AMER. ZOOL., 21:83-101 (1981)
A Functional Approach to the Phylogeny of the
Pharyngognath Teleosts1
KAREL F. LIEM
Musem of Comparative Zoology, Harvard University,
Cambridge, Massachusetts 02138
AND
P. H. GREENWOOD
Department of Zoology, British Museum (Natural History),
London SW7 5BD, England
SYNOPSIS. Functional morphological analysis has revealed the existence of three functionally and morphologically different mechanisms underlying the tongue-parasphenoid
and pharyngeal-parasphenoid bites in advanced teleost fishes. The bite is specialized differently in Pristolepis and the Anabantoidei, and in a primitive condition in both the
Nandidae and Channiformes. These taxa belong to at least three unrelated lineages and
do not share a common ancestry as was previously postulated. It has been possible to show
how an originally primitive character can acquire a new biological and phylogenetic meaning by being integrated into a specialized functional complex. Based on functional data
on the pharyngeal jaw apparatus, a new hypothesis is proposed stating that the Cichlidae,
Embiotocidae, Labridae, Odacidae and Scaridae represent a monophyletic assemblage.
This case study has demonstrated that reciprocal illumination of functional morphological
and phylogenetic findings can lead to: (1) better tested and more precise phylogenetic
hypotheses; (2) the construction of new hypotheses on the basis of specialized character
complexes which were unrecognized by the use of a purely descriptive morphological
approach.
ture of this mutual interdependence of
Initial hypotheses on the phylogenetic structural elements in a functional context
interrelationships of organisms are usually {e.g., Hoogerhoud and Barel, 1978), it can
based on a limited set of similarities in iso- sort out characters that are closely intelated structural elements. In general, the grated within a major functional complex
information contained in these selected from those that are indeed independent
isolated elements is sufficient to formulate because they belong to a different funcan initial phylogenetic hypothesis. How- tional component. It is in this context that
ever, after proposing an initial phylogeny, functional morphology can play a role by
most workers prefer to test it against com- providing a practical tool to make more
peting hypotheses, find more characters or precise statements about the characters
analyze the original set of characters more upon which phylogenetic hypotheses have
precisely. When attempting to expand the been made. Consequently, data generated
data base one usually searches for more by functional morphologists can be used to
structural characters, which are truly in- test competing phylogenetic hypotheses
dependent from the original set of char- from an entirely novel approach. Apart
acters. It is axiomatic that structural ele- from its potential value as a tool for testing
ments are integrated into distinct patterns existing phylogenetic hypotheses, funcin order to work together to perform one tional morphology may play a role in dior more well defined functions. Because recting our attention to major character
functional morphology analyzes the na- complexes, whose phylogenetic importance has not been recognized previously
because the more conventional approaches
were too narrowly focussed. When such
1
From the Symposium on Functional-Adaptive Anal- new character complexes are found, new
ysis in Syslematics presented at the Annual Meeting of hypotheses on phylogenetic relationships
the American Society of Zoologists, 27-30 December
can be formulated.
1979, at Tampa, Florida.
INTRODUCTION
83
84
K. F. LIEM AND P. H. GREENWOOD
In this paper two case studies concerning the functional morphology of some aspects of the feeding apparatus in the acanthopterygian fishes are discussed: (1) A
functional reevaluation of a character previously used in an isolated morphological
sense; (2) The formulation of a phylogenetic hypothesis on the basis of a suite of
interrelated characters whose recognition
is the result of functional analysis.
Although the two case studies are presented separately, they are closely interrelated because of a common thread uniting the functional morphological approach
to studies of teleostean phylogeny.
BITING MECHANISMS INVOLVING TEETH
ON THE PARASPHENOID
Parasphenoid bite
The presence of teeth on the parasphenoid is known from such primitive teleosts
as the osteoglossomorphs, clupeomorphs
and elopomorphs. The presence of parasphenoid teeth in some acanthopterygians
has also received a great deal of attention
in the literature {e.g., Liem, 1963, 1970;
Barlow et al, 1968; Gosline, 1968, 1971;
Nelson, 1969).
Morphology
and phylogenetic hypothesis.
