In a quantitative study of glycogen utilization in crucian carp
Johnston & Goldspink (1973c) found that glycogen utilization at
three lengths's was two to three times higher in red than in white
muscles. However, since red fibres only comprise 7% of the trunk
musculature they only account for 15-20% of the total glycogen
utilized at this swimming speed.
Crabtree & Newsholme (1972) have demonstrated a good corre-
lation between hexokinase activities in various muscles and calculated
maximum capacities for glucose oxidation. Table VI gives values for
red and white muscle hexokinase activities in various species. It can
be seen that the importance of aerobic glucose utilization is likely
to vary considerably between species for both myotomal muscle
types. White fibres in two species of trout and the skipjack tuna have
high hexokinase activities comparable to those of red muscle (Table
VI). Other evidence for a significant aerobic capacity in the white
muscles of these species is as follows. In rainbow trout the ratio of
mitochondria between red and white muscles is 8: 3 by number (Nag,
1972). Activities of citrate synthetase and cytochrome oxidase in
brook trout white muscle are 25-35% of that of red muscle a ohnston
& Moon, 1980b). Thus in at least trout, and possibly tuna, the
aerobic capacity of the white muscle is probably sufficient to sup-
port sustained activity and blood glucose may be an important fuel.
A number of early studies reported lactate accumulation two to
three times resting levels in various salmonids forced to swim at
sustained swimming speeds (Black, Bosomworth & Docherty, 1966).
These results may well reflect the presence of a generalized stressed
reaction in acutely exercised fish (see Wardle, 1978). Studies of trout
trained to swim in an exercise chamber for several weeks prior to
~xnerimentation show no net accumulation of lactate over rested
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fish for speeds up to at least four body lengths/s (.1ohnston & Moon,
1980b).
However, in many species it would appear that anaerobic path-
ways are important in providing ATP for sustained activity. For ex-
ample, Smit et at. (1971) have calculated that goldfish (Carassius
auratus) obtain 80% of their energy requirements anaerobically
during high speed sustained swimming. Further evidence for the
importance of anaerobic pathways at sub-maximal swimming speeds
comes from measurements of key enzyme activities following endur-
ance exercise training (see Johnston & Moon, 1980a,b). In contrast
to mammals, endurance ,exercise training in fish leads to an increase
in glycolytic enzyme activities with little change in overall aerobic
capacity of the muscles Uohnston & Moon, 1980a,b).
MetabolicFateof LactateProducedby the SwimmingMuscles

The metabolic fate of lactate produced during sustained and follow-
ing burst swimming, has been the subject of a large number of
papers. It is likely that a major part of the lactate produced during
exercise is oxidized to pyruvate (Bilinski, 1974). Bilipski & Jonas
(1972) have demonstrated that gills, liver, red muscle and kidney
are all able to oxidize 14C-lactate at high rates in vitro. Bone (1975)
has suggested that fish may be able to maintain overall aerobic
balance by transferring lactate produced by anaerobic glycogenolysis
in the white muscle to the gills and other peripheral sites for sub-
sequent oxidation. The extent to which fish liver can utilize lactate
as a gluconeogenic substrate is unclear. Black, Bosomworth et at.
(1966) concluded that the Cori cycle is of little importance in trout
since liver glycogen levels are not restored to normal even 24 h fol-
lowing burst swimming. However, recently it has been demonstrated
that eel hepatocytes convert lactate to glucose at high rates in vitro
(Renaud & Moon, 1980).
Wittenberger and co-workers have suggested that red muscle
operates a direct glucose-lactate exchange with white muscles
(Wittenberger & Diacuic, 1965; Wittenberger, 1973; Wittenberger,
Coprean & Morar, 1975 ) .This idea developed from a suggestion by
Braekkan (1956) that red muscle in fish is homologous to the liver
in higher vertebrates. The demonstration of a contractile function for
red muscle and the large diffusion distances between red and white
muscle masses rules out this hypothesis at least in its more extreme
forms. However, on the basis of a variety of indirect evidence it has
been proposed that red muscle does have a significant role in syn-
thesizing glucose from circulating lactate (see Driedzic & Hochachka,
Fed Starved
,
i
~
'0
E
c
~
-
Fed Starved Fed Storvod
-
F.d S,.,..d IV IV
FIG. 13. Activities of glycolytic and gluconeogenic enzymes in red and white muscles and
liver of fed and four-month-starved plaice (Pleuronectes platessa) (from Moon & Johnston,
1980). (Top) Activities (ILmol rnin-l 9 dry weight-l ) of hexokinase, glucose-6-phosphatase
(G-6-Pase) and p-nitrophenyl phosphatase (pNPPase). (Centre) Activities (ILmol min-I 9 dry
weight-l) of phosphofructokinase (PFK) and fructose-l,6 bisphosphatase (FDPase). (Bot-
tom) Activities (ILmol min-I 9 dry weight-1) of pyruvate kinase (PyK). Phosphoe-enol
pyruvate carboxykinase (PEP Ck) activities are given for the soluble (left) and bound (right)
fractions of liver (LV) and red muscle (RM). Note the very low activities in red muscle. No
activities of PEP Ck were detected in white muscle. In each case bars represent enzyme
activities in liver (left), red muscle (centre) and white muscle (right). Data represent mean
y ~F, nf .;y fi.h
1975; Wittenberger et at., 1975; Hulbert & Moon, 1978; Batty &
Wardle, 1979). For example, Batty & Wardle (1979) have calculated,
on the basis of in vivo 3H-glucose turnover experiments in plaice,
that the transport of glucose into the muscle following recovery from
exercise is insufficient to account for the observed rates of glycogen
formation. However, a significant gluconeogenic role for red muscle
is not supported by measurements of key enzyme activities O ohnston
& Moon, 1979; Moon & Johnston, 1980). Activities of pyruvate
carboxylase, PEP carboxykinase and glucose-6-phosphatase in plaice
are either absent or present at very low levels in red muscle compared
to liver, even under conditions of starvation which would be expected
to augment gluconeogenesis (Fig. 13). Whether gluconeogenesis
occurs in the red muscle of other species or whether the very low
enzyme levels in plaice red muscle are sufficient to account for some
glycogen syn thesis during a long recovery period ( 12 h) remains to
be seen.
Utilization of Muscle Proteins
Many species of fish undergo periods of seasonal starvation linked to

