AMER. ZOOL., 29:333-352 (1989)
Respiratory Gas Bladders in Teleosts:
Functional Conservatism and Morphological Diversity1
KAREL F. LIEM
Museum of Comparative Zoology, Harvard University,
Cambridge, Massachusetts 02138
SYNOPSIS. Respiratory gas bladders are found in the Osteoglossomorpha, Elopomorpha
and Euteleostei and are absent in the Clupeomorpha. All teleosts with respiratory gas
bladders share a common pattern of air ventilation: during the transfer phase gas is
transferred passively from the gas bladder to the buccal cavity. Subsequently, gas is expelled
during the active expulsion phase mediated by action of the geniohyoideus muscle causing
a positive pressure pulse in the buccal cavity. This is followed by an active intake phase
by action of the sternohyoideus muscle creating a negative pressure pulse, which is succeeded by an extensive compressive phase by action of the geniohyoideus muscle forcing
fresh air into the gas bladder. Saltatory evolution of gas bladders and their buccal pumps
seems to have proceeded by major transformations in structural design without appreciable
changes in the pattern of neural control. The hypothesis of symmorphosis in gas bladder
design is well corroborated by the independent evolution of accessory esophageal pumps
in three unrelated lineages. Evolutionary reversals (Primitive lung evolving into nonrespiratory hydrostatic swim bladder which subsequently reverts back to become a respiratory
gas bladder) have occurred repeatedly. Such reversed shifts are facilitated by the conserved
neuromuscular pattern during functional transformations. Experimental comparative evidence is offered for the notion that evolutionary innovations may involve the addition of
entirely new functions (respiratory) of a structural complex (gas bladder) while the original
functions (hydrostatic, hearing and sound production) are rigidly retained. The paucity
in Elopomorpha and absence in Clupeomorpha of respiratory gas bladders reflect the lack
of functional demands for new habits in the environment rather than the absence of
essential preexisting building blocks.
ically or permanently hypoxic habitats, in
which a premium was put on air breathing
capabilities (e.g., Randalls a/., 1981; Liem,
1987). In such habitats, survival depends
on the fish's ability to use atmospheric oxygen. In many teleosts inhabiting such environments (Table 1) gas bladders became
converted to respiratory lunglike organs
while simultaneously maintaining the original buoyancy function (Gans, 1970). This
paper examines how respiratory gas bladders are ventilated in the various teleostean lineages. Do the mechanisms of air
ventilation exhibit a pattern of diversity
paralleling the morphological diversity of
gas bladders? One of the major questions
in functional morphology is whether morphological diversity and specializations are
linked to matching functional features.
This study addresses this question by furnishing a functional morphological perspective of the respiratory gas bladders in
all major teleostean lineages. Can the
1
From the Symposium on Vertebrate Functional Mor- unequal representation and differing
phology: A Tribute to Milton Hildebrand presented at thediversity of gas bladders among teleostean
Annual Meeting of the American Society of Zoolo- lineages be explained as a stochastic pheINTRODUCTION
Gas bladders (air bladders, swim bladders) have evolved in numerous teleosts in
a great array of form, size and position
primarily in response to buoyancy requirements imposed by the aquatic habitat. Neutral buoyancy conveys an unquestionable
selective advantage to fishes with pelagic
life habits (Steen, 1970). Highly specialized
devices in the form of such engineering
marvels as the red glands or rete's have
evolved independently in many representatives of three of the four major lineages
(Alexander, 1966; Lauder and Liem, 1983).
The repeated occurrence of these specialized regulatory mechanisms in unrelated
teleostean lineages testifies to the effectiveness of the selection forces favoring
neutral buoyancy in the aquatic habitat.
During their evolutionary diversification
various teleost lineages penetrated period-
gists, 27-30 December 1986, at Nashville, Tennessee.
333
334
KAREL F. LIEM
nomenon or is it the result of intrinsic
(historical) and extrinsic (environmental)
factors? By casting this functional morphological analysis in a comparative mold it
may gain an evolutionary perspective of
respiratory gas bladders which has eluded
previous studies because they did not integrate sufficiently the morphological, functional, and comparative aspects.
MATERIALS AND METHODS
The respiratory gas bladders and associated buccal pumps have been analyzed
by high speed light movies, high speed
cineradiography, electromyography, and
by Millar Mikro-Tip Catheter Pressure
Transducers. For details of the procedures
the reader is referred to Deyst and Liem
(1985).
Living specimens of Amia calva, Arapaima gigas, Pantodon buchholzi, Notopterus
chitala, Gymnarchus niloticus, Hoplerythrinus
unitaeniatus, Gymnotus carapo, and Pangas-
der in Amia exhibits the most primitive
evolutionary state, and is hypothesized to
resemble the ancestral condition for the
Teleostei. Amia has both well developed
gills and a respiratory gas bladder with
alveolar walls containing sheets of striated
muscle covering all except the dorsal aspect
of the bladder (Johansen et al., 1970). A
recent study on the muscular basis of aerial
ventilation in Amia (Deyst and Liem, 1985)
revealed that ventilation proceeds by the
action of a specialized pulse pump resembling that of the lungfish Protopterus.
New data and analytical methods make
it necessary to reappraise the earlier findings (Deyst and Liem, 1985) on the gas
bladder of Amia. Aside from a critical reappraisal, I will provide a more comprehensive and detailed functional morphological
foundation which can be used in comparative biology of the more derived taxa of
the apomorphic sister group of Amia, the
Teleostei.
ius sutchi have been studied. All are deposited as voucher specimens in the Museum The pattern of ventilation in Amia
of Comparative Zoology (MCZ).