The prevailing hypothesis (Nelson, 1969,
pp. 496-497) is that the presence of teeth
on the parasphenoid in certain acanthopterygian fishes (Pristolepis, Nandus, Badis,
Channa and anabantoids) is a primitive
character. However, when the presence of
parasphenoid teeth (Fig. 1) is considered
in conjunction with the opposing tooth
bearing ventral elements (basihyal, third
hypobranchial and fifth ceratobranchials)
the character complex seems to contain
potentially important phylogenetic information.
In Pristolepis the area occupied by the
parasphenoid teeth probably is secondarily
increased, but in the other forms the teeth
are restricted to a small posterior patch
(Fig. 1). The basihyal teeth of Pristolepis
oppose the parasphenoid teeth (Fig. 1A:
bh, ps). But, although Nandus possesses :%
toothed basihyal (Fig. ID: bh), this ventral
element does not oppose the more posteriorly located parasphenoid teeth (Fig. ID:
ps). In the other groups with parasphenoid teeth there is a trend towards a posterior shift so that the teeth of the third
hypobranchials (Fig. 1A-D: hbs) oppose
the posteriorly shifted parasphenoid teeth.
In anabantoids, a further backward shift
of the parasphenoid bite seems to have occurred with the result that they came to
oppose the lower pharyngeal jaws (Fig. IB,
C: ps, lpj).
The prevailing hypothesis derived from
the evidence of the parasphenoid bite is
(Nelson, 1969): "If such was the evolutionary role of the third hypobranchial toothplates, they, in opposing the parasphenoid
teeth, would be an important character
suggesting that nandids, pristolepids,
ophiocephalids, and even anabantoids,
from which hypobranchial teeth are absent, are closely related to one another and
constitute a primitive but diversified group
of spiny-finned fishes with a world-wide
distribution in tropical fresh water."
Functional analysis. Using electromyog-
raphy, cineradiography and high speed
light movies (for details of techniques see
Liem, 1978) more precise knowledge can
be gained of the biomechanics of the parasphenoid bite. These approaches may enable us to recognize the structural elements that work together to form the
integrated functional complexes underlying the parasphenoid biting mechanism.
Because the experimental procedures are
complex and time-consuming, the func-
FIG. 1. Diagrams of the dorsal aspect of the ventral elements of the left hypobranchial arches (to the left of
vertical dotted lines) and ventral aspect of the left half of the neurocranium, with ventral aspect of the upper
pharyngeal jaw (upj) (to the right of the vertical dotted line). The vertical dashed line indicates the median
plane of the head. Dashed arrows indicate occluding pairs of elements and direction of principal movements
of the elements. A, Pristolepis fasciatus (Pristolepidae); B, Anabas testudineus (Anabantidae); C, Macropodus
opercularis (Belontiidae); D, \'andus nebulosus (Nandidae); E, Badis badis (Badidae); F. Tilapia melanopleura
(Cichlidae). bh, basihyal; hb3> third hypobranchial; lpj, lower pharyngeal jaw; ps, parasphenoid; upj, upper
pharyngeal jaw.
PHARYNGOGNATH TELEOSTS
85
86
K. F. LIEM AND P. H. GREENWOOD
AP
LA
DO
PM
IML
HV
IOP
FIG. 2. On left, lateral aspect of cephalic muscles after removal of lacrimal, circumorbital bones and eyeball
of Pristolepis fasciatw. On right, medial aspect of the right hyoid apparatus and associated muscles with the
hyoid (HY) disarticulated from the fossa (F) of the basihyal in which condyle (C) was lodged; the tip of the
right mandible is shown indicating muscle insertions. In center, diagram of the active periods of the muscles
as obtained from electromyography during feeding (mastication). A,, part A, of adductor mandibulae complex; Aj A3, parts A2 and A3 of adductor mandibulae complex; AP, adductor arcus palatini; BH, basihyal;
C, condyle on hyoid; DO, dilatator operculi; F, fossa in basihyal; GHA,, part 1 of geniohyoideus between
mandible and basihyal; GHA 2 , part 2 of geniohyoideus between mandible and hyoid referred to as geniohyoideus anterior; GHP, posterior part of geniohyoideus referred to as geniohyoideus posterior; GHG, part
of geniohyoideus running between the basihyal and hyoid; HY, hyoid; IML, interoperculomandibular ligament; IOP, interoperculum; LA, levator arcus palatini; LO, levator operculi; PM, premaxilla; POP, preoperculum; PS], power stroke 1; PS2, power stroke 2; rs, release stroke; SH, sternohyoideus.
tional studies are necessarily limited both 2). During the power stroke the teeth of
in scope and taxonomic representation. the basihyal occlude against those of the
However, we have analyzed the key taxa parasphenoid. Occlusion is accomplished
in the series of acanthopterygians, which by an anterodorsal movement of the basiaccording to Nelson's hypothesis have a hyal. Toward the end of the power stroke
parasphenoid biting mechanism and are there is a slight tilting of the basihyal so
therefore more closely related to each oth- that the posterior end moves dorsally.
er than to any other teleosts.