fluctuations in food supply (see Love, 1970). In fish that do not
store large quantities of lipid, white muscle myofibrillar proteins
serve as an important source of metabolic precursors during starvation.
For example, in plaice, after four months starvation white muscle
water contents increase from around 75 to 95% with a corresponding
loss of contractile proteins (Johnston & Goldspink, 1973b;Johnston,
1981). It seems likely that amino acids released from the muscles
during starvation are converted to glucose via gluconeogenic path-
ways in the liver and hence constitute an important fuel for muscular
activity under these conditions (Moon & Johnston, 1980).
Finally a number of authors have suggested that fish muscles are a
major site of amino acid oxidation. For example, glycine and histidine
together constitute around 50% of the free amino acid pool in the
muscles of salmonid fishes (Fontaine & Marchelidon, 1971). The
1
initial enzyme in histidine degradation is histidase, which is found in
high titres in the muscles of some fish but not mammals and has a
Km for histidine which is five times lower than the liver analogue
(see Driedzic & Hochachka, 1978). Wood, Duncan & Jackson (1960)
have suggested that histidine is oxidized in situ as an energy source
by salmon muscle during spawning migration. There is, however, as
yet little direct evidence for amino acid oxidation in fish muscles (for
a review see Driedzic & Hochachka, 1978).
106 Ian A. Johnston
ACKNOWLEDGEMENTS
The author's work is supported by grants from the Natural Environ-

ment Research Council, Science Research Council and Wellcome
Trust.
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Symp. zaal. Sac. Land. (1981) No.48.

Structure and Function of Fish Muscles

Adaptations for aquatic locomotion account for many of the special-

vertebrates (see Bennett, 1978). In general, the power requirements

metabolism in multiply innervated fast muscles remains one of the

A wide variety of body forms and modes of swimming have been

fish muscle. In other vertebrates, locomotory muscles contain a

Outer red 0.06 0.51

Outer white 0.55

The arrangement of fibre types of some representative teleosts is

trout there is a continuous distribution of white muscle fibre diam-

In some species another type of fibre occurs in an intermediate

There have been a number of recent quantitative studies of the fine

Fractional volume (%) occupied by sarcoplasmic reticulum and T-system in some

Sarcoplasmic reticulum T -system

Species Muscle Type

Salmo gairdnerib 5.1 13.7 0.10

Tonic Twitch Ton.ic Twitch

Slow Fast Slow Fast

Twitch Twitch Twitch Twitch

Guinea pigd,e 3.2 4.6 0.14 0.27

of the Z disc (Franzini-Armstrong & Porter, 1964; Kilarski, 1966;

a cart-wheel with spokes radiating to a small central hub of sarco-

INNERVATION AND ElECTROPHYSIOlOGICAl PROPERTIES

In dogfish, red fibres receive a number of terminations of the en-

FIG. 5. A diagrammatic representation of the different patterns of motor innervation (left)

From electrophysiological measurements of membrane space con-

activated by junction potentials the electrophysiology of fish slow

In spite of the separation of fish fibre types into different positions

REGULATION OF MUSCLE CONTRACTILITY

Some features of the regulation of contractility in fish skeletal muscle

myoplasmic free calcium concentration within the range 0.1 to

FIG. 9. Diagrammatic representation of the role of parvalbumins in Ca2+ movements in fish

Activation of myosin crossbridges in fish muscle is achieved

FIBRE RECRUITMENT DURING SWIMMING

of the 20,500 species of living fishes. However, at present the results

For example the threshold speed for recruitment of white fibres is

EnzymeActivities of Redand White MuscleFibres

ADP 0.4 0.6

AMP 0.2 0.2

Phosphoryl Creatine 9.3 25.7

Activity expressed as IJ.mol Pi releasedfmg myofibrillar proteinfmin.

speeds of shortening. On this basis, white muscles of the trout and

mammalian muscles (Fischer, Blum et at., 1975). While rabbit muscle

small changes in ATP lead to proportionately larger changes in AMP

Data from Zammit & Newsholme (1979).

1972). Thus it seems likely that oxidation of fats as fuels is much

MetabolicFateof LactateProducedby the SwimmingMuscles

Utilization of Muscle Proteins

Many species of fish undergo periods of seasonal starvation linked to

The author's work is supported by grants from the Natural Environ-

Alexander, R. McN. (1969). The orientation of muscle fibres in the myomeres of

Bone, Q. (1964). Patterns of muscular innervation in the lower chordates. lnt.

108 Ian A. Johnston

Hamoir, G. (1978). Differentiation proteinique des muscles striesblancs,jaunes

Johnston, I. A. & Moon, T. W. (I980b). Exercise training in skeletal muscle of

Mansour, T. E. (1972). Phosphofructokinase. CUlT. Top. CellRegul. 5: 1-46.

Webb, P. W. (1975). Hydrodynamics and energetics of fish propulsion. Bull.

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