We can distinguish four phases in the
For anatomical studies the following pattern of ventilation of the respiratory gas
specimens of the MCZ have been studied: bladder:
Megalops cyprinoides (MCZ 34181); Ara(1) The transfer phase (Fig. 1: 1, 2). Durpaima gigas (MCZ 46854); Heterotis sp. ing this phase air flows from the gas blad(uncatalogued); Pantodon buchholzi (MCZ der into the buccal cavity. This transfer can
52921); Gymnarchus niloticus (MCZ 48574); proceed either passively or actively. Passive
Notopterus chitala (uncatalogued); Erythri- transfer results from a hydrostatic pressure
nus erythrinus (MCZ 29997); Hoplerythrinus decrease in the cranial region of the bladunitaeniatus (MCZ 58010); Lebiasina bimac- der as the fish raises its head toward the
ulata (MCZ 30939); Piabucina festae (uncat- surface. As the sphincter of the glottis
alogued); Umbra limi (MCZ 60450); Gym- relaxes, air passes from the gas bladder to
notus carapo (MCZ 45189); and Pangasius the buccal cavity. As evident from the elecsutchi (uncatalogued).
tromyographic profile (Fig. 2) passive
transfer is not accompanied by muscular
T H E PRIMITIVE RESPIRATORY GAS
activity except for that of the epaxial musBLADDER IN AMIA: A REAPPRAISAL
cles which are responsible for raising the
Amia is the only living halecomorph fish head toward the surface, but this occurs in
representing the primitive (plesiomorphic) active transfer, too (Fig. 2). In sharp consister lineage of the Teleostei (Lauder and trast active transfer is always accompanied
Liem, 1983). As such it occupies a key evo- by activity in the sternohyoideus muscle
lutionary position. It is therefore impor- (Fig. 2), which lowers the buccal floor (Lautant to describe the mechanism in Amia as der, 1980) thereby enlarging the buccal
accurately and as thoroughly as possible. I cavity. Expansion of the buccal cavity lowpresent a description of the ventilatory ers the mouth pressure to below that in the
mechanism of Amia as a baseline which will gas bladder and the air is drawn into the
serve as an outgroup in subsequent com- mouth.
parative studies. The respiratory gas bladIt is hypothesized that both passive and
335
RESPIRATORY GAS BLADDERS
TABLE 1. Occurrence of respiratory gas bladders in teleosts.
Osteoglossomorpha
Elopomorpha
Clupeomorpha
Euteleostei
Arapaima gigas
Helerotis niloticus
Pantodon buchhohi
Gymnarchus niloticus
Xotopterus kapirat
Xotopterus chitala
Xotopterus notopterus
Xenomystus nigri
Megalops cyprinoides
Mega lops atlanticus
None
Erythrinus erythrinus
Hoplerythrinus unitaeniatus
Lebiasina bimaculata
Piabu cina festa e
Gymnotus carapo
Phractolaemus ansorgei
Pangasius sutchi
Umbra limi
active transfer are aided by contraction of snout protruded above the water surface,
the striated muscles surrounding the gas the fish opens its mouth and expands the
buccal cavity drawing fresh air in. At the
bladder (Johansen et al., 1970).
(2) The expulsion phase (Fig. 1: 3,4). After end of the intake phase (Fig. 1: 6) the very
the air fills the greatly expanded buccal large expanded buccal cavity is completely
cavity, it is expelled through the mouth filled with air. The intake phase is charwhich protrudes above the water surface. acterized by strong activity of both the
Expulsion of the gas from the buccal cavity epaxial and sternohyoideus muscles (Fig.
takes place as the floor of the mouth is 2). This phase has an average duration of
elevated by the interhyoideus muscle (Fig. 200 msec.
2; GH,, GH2) thereby compressing the buc(4) The compressive phase (Fig. 1: 6, 7, 8).
cal cavity. Activity in the sternohyoideus The fresh air is actively compressed into
muscle (Fig. 2) ceases. At the end of the the gas bladder as evident from the strong
expulsion phase, a residual volume of air and long burst of activity of the major bucremains in the gas bladder (Fig. 1: 4) even cal cavity compressor, the interhyoideus
when recordings were made at 30°C. (geniohyoideus) muscle (Fig. 2). Even
Johansen et al. (1970) showed that at higher though most of the air has already been
temperatures air breaths tended to be ini- displaced from the buccal cavity to the gas
tiated at progressively higher air bladder bladder before the fish begins its downoxygen tensions. They also found that at ward swim, it is possible that the compres30°C the initial air bladder Po 2 after an air sive action of the interhyoideus is aided by
breath approached that in air, thus a com- hydrostatic pressure. It is also clear from
plete expulsion of the gas in the air bladder the cineradiographic recordings that in
prior to air intake was postulated. How- Amia the buccal cavity volume is not a limever, numerous cineradiographic record- iting factor as may be the case in some
ings at 30°C show that a residual volume other air breathing fishes (Gans, 1970).
of gas remains at the conclusion of the Invariably excess air (Fig. 1: 8e) is being
expulsion phase (Fig. 1: 3, 4, 5). When the expelled repeatedly from under the opergas has been transferred from the gas blad- culum after the gas bladder has been fully
der to the buccal cavity, one can observe filled.
a collapse of the ventral abdominal region.
This collapse is not caused by contractions
RESPIRATORY GAS BLADDERS
of the abdominal and flank muscles, since
IN TELEOSTS
none of them show any activity during the
Respiratory gas bladders evolved in three
entire ventilatory cycle. The collapse is
of
the four major teleostean lineages (Table
apparently the result of the sudden reduc1).