Two kinds of power strokes (Fig. 2: P1;
The taxa are Pristolepis fasciatus (Pristo- P2) can be recognized. In type 1 (Fig. 2: P,)
lepidae), Badis badis (Badidae), Nandus neb- the adductor mandibulae complex (A2, A3)
ulosus and Monocirrhus polyacanthus (Nan- is active, while in type 2 (P2) the adductors
didae), Channa striatus (Channiformes or remain silent. Type 2 is more variable in
Ophicephaliformes), Anabas testudineus both pattern and duration but can be charand Helostoma temmincki (Anabantoidei). acterized by multiple activities of all four
We have selected only those functional fea- subdivisions of the geniohyoideus muscle
tures that are most directly related to the and silence of the adductor mandibulae
parasphenoid bite, leaving out other func- muscles (Fig. 2). A very brief release stroke
tional data.
(rs) is effected through the action of the
In Pristolepis, the electromyographic sternohyoideus muscle (Fig. 2: SH).
profile (Fig. 2) during chewing is the most
The kinematic profile of the basihyal accomplex and specialized ever recorded companying these elaborate electromyfrom a teleost. Four distinct subdivisions ographic patterns is also very complex if
of the geniohyoideus muscle (protractor compared with that of other teleosts. The
hyoideus of Winterbottom, 1974) are ac- movements of the basihyal are not restricttive during the power stroke. Each subdi- ed to the sagittal plane. In addition to dorvision has a characteristic pattern of activ- soventral and fore-and-aft movements, the
ity in respect to onset and duration (Fig. bone rotates around its long axis to exert
PHARYNGOGNATH TELEOSTS
a grinding action on the prey. Because of
the strong occlusion between the teeth of
the parasphenoid and those of the basihyal, the hard exoskeletons of prey can be
broken prior to swallowing. The limited
^fctcursions of the toothed third hypobranchial (Fig. 1A: ht^) seem to occur passively
in conjunction with movements of the lower pharyngeal jaw rather than with the
hyoid apparatus.
Although Nandus has teeth on both the
basihyal and parasphenoid (Fig. ID), a
true tongue-parasphenoid bite is absent.
The electromyographic profile during
prey handling is characterized by short
bursts of activity in the geniohyoideus
muscle, with occasional, irregularly interspersed firings of the sternohyoideus and
adductor mandibulae complex (Fig. 3).
Power and release strokes do not occur.
Instead the basihyal undergoes some protrusive and retrusive movements in the
sagittal plane. It neither opposes nor occludes with the teeth on the parasphenoid.
The electromyographic and kinematic
profiles in Nandus indicate that the prey is
being positioned and moved posteriorly
rather than triturated. Prey is swallowed
intact. Such a biomechanical pattern corresponds with that of more generalized
and primitive fishes. Kinematically the
toothed third hypobranchials are linked
with the lower pharyngeal jaws (fifth ceratobranchials); their movements do not indicate any opposition or occlusion against
the teeth of the parasphenoid. Instead, the
toothed third hypobranchial seems to play
an accessory role in swallowing large prey.
Badis lacks teeth on the basihyal and the
teeth on the parasphenoid are restricted to
the posterior part of the bone (Fig. IE: ps).
Its kinematic and electromyographic profiles during prey handling are virtually
identical to those of Nandus (Fig. 3). Similarly Badis does not triturate its prey by
means of a tongue-parasphenoid bite.
In Channa, prey handling within the
mouth proceeds very differently from that
in the previous taxa. Electromyographically a distinct pattern can be seen, during
which the geniohyoideus muscles remain
inactive, while the adductor mandibulae
complex and sternohyoideus muscle ex-
87
FIG. 3. Diagrams of the active periods of the muscles
in Nandus (Nandidae), Badis (Badidae), Anabas (Anabantidae) and Channa (Channiformes, Ophicephaliformes) during "mastication." Dotted blocks indicate
activity in less than 40% of the recordings. A2.3, parts
A2 and A3 of the adductor mandibulae complex;
GHA, GHP, geniohyoideus anterior and posterior
muscles; SH, sternohyoideus.
hibit activity in an alternating pattern (Fig.
3). During this activity Channa seems to
rely on the creation of a water current as
a prey transport system. Strong activity of
the sternohyoideus muscle lowers the floor
of the mouth to suck in more water. The
succeeding action of the adductor mandibulae compresses the buccal cavity to move
the prey further back. Channa swallows its
prey whole.
Anabas testudineus does triturate its prey
by means of a parasphenoid-biting mechanism. The electromyographic profile is
dominated by long periods of cyclical activity of the geniohyoideus muscles, interrupted by periods of silence (Fig. 4). This
regular pattern of activity of the geniohyoideus muscle is accompanied by an absence of activity in the sternohyoideus and
adductor mandibulae muscles (Fig. 4: SH,
GH). Activity in the geniohyoideus muscle
is linked indirectly with the parasphenoidbiting mechanism.
The pharyngeal jaw apparatus of Anabas
is very specialized both morphologically
and functionally. Its morphology deviates
from the generalized percoid condition in
the following ways: (1) Left and right fifth
ceratobranchials are enlarged and united
to form a single lower pharyngeal jaw
(Figs. IB, C: lpj, cb5); (2) A very strong
epibranchial-ceratobranchial ligament (Fig.
8 C: eel) connects the fourth epibranchial
to the posterior part of the lower pharyngeal jaw, transmitting dorsally directed
movements of the epibranchial to the lower pharyngeal jaw; (3) The origins of the
hypertrophied fourth levator externus
and the levator posterior (Fig. 8C: le4, lp)
88
K. F. LIEM AND P. H. GREENWOOD
•
L.P
LE.
POF
ANARAR
PS
: rs :
^ _
i
— — -
-;-
PRISTOLEPIS
: pro; ret
:
:
_
:
— ™ -J-
l.nBOCHILOTES
PSI- ts :psj:
•
»
—^3~~
;
•
:
PH
RH
:
GH
^
;
:
:
;
i
B
:
:
!
FIG. 4. Diagrams of the active periods of the muscles
in Anabas (Anabantidae); Pristolepis (Pristolepidae)
and Lobochilotes (Cichlidae) during the mastication of
food. GH, geniohyoideus; LE,, fourth levator externus; LP, levator posterior; PCE, pharyngocleithralis
externus; PH, pharyngohyoideus; pro, protraction;
ps, power stroke; ps,, power stroke 1; ps^ power
stroke 2; ret, retraction; rs, release stroke; SH, sternohyoideus; ts, transitional stroke.
are shifted posterolaterally so that the fibers run vertically; (4) The opposing teeth
of the parasphenoid and the lower pharyngeal jaw are enlarged.
The electromyographic profile of the
parasphenoid-lower pharyngeal jaw bite
is also specialized (Fig. 4). We can recognize a power stroke (ps) and a shorter release stroke (rs). During the power stroke
the levator posterior (LP), fourth levator
externus (LE4), sternohyoideus and pharyngocleithralis externus (PCE) are active.
Synchronous actions of the fourth levator
externus and levator posterior are summated, rotating the lower pharyngeal jaw
so that its tooth bearing posterior half
moves anterodorsally to press against the
stationary parasphenoid teeth. At the same
time the action of the pharyngocleithralis
externus muscle reinforces the rotation or
bite against the parasphenoid teeth by acting as the second force in a force couple.
Action of the pharyngohyoideus muscle
(PH), aided by synchronous action of the
geniohyoideus muscle during the release
stroke (rs), pulls the lower pharyngeal jaw
back into the resting position. Thus, mastication in Anabas is realized by the rotational movements of the lower pharyngeal
jaw while the upper pharyngeal jaws (Fig.
IB, C: upj) are recruited only during swallowing by actions of the levatores interni
and retractor dorsalis muscles. Such a
sharp division of functions in the pharyngeal jaw apparatus is a specialization not
encountered in any teleostean group outside the anabantoids.