They are absent from the herringlike
tion of the volume of the abdominal cavity
fishes,
the Clupeomorpha. In the Elopowhen the gas bladder is deflated. The avermorpha
only tarpon, Megalops cyprinoides
age duration of the expulsion phase is 200
and
M.
atlanticus,
possess a respiratory gas
msec.
bladder. Respiratory gas bladders are well
(3) The intake phase (Fig. 1: 5). With the represented in a great variety in the Osteo-
337
RESPIRATORY GAS BLADDERS
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FIG. 2. Electromyographic profiles of Amia calva during two modes SBS
of air ventilation. In one mode, the
transfer phase is passive, in the second mode it is active. C, compressive phase; E, expulsion phase; EP, epaxial
muscles; I, intake phase; GH,, GH2, interhyoideus muscle at respectively medial and lateral positions; SH,
sternohyoideus muscle. Time scale, 200 msec.
glossomorpha as well as the Euteleostei.
With the exception of Megalops all other
teleosts with respiratory gas bladders are
freshwater inhabitants. It is believed that
air breathing in Megalops atlanticus is
important during critical times when the
juveniles live in fresh and brackish waters
(Shlaifer and Breder, 1940; Shlaifer, 1941).
Morphological diversity in the
Osteoglossomorpha
The greatest morphological diversity in
gas bladder morphology among teleosts is
found in this lineage (Fig. 3), with Arapaima exhibiting the most primitive configuration (Greenwood and Liem, 1984),
which resembles that of Amia very closely.
It is a voluminous alveolate bladder with a
dorsal entry into the esophagus via an
extremely short "pneumatic duct." A
detailed functional anatomical description
is given elsewhere of the gas bladder in
Arapaima (Greenwood and Liem, 1984).
The gas bladder of Heterotis closely resembles that of Arapaima. The gas bladder in
Arapaima and Heterotis differs from that of
FIG. 1. Selected frames of a high-speed cineradiographic film of Amia calva (total length = 24 cm) during
air ventilation, to visualize the pulse pumping mechanism. 1-2, passive transfer phase; 3-4, expulsion phase;
5, intake phase; 6-8, compressive phase. Note residual gas in gas bladder at the end of expulsion (4, rg) and
concave profile of the ventral abdominal contour (3) as a result of the partial collapse of the abdominal wall
when gas bladder is emptied, be, buccal cavity; e, expelled gas bubble after being released through the opercular
opening; g, partially emptied gas bladder; gb, gas bladder; gbf, fresh air in buccal cavity; gbs, gas in the
buccopharyngeal cavity; rg, residual gas in gas bladder.
338
KAREL F. LIEM
C2
ARAPAIMA
NOTOPTERUS
PANTODON
FIG. 3. Respiratory gas bladder morphology of Amia
and representative osteoglossomorphs. E, esophagus;
GB, gas bladder; GE, cranial extension of the gas
bladder; GT, extensions of the gas bladder penetrating the vertebral elements including the transverse
processes; M, striated muscle; RG, respiratory gas
bladder; S, stomach.
Amia in having a close association between
its lateral walls and the body wall and an
attachment to the overlying kidneys. Such
specializations are also found in Pantodon
(Fig. 3) which exhibits even greater specializations by having numerous extensions
of the gas bladder penetrate the transverse
processes of the vertebrae (Fig. 4). In this
way buoyancy is maximized in Pantodon,
which is a surface dweller capable of leaping out of the water and gliding through
the air above the water for short distances.
As such, Pantodon's gas bladder represents
a highly specialized evolutionary condition
in which both respiratory (Schwartz, 1969)
and buoyancy functions (Poll and Nysten,
FIG. 4. Ventral view of vertebral column of Pantodon
buchhohi. Transverse processes (TP) are spongy or
pneumatic, accommodating branches of the gas bladder. C,, C2, first and second vertebrae.
1962) are maximized. The greatly enlarged
alveolate gas bladder satisfies the greater
portion of the gas exchange requirements
of the fish, which is an obligatory air
breather (Schwartz, 1969). At the same
time, buoyancy is maximized to an extent
not encountered in any other fish and
involves unique invasions of gas bladder
extensions into skeletal elements thereby
effectively pneumatizing the skeleton (Fig.
4) in a way analogous to that in birds. This
simultaneous specialization and optimization of two disparate functions of the gas
bladder in Pantodon exemplifies the
supremacy of natural selection. It further
demonstrates that, when two features of a
single integrated structural complex do not
constrain one another, each can be acted
upon by selection resulting in the synchro-
RESPIRATORY GAS BLADDERS
nous emergence of two radically different
specializations affecting the same structural complex.
Among osteoglossomorphs, Notopterus
possesses a highly specialized gas bladder
which has been extensively documented by
Dehadrai (1962). The voluminous gas
bladder possesses an extensive caudal
extension (Fig. 3). From this caudal extension, a series of ventral fingerlike projections descend on either side of the anal
pterygiophores. Such a morphological specialization is unique among the teleosts.
Anteriorly, the gas bladder sends out a projection toward the ear to improve the hearing abilities of the fish. Furthermore, the
gas bladder is thought to play a major role
in sound production (Greenwood, 1963).
This otic anterior projection is functionally
and structurally decoupled from the rest
of the bladder by a valve (Dehadrai, 1962).
A specialized striated muscle thought to be
derived from the axial musculature
(Dehadrai, 1962) runs on each side of the
gas bladder of Notopterus making it one of
the most specialized among teleosts.