Phylogenetic implications. The data obtained by functional analysis indicate that
a true "parasphenoid bite" is restricted to
Pristolepis and the Anabantoidei.
9
Although the toothed parasphenoid, basihyal and third hypobranchial in Nandus
(Fig. ID), Badis (Fig. IE) and Channa seem
to resemble those of Pristolepis (Fig. 1A)
and the Anabantoidei (Fig. IB, C), they are
actually not comparable. In Nandus, Badis
and Channa, the toothed parasphenoid
and ventral elements constitute components of a functional complex involved in
a primitive swallowing mechanism, which
occurs in many generalized acanthopterygian lineages and unrelated basal euteleosteans. The dental characters in Nandus, Badis and Channa are not integrated
with either a specialized biting or swallowing apparatus but seem to perform their
original function as hooking devices to
prevent the prey from moving forward
during the primitive mode of swallowing.
Thus the presence of parasphenoid teeth
and toothed basihyal and third hypobranchials in the Nandidae, Badis and Channidae are primitive characters and thus
provide no meaningful phylogenetic information.
In sharp contrast, the toothed parasphenoid, basihyal and third hypobranchials in
Pristolepis are integral components of a
very specialized functional complex, which
is responsible for a unique tongue-parasphenoid bite. Both functionally and morphologically this tongue-parasphenoid bite
is specialized, involving complicated subdivisions of the geniohyoideus muscle, occluding and grinding movements of the
unusually expanded basihyal, and very
complex, multiple muscle contractions
which indicates the presence of special
neuronal circuits. Thus the specialized and
complex tongue-parasphenoid bite in Pristolepis is not comparable to the more primitive, stereotyped manipulatory and swallowing mechanisms of the Nandidae, Badis
and Channidae. Although the presence of
teeth on the parasphenoid, basihyal and
third hypobranchial in Pristolepis may be
primitive, the character has been incor-
PHARYNGOGNATH TELEOSTS
89
porated into a very specialized, complex, lowing apparatus in nandids and channids
and well circumscribed functional com- are primitive, and do not indicate phyletic
plex, the nature of which is more mean- relationships with Pristolepis. Monophyly
ingful and informative in phylogenetic of the Anabantoidei is substantiated by the
studies than are the dental features viewed unique lower pharyngeal jaw-parasphe01 isolation.
noid bite, which is functionally separated
Another specialized bite involving para- from the swallowing mechanism. It is possphenoid teeth is found in the Anaban- sible that Badis (Fig. IE) and the Anabantoidei. Here the parasphenoid bite occurs toidei share the subdivision of the parabetween the lower pharyngeal jaw (fifth sphenoid-lower pharyngeal jaw bite and
ceratobranchials) and the teeth located on the upper pharyngeal jaw swallowing
the posterior extremity of the parasphe- mechanism. Morphologically, Badis posnoid (Fig. IB, C: ps, lpj). Functionally and sesses all the necessary specializations (i.e.,
morphologically the bite is specialized, in- parasphenoid teeth on the posterior exvolving a special ligament, muscular mod- tremity of the parasphenoid (Fig. IE),
ifications and complex action patterns in hypertrophied fourth levator externus
the levator posterior, levator externus, and levator posterior muscles) for a lowsternohyoideus, and pharyngocleithralis er pharyngeal jaw-parasphenoid bite,
externus muscles (Fig. 4). The upper pha- but, unfortunately its small size has been
ryngeal jaws and retractor dorsalis muscles a hindrance in testing the hypothesis
are functionally separated from the bite, experimentally. Thus the hypothesis that
being active mainly during swallowing Badis and the Anabantoidei share a recent
common ancestry (Barlow et al., 1968) re(Fig. IB, C: upj).