A very different structural specialization
among osteoglossomorphs is found in the
alveolate gas bladder of Gymnarchus. The
structural specialization involves the large
but short pneumatic duct that enters the
esophagus dorsally at its very posterior
extremity (Fig. 5). Anterior to this junction, the esophagus is greatly expanded and
muscular. As will be discussed later, this
specialized voluminous, muscular esophagus plays a key role in the ventilatory mech-
339
ERYTHRINUS
FIG. 5. Respiratory gas bladder morphology in the
osteoglossomorph Gymnarchus and specialized euteleosteans. AG, anterior chamber of gas bladder; E,
esophagus; G, nonrespiratory portion of gas bladder;
M, striated muscle; RG, respiratory gas bladder; S,
stomach.
tical to those in Amia. When using Amia as
the outgroup for teleosts, the gas bladders
in Megalops and Arapaima must be considered primitive among teleosts. Even though
it retains an air-breathing function, the gas
bladder of Megalops cyprinoides has a dras-
tically reduced surface area if compared
with Amia (de Beaufort, 1908). Air breathing seems to have a great survival value
especially during juvenile stages of the life
anism.
history of the tarpon when it lives in estuMorphological diversity in
aries in which oxygen levels may drop or
Elopomorpha and Euteleostei
vary unpredictably. In the open seas the
adult
Atlantic tarpon, M. atlanticus, still
The only air-breathing elopomorphs,
surface
frequently to air breathe. Based on
Megalops cyprinoides and M. atlanticus, have
very large gas bladders of which the walls anatomy it may be postulated that M. cypriare moderately alveolate. In cyprinoides noides does not rely on air breathing as
alveolar-like tissue is confined to four nar- much as M. atlanticus and may represent
row longitudinal bands extending three- an intermediate stage in the evolutionary
fourths the length of the gas bladder (de transformation from the primitive lunglike
Beaufort, 1908). The gas bladder of Mega- gas bladder as seen in Amia to a non-reslops exhibits very close anatomical resem- piratory gas bladder primarily suited for
blances to that of Amia. Its configuration buoyancy functions as found in most
and connection to the esophagus are iden- teleosts.
340
KAREL F. LIEM
The gas bladders in the Euteleostei may 5). But in Phractolaemus the long pneumatic
be secondarily respiratory in function. All duct originates on the left side of the
members with respiratory gas bladders esophagus and enters into the left anterior
(Table 1) are relatively derived (advanced) part of the gas bladder (Thys van den
euteleostean taxa. Most of the respiratory Audenaerde, 1961; Jeffrey Graham, pergas bladders are found in the Ostariophysi sonal communication).
or Cypriniformes. They all retain a nonrespiratory anterior chamber for enhanc- Functional aspects of the
ing hearing functions while the posterior osteoglossomorph gas bladder
chamber becomes variously specialized for
Arapaima gigas. Since Arapaima reprerespiratory functions (Fig. 5). Erythrinus, sents a primitive state in the evolution of
Lebiasina, Hoplerythrinus, and Piabucina respiratory gas bladders in teleosts, it is
possess very specialized respiratory poste- important to understand the basic mechrior chambers (Rowntree, 1903; de Beau- anism underlying its ventilation. On the
fort, 1908; Graham et al, 1977; Kramer, basis of high speed cineradiography,
1978). The anterior half is alveolate and Greenwood and Liem (1984) offered a
the posterior half has a smooth wall with hypothesis contradicting the aspiratory
a well developed muscle (Kramer, 1978). model of Farrell and Randall (1978).
Anteriorly, the pneumatic duct is large and Greenwood and Liem suggested that Aralong, entering the esophagus in its left lat- paima ventilates air by buccal pumping in
eral wall at its posterior extremity (Fig. 5). a way very similar to Amia, in four phases,
Among the Euteleostei and Osteoglos- with the exception that during the expulsomorpha, Erythrinus, Hoplerythrinus, Gym- sion phase, air is expelled from beneath
notus, and Gymnarchus share a specialized the operculum rather than through the
feature in which the pneumatic duct enters mouth (Fig. 11). Preliminary studies show
the esophagus at its posterior extremity that Arapaima exhibits a pressure profile
next to the junction with the stomach (Fig. very similar to that of Amia. Figure 11 shows
5). In all four genera the voluminous, mus- the transfer phase, when gas flows from
cular esophagus plays an accessory role in the gas bladder into the mouth, is long
emptying and filling the gas bladder. In lasting (250-275 msec) and accompanied
this aspect the convergence between the by an early burst of the geniohyoideus musgas bladders of the euteleostean Gymnotus cle. The action of this muscle compresses
and the osteoglossomorph Gymnarchus is the buccopharynx and forces out water just
noteworthy (Fig. 5). Other features of these prior to the transfer of gas from the gas
two genera such as their behavior and body bladder. After most of the gas has left the
morphology, and their electric sensory gas bladder to fill the buccopharynx, the
expulsion phase begins (Fig. 11) by action
perceptions are also convergent.
of the geniohyoideus muscle. Air is then
Other euteleosteans (Pangasius, Umbra) taken into the buccal cavity by a sudden
have relatively simple respiratory gas blad- drop in pressure caused by action of the
ders, all with alveolate walls and short sternohyoideus. After the intake phase, the
pneumatic ducts entering the dorsal wall geniohyoideus becomes active, raising the
at the very beginning of the esophagus (Fig.
FIG. 6. Selected frames of a high-speed cineradiographic film of Xotopterus chilala (total length = 29 cm)
during air ventilation, to visualize the pattern of the pulse pump. During the transfer phase gas flows from
the gas bladder to the buccal cavity (1-2). Xote that the gas bladder (g) does not change its shape but volume
changes slightly. The expulsion phase (3-4) is characterized by the expulsion of gas (e) through the opercular
opening. At the end of the expulsion phase, the gas bladder remains partially filled. During the intake phase
(5-6) air is drawn into the buccal cavity which becomes fully expanded with air. The compressive phase (78) follows intake, and the air in the buccal cavity is compressed and forced into the gas bladder even though
some of the air also escapes through the opercular opening (e). c, cleithrum; e, expelled excess air; e, expelled
gas; g, gas bladder; gb, gas in buccal cavity; m, mandible; o, otolith; p, parasphenoid; s, swim bladder of prey
which was recently swallowed whole: v, vertebral column.
RESPIRATORY GAS BLADDERS
341
KAREL F. LIEM
pressure in the buccal cavity. As a result
the gas bladder becomes filled while excess
fresh air escapes from the opercular opening (see also Greenwood and Liem, 1984).
The compressive phase is prolonged and
takes 385-400 msec to complete. Thus,
both pressure and electromyographic profiles during air ventilation in Arapaima are
virtually identical to those of Amia (Fig.
11). Arapaima seems to combine primitive
morphology with a primitive pattern of air
ventilation.
Notopterus chitala. Morphologically the
gas bladder of Notopterus deviates in many
important ways from that of Amia. As discussed above, the gas bladder of Notopterus,
together with that of Pantodon, represents
the most specialized form among that of
all teleosts with respiratory gas bladders.
Is specialized gas bladder morphology
accompanied by a corresponding derived
pattern of ventilation? High speed cineradiography and electromyography reveal
the following pattern during an air breath
(Figs. 6, 7).
Transfer phase—The fish swims toward
the surface (Fig. 6: 1) and gas can be seen
to flow from the gas bladder into the buccal
cavity (Fig. 6: 2, gb). After 200-225 msec
the buccal cavity is filled with gas, while
the gas bladder remains filled with gas but
its volume as estimated from the gas bladder profiles of the individual X rays
decreases by approximately 35 percent (Fig.
6: lg). The transfer phase proceeds without any activity in the buccal muscles (Fig.
7). It is postulated that the striated muscles
on the gas bladder (Fig. 3) are active.
Expulsion phase—Once the buccopharynx is filled with air, the expulsion phase
begins. As the posterior intermandibularis
(the functional analogue of the geniohyoideus and interhyoideus) muscle becomes
active and the pressure in the buccal cavity
increases (Fig. 7: PIM; BP) and the gas is
expelled from the mouth through the
opercular opening (Fig. 7: 3, 4: e). Expulsion takes place within 100 msec and the
fish's position is oblique with its snout
slightly protruded from the surface.
Intake phase—With its snout above the
water surface, the fish sucks in air (Fig. 6:
5) through its open mouth. This is the result
of the actions of the levator operculi (Fig.
7: LO) and sternohyoideus (SH), which
expand the buccal cavity thereby lowering
the buccal pressure (Fig. 7: BP). Cineradiographically one can observe the filling
of the buccal cavity with air (Fig. 6: 6, gb).
Intake requires less than 75 msec and is
immediately followed by the compressive
phase as the fish begins its descent in the
water column.
Compressive phase—The fish has closed
its mouth by action of the adductor mandibulae muscle (Fig. 7: AM) and the buccal
cavity becomes compressed by actions of
the adductor arcus palatini, adductor mandibulae and posterior intermandibularis
muscles. Their combined actions raise the
pressure in the buccal cavity significantly
(Fig. 7: AAP, AM, PIM, BP). Continued
activity of the sternohyoideus may aid
compression if its line of action moves above
the jaw joint. Cineradiographically, the
fresh air can be seen to flow into the gas
bladder, while excess air escapes through
the opercular aperture (Fig. 6: 7, 8, e). The
compressive phase lasts over 225 msec.
Aquatic breathing—Immediately after the
compressive phase of the aerial breathing
cycle the fish begins the aquatic breathing
cycle with the expansive phase, drawing
water into the buccal cavity by action of
the sternohyoideus muscle, followed by the
compressive phase, forcing water from the
buccal cavity through the gill curtain into
the opercular cavity. The compressive
phase of the aquatic cycle is brought about
by the adductor arcus palatini and poste-
Fic. 7. Electromyographic and pressure profiles during air and aquatic ventilation in Xotopterus chitala (total
length = 29 cm). AAP, adductor arcus palatini; AM, adductor mandibulae complex; BP, buccal pressure; C,
compressive phase; E, expulsion phase; EXP, expansive phase; I, intake phase; LO, levator operculi muscle;
PIM, posterior intermandibularis muscle; SH, sternohyoideus muscle. Pressure scale, 5 cm H2O; time scale,
100 msec.
343
RESPIRATORY GAS BLADDERS
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344
KAREL F. LIEM
surfacing and taking in fresh air first before
exhaling (Fig. 8: 1). It fills its buccal cavity
with air by action of the sternohyoideus
muscle which creates a low pressure in the
buccopharyngeal cavity. It then begins a
long process of compression by first forcing air from the buccopharyngeal cavity
into the voluminous esophagus (Fig. 8: 2,
b, e). The geniohyoideus muscles raise the
pressure in the buccopharyngeal cavity.
Once the buccopharyngeal cavity is completely emptied, one can see an air-filled
esophagus of an enormous dimension (Fig.
8: 3, e). Subsequent contraction of the
esophagus will force air into the gas bladder via the pneumatic duct. In exhalation,
which follows inhalation (Fig. 8: 4), gas
flows from the gas bladder into the esophagus via the pneumatic duct without any
activity in the buccal muscles. As the esophagus fills it contracts antiperistaltically,
forcing air into the buccal cavity from
which it escapes through the mouth (Fig.
8: 5-8). Exhalation in Gymnotus is analogous to the transfer and expulsion phases
of other teleosts during which gas flows
from the gas bladder to the buccal cavity.
In Gymnotus the esophagus is interposed as
an expandable temporary reservoir that
acts as a two-way force pump, driven by
peristalsis and reversed peristalsis. As a
result, transfer proceeds without any
Functional aspects of the
actions of the buccal muscles (Fig. 11),
euteleostean gas bladder
whereas exhalation is completed by a series
Gymnotus carapo. A broader comparative of 3 actions by the geniohyoideus muscles
study to include the euteleosteans is pre- (Fig. 11) which by lifting the buccal floor
sented in order to make general conclu- compress the buccal cavity thereby forcing
sions concerning the correlation between gas bubbles out of the mouth.
morphological transformations and the
nature of motor patterns governing the
DISCUSSION
functions of the structural complexes associated with the respiratory gas bladders.
The holistic principle of symmorphosis
The most specialized motor patterns can defined as a state of structural design combe expected in the morphologically most mensurate to multiple competing funcspecialized forms. Thus this analysis focuses tional needs resulting from regulated moron the most derived form among the Eute- phogenesis, is probably best exemplified in
leostei, Gymnotus, with the goal to elucidate the respiratory system of higher vertethe greatest deviation from the general- brates (Duncker, 1971,1972; Weibel, 1984,
ized pattern of Amia which seems so per- p. 59) as well as lower vertebrates (Hughes
vasive in the teleosts.
and Morgan, 1973). According to this prinThe banded knife fish exhibits the most ciple air breathing fishes inhabiting hypoxic
specialized respiratory pattern among the waters must have the design and dimeneuteleosteans (Liem et al., 1984). It is pecu- sions of their respiratory gas bladders and
liar in starting the air ventilation cycle by muscular pumps optimally matched to meet
rior intermandibularis muscles. It is clear
from both the pressure and electromyographic profiles (Fig. 7) that the aerial
breathing cycle differs significantly from
the aquatic one. Aquatic ventilation proceeds in two cycles while air ventilation has
four cycles. The compressive phase during
aquatic breathing is effected by very short
bursts of the adductor arcus palatini and
posterior intermandibularis muscles and
the sternohyoideus is silent. During aerial
ventilation the sternohyoideus is quite
active and so is the adductor mandibulae
complex (Fig. 7: AM), which remains inactive during the compressive phase of the
aquatic cycle. Thus there is no evidence to
support the hypothesis that, in general,
aerial respiratory cycles can be derived
from aquatic cycles (Randall et al., 1981).
General conclusion—Despite the highly
specialized morphology of the gas bladder
in Notopterus, the pressure and electromyographic profiles during air ventilation
resemble that of Amia very closely (Fig. 11),
differing only in minor details. Thus the
motor pattern underlying air ventilation
appears to be conserved despite significant
morphological transformations of the gas
bladder, the key jaw muscles and bones of
the buccal pulse (force) pump.
RESPIRATORY GAS BLADDERS
345
their metabolic demands. Thus, this prin- then forced into the esophagus by the bucciple uses the multiple, synergistic or con- cal pressure pump. The esophagus underflicting functional parameters as a gauge. goes peristalsis forcing the air into the gas
If symmorphosis indeed occurs, one would bladder. This filling of the gas bladder is
expect convergence in several structural then followed by exhalation whereby gas
complexes because similar functional is allowed to flow into the esophagus, which
demands (air ventilation, gill ventilation, upon being fully filled will undergo antifeeding and buoyancy) would necessarily peristalsis to expel the gas via the buccal
induce similar morphological design. One cavity.
part of this discussion will examine the role
It is indeed remarkable that a similar
of symmorphosis in convergent evolution. esophageal pump is found in a completely
However, it can be argued that animals are unrelated fish, the osteoglossomorph Gymnot necessarily at maximum equilibrium narchus (Fig. 10). Gymnarchus also utilizes
with the fluctuating environments over anti-peristalsis of the esophageal pump
time. Adaptations and morphogenetic during exhalation and esophageal peripotential may well be constrained and can- stalsis for inhalation (Fig. 10: 2, 7, 8, 9, e),
alized by historical factors (Liem and Wake, even though the sequence of ventilation is
1985). The second part will address the the opposite from that in Gymnotus and
questions: (1) Is specialized morphology Hoplerythrinus. As Gymnarchus approaches
("hardware") consistently accompanied by the surface, its esophagus becomes filled
corresponding specialized motor output with gas (Fig. 10: 2, e), which then flows
("software") in the various teleostean lin- into the buccal cavity (Fig. 10: 3, b). Gas is
eages; (2) Is there a predisposition for con- expelled through the opercular opening
servatism in a particular lineage; (3) Have (Fig. 10: 5), and a small residual volume
environmental demands molded gas blad- remains in the gas bladder. After the fish
der morphologies and their associated expels gas from its buccal cavity, fresh air
muscular pumps similarly or dissimilarly in is forced into the esophagus via the pharthe various teleostean lineages?
ynx (Fig. 10: 7,8, e, p). Once the esophagus
is filled, it forces the air into the respiratory
gas bladder (Fig. 10:9, 10) via the "glottis"
Symmorphosis and convergent evolution
One of the historical consequences of which is provided with a powerful sphincsymmorphosis is probably convergent evo- ter.
lution. The degree of symmorphosis that
The convergent occurrence of the highly
has molded the morphological design of specialized esophageal pump in the three
teleostean gas bladders may therefore be unrelated lineages can best be explained
correlated with the frequency of conver- by the position of the entrance of the pneugent features in the different lineages. matic duct into the esophagus. In all three
Within the Euteleostei a truly striking case taxa, the pneumatic duct enters very far
of convergence can be seen in the siluri- posteriorly into the esophagus at the juncform Gymnotus (Fig. 8) and the characiform tion with the stomach. The relatively large
Hoplerythrinus (Fig. 9; Kramer, 1978). distance for gas to be moved from the bucAccording to Fink and Fink (1981) the cal cavity to the gas bladder through the
Gymnotoidei is a sister group of the Silu- entire length of the esophagus, which by
roidei and only distantly related to the its muscular nature offers considerable
Characiformes. Yet the peculiar gas blad- resistance, would necessitate an auxiliary
der morphology and very specialized pump. The esophagus with its built-in elasesophageal pump in the two groups are ticity and striated muscle walls is previrtually identical (Figs. 8, 9; Liem et al., adapted to function as an auxiliary pump.
1984). Further, the unique pattern of ven- Recent data show that a fish with a postetilation found in Gymnotus (Fig. 8) is exactly riorly located entrance into the esophagus
mirrored in Hoplerythrinus. In both taxa air does have an esophageal pump regardless
ventilation starts with inhalation during of its phylogenetic position. Ontogenetiwhich fresh air is drawn into the mouth, cally, gas bladders emerge as outpocket-
346
KAREL F. LIEM
RESPIRATORY GAS BLADDERS
347
be
B
ag
: rg
('
'
•yes
FIG. 9. Tracings of images of selected frames of a lateral cineradiographic film taken at 100 frames per sec
of ventilation in Hoplerythrinus unitaeniatus (total length = 15 cm). Cavities filled with gas are not shaded. Fish
begins with the intake phase (A, B), after which the compressive phase proceeds in 2 steps. At first the
esophagus is filled and air is then forced from the esophagus to the gas bladder by peristalsis (C, D). After
the compressive phase has been completed (D), the transfer phase begins with the filling of the esophagus
(E). Anti-peristalsis will force the gas to enter the buccal cavity after which it is expelled either through the
mouth or the opercular opening (F). ag, anterior chamber of the gas bladder; be, buccal cavity; es, esophagus;
gb, expelled gas bubble; pg, posterior non-respiratory gas bladder; rg, respiratory gas bladder.
ings from the esophagus. The site from
which this outpocketing grows varies considerably in the various taxa without any
apparent functional consequences except
when the site happens to be at the posterior
end of the esophagus. A posteriorly positioned pneumatic duct creates a functional
problem of moving air to and from the
buccal cavity. This functional problem is
solved by the differentiation of an accessory esophageal pump, which has arisen
independently in three unrelated lineages.
The convergent occurrence of the accessory esophageal pump is indeed admirably
Fie. 8. Prints of images of selected frames of a lateral cineradiographic film taken at 150 frames per sec
during ventilation in Gymnotus carapo (total length = 16 cm). The fish begins with an intake phase (1) at the
surface of the water filling its entire buccopharyngeal cavity with fresh air. As it descends in the water column
the compressive phase begins in two stages. First air is forced into the esophagus which expands to an enormous
size (2, e). Then the esophagus undergoes peristalsis squeezing the air into the gas bladder (3, 4, e). After
the compressive phase is completed, the transfer phase begins and proceeds in two steps. Gas passes from the
gas bladder into the esophagus (5) and then by anti-peristalsis of the esophagus into the buccal cavity (6, e,
b). The gas is then actively expelled from the mouth (7, 8). b, buccal cavity; e, esophagus; g, respiratory gas
bladder; g', anterior chamber of the gas bladder.
348
KAREL F. LIEM
matched to the functional requirement of
moving gas in and out of the gas bladder
via an elongate esophagus and pneumatic
duct when the later originates from the
posterior extremity of the former.
Functional conservatism during
evolutionary diversification
The great morphological diversity of the
gas bladders and associated buccal pumps
in the Osteoglossomorpha (Figs. 3, 5;
Greenwood, 1963, 1971, 1973) as well as
in the Euteleostei (fig. 5 in de Beaufort,
1908; Lauder, 1980) is well documented.
Yet there is no corresponding diversity in
the pattern of muscle activity mediating
the ventilatory function (Fig. 11). The conserved pattern proceeds as follows: (1) passive transfer phase, followed by (2) an
expulsion phase mediated by action of the
geniohyoideus or another compressive
muscle producing a positive pressure pulse
in the buccal cavity; active expulsion is succeeded by an active intake phase by action
of the sternohyoideus muscle resulting in
a negative pressure pulse in the buccal cavity; the final phase is an extended compressive phase primarily driven by action
of the geniohyoideus muscle forcing the
air into the gas bladder (Fig. 11). The pattern of motor output to the muscles underlying the mechanism of ventilation is conserved despite major morphological
changes in the design of the buccal pump
FIG. 10. Prints of images of selected frames of a
lateral cineradiographic film taken at 100 frames per
sec during ventilation in Gymnarchus nilotkus (total
length 12.5 cm). The fish begins with a two step transfer phase (1—4) during which gas passes from the gas
bladder (g) to the esophagus (e). Then anti-peristalsis
forces the gas into the buccal cavity (4). The expulsion
phase (5) completes exhalation when air is expelled
through the opercular opening. Note that a very small
residual volume of gas remains (5). At the surface,
the fish starts the intake phase filling its buccopharyngeal cavity. An extended two step compressive
phase follows (7-9) with the air being moved from
the buccal cavity into the pharynx (p) and esophagus
(e). From the esophagus fresh air is forced into the
gas bladder by peristaltic action. In (10) inhalation
has been completed with the gas bladder fully filled,
b, buccal cavity; e, esophagus; g, gas bladder; p, pharynx.
RESPIRATORY GAS BLADDERS
349
AMIA
FIG. 11. Summary diagrams of the four phases of air ventilation in various fish taxa. Representative pressure
profiles are depicted together with representative electromyograms (activity is depicted with solid bars) of
the key muscles driving the pulse pump. BP, buccal pressure; C, compressive phase; E, expulsion phase; GH,
geniohyoideus; I, intake phase; IH, interhyoideus, which functions as the teleostean geniohyoideus; P, preparatory phase; PIM, posterior intermandibulars; SH, sternohyoideus; T = Transfer phase. Pressure scale, 5
cm HjO; time scale, 200 msec.
and gas bladder during the evolutionary
diversification of the osteoglossomorphs
and euteleosteans. Thus the differences in
air breathing patterns and performances
have a morphological basis involving
peripheral structures ("hardware") rather
than a neural one ("software").
Even in physoclistous teleosts that use
suprabranchial cavities as respiratory
chambers instead of gas bladders, the identical pattern of motor output drives the
ventilatory pump (Liem, 1987). Thus, a
strictly conserved neural control of muscles underlying air ventilation does not
necessarily limit the potential for morphological diversification of the buccal appa-
ratus and aerial respiration structure. The
structural diversification in the buccal
apparatus is further related to feeding
functions and does not appear to have been
constrained in any way by the functional
demands for ventilating the gas bladder.
Diversity of the oral structures of teleosts
with nonrespiratory gas bladders does not
exceed those of related teleosts with respiratory gas bladders. Thus, two functional
demands can be satisfied at the same time
by shared integrated structural elements
that can undergo major transformations
thereby simultaneously accommodating
both functions despite a conserved pattern
of motor output. Evolution is therefore not
350
KAREL F. LIEM
necessarily initiated by a change in neural
control of behavior or function triggering
a cascade of gradual changes in structural
design. To the contrary, saltatory evolution of respiratory gas bladders and their
buccal pumps seems to have proceeded by
major transformations in structural design
without appreciable changes in the patterns of neural control.
Environmental and historical
canalization of gas bladder design
Design defined as the organization of
biological structure in relation to a function is often thought to have been canalized in such a way as to either restrict or
increase the potential structural and functional diversification of descendant taxa
(Liem and Wake, 1985). Most major evolutionary advances depended on shifts into
new adaptive zones, and the feasibility of
such shifts, in turn, depended on available
preadaptive designs. Respiratory gas bladder design evolved in three of the four
major teleostean lineages (Table 1), and
underwent extensive radiations in two lineages (Figs. 3, 5) accompanied by strikingly
convergent specializations. Such convergent patterns can be interpreted to mean
that historical factors or intrinsic design
was not significant in limiting structural
diversity. It is especially important to note
that this diversity in form did not require
any changes in the neuromuscular patterns
(Fig. 11). The independent emergence of
lunglike organs from gas bladders in
teleosts demonstrates the relative slightness of reconstruction that seems to be necessary for successful adaptation to rather
drastic shifts of adaptive zones. Once the
gas bladder became secondarily respiratory, it set the stage for the independent
evolution of a series of convergent specializations in the Osteoglossomorpha and
Euteleostei in response to similar functional demands. Thus the evolutionary patterns of the respiratory gas bladders in the
Euteleostei and Osteoglossomorpha (Figs.
3, 5, 11) reflect three major principles: (1)
the ever-present pressure of environmental factors; (2) the opportunistic nature of
evolution; and (3) the potential variability
of design.
The absence of respiratory gas bladders
in the Clupeomorpha and the rarity in the
Elopomorpha (Table 1) may best be correlated with the lack of selective forces
favoring a niche shift. The vast majority
of clupeomorphs and elopomorphs are
oceanic and inhabit typically oxygen-rich
water. There is no evidence for arguing
the lack of preadaptive (sensu Bock, 1959;
Mayr, 1976, p. 100) features in the clupeomorph and elopomorph gas bladders
which precluded the minor reconstruction
of a membranous surface for respiratory
surfaces. The existing pneumatic duct, the
morphology of the buccal pump and neural
control apparatus in the Clupeomorpha and
Elopomorpha are already functionally
poised to assume the new tasks since they
are identical in design (de Beaufort, 1908;
Kirchhoff, 1958; Vrba, 1968) to those of
the primitive Euteleostei and Osteoglossomorpha, in which respiratory gas bladders have evolved.
This comparative functional study supports three evolutionary notions: (1)
reversed evolution is possible, i.e., primitive lungs evolved into non-respiratory
hydrostatic swimbladders, which subsequently reverted back to become respiratory gas bladders. Such a shift is facilitated
by the conserved neuromuscular pattern
during the functional transformation; (2)
evolutionary innovations are not restricted
to an intensification or change of function
of existing structures (Mayr, 1976), but may
involve the addition of a new function (respiratory) while the original functions
(hydrostatic, hearing, and sound production) are maintained; and (3) evolutionary
innovations such as respiratory gas bladders do not emerge in the absence of functional demands of new habits even if the
taxon possesses the essential preexisting
building blocks.
ACKNOWLEDGMENTS
I thank Elizabeth Brainerd, Ernest Wu,
Karsten Hartel, Jeffrey Graham, and Neal
Smatresk for their very substantial contributions in improving and correcting the
manuscript and adding significantly to the
data base of this paper. I am also greatly
indebted for constructive discussions with
RESPIRATORY GAS BLADDERS
351
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of fish gills in relation to their respiratory funcgreatly benefitted from the skills and help
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harengus L. Zool. Jahrb. Anat. 76:461-540.
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D. L. 1978. Ventilation of the respiratory
important ways to make it possible for me Kramer,
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