Such a distinct division of labor (masti- mains to be tested by other methods.
cation by the parasphenoid—lower pharynThe hypothesis that Pristolepis and the
geal jaw bite, and swallowing by fore-and- Anabantoidei are related on the basis of
aft movements of the upper pharyngeal their possessing parasphenoid teeth must
jaws) has not been recorded outside the be rejected. The tongue-parasphenoid bite
Anabantoidei. Mastication and swallowing of Pristolepis differs significantly from the
are controlled by complex and relatively anabantoid lower pharyngeal jaw-paraindependent neuronal circuits which de- sphenoid bite, because although both bitviate drastically from those in Pristolepis ing mechanisms are specialized, they inand more generalized acanthopterygians. volve different muscle groups, nerves,
The presence in anabantoids of teeth on neuronal circuits in the central nervous
the posterior extremity of the parasphe- system and biomechanical patterns. The
noid reflects how an originally primitive gradualistic hypothesis stating that: (1)
character can take up a new meaning by There has been a tendency toward a gradbeing integrated into a specialized func- ual posterior shift of the teeth on the ventional and morphological complex which tral elements during the evolution of prisnot only plays an important biological role tolepids, nandids, and anabantoids; (2)
but also indicates a common ancestry for and "it is easy to imagine how the peculiar
all taxa possessing it.
condition of anabantoids could have arisen
On the basis of the functional morpho- by a backward shift of the bite of the paralogical data presented here, the hypothesis sphenoid teeth, with the result that they
that nandids, pristolepids, channids and came to oppose the lower pharyngeals"
even anabantoids are closely related to one (Nelson, 1969, p. 496) cannot be supportanother must be rejected. The features as- ed, because even though such a toposociated with the tongue-parasphenoid graphical shift of the primitive tooth plates
bite in pristolepids are specialized and may have evolved by simple morphogeunique, making them autapomorphic for netic mechanisms, the tongue-parasphePristolepis. The dentition on the parasphe- noid and lower pharyngeal jaw-parasphenoid, basihyal and third hypobranchial noid bites are based on radically different
and all features associated with the swal- muscular, neuronal and biomechanical
90
K. F. LIEM AND P. H. GREENWOOD
Although functional analysis has been
useful in testing existing hypotheses on the
interrelationships of acanthopterygian
fishes with parasphenoid teeth, it has not
indicated the precise sister group relationships of the Pristolepidae, Nandidae, B a ^
idae, Anabantoidei, and Channiformes.
PHARYNGOGNATHY: THE FORMULATION
OF A PHYLOGENETIC HYPOTHESIS
What is pharyngognathy ?
FIG. 5. On left is the lateral view of the branchial
apparatus and muscles after removal of operculum,
suspensory apparatus, gills, gill rakers and mucous
membrane in Petrochromis fasciatus (Cichlidae). On
right are the myograms during a masticatory cycle
when the fish is feeding on hard food. Vertical interrupted lines delineate the boundaries of the three
strokes during each masticatory cycle: P, (power
stroke 1), T (transitional stroke) and P2 (power
stroke 2), ad2_5, second-fifth adductors; ao, adductor operculi; bl, Baudelot's ligament; cb,_5, first-fifth
ceratobranchial; cl, cleithrum; es, esophagus; gh,
geniohyoideus; Ie2_4, second-fourth levator externus; li,,2, first and second levator internus; lp, levator
posterior; pb,, first pharyngobranchial; pee, pharyngocleithralis externus; pci, pharyngocleithralis internus; ph, pharyngohyoideus; pp, process on sphenotic; rd, retractor dorsalis; uh, urohyal; v,_4, firstfourth vertebra; va, ventral apophysis on fourth vertebra.
specializations. The gradualistic hypothesis deriving the anabantoid parasphenoidlower pharyngeal jaw bite from the pristolepid tongue-parasphenoid bite is further weakened by the fact that the postulated evolutionary intermediate, the
Nandidae, possesses the primitive swallowing mechanism involving the toothed basihyal, parasphenoid and third hypobranchial. The functional data indicate
independent phylogenetic origins for the
pristolepid tongue-parasphenoid bite and
the anabantoid lower pharyngeal jawparasphenoid bites.
Some groups of advanced euteleosteans
possess fused fifth ceratobranchials (a lower pharyngeal jaw), opposing the upper
pharyngeal jaws, which articulate with
apophyses of the cranial base (Fig. IF: lpj,
upj; Fig. 9). The bite is therefore an upper-lower pharyngeal jaw bite. Fishes having those powerful pharyngeal jaws are referred to as being pharyngognathous; the
specialized "biting" mechanism involving
such specialized upper and lower pharyngeal jaws is often called pharyngognathy.
Among advanced euteleosteans, pharyngognathy is found in the Labroidei, Cyprinodontoidei, Embiotocidae, Cichlidae,
Pogonias, Girellidae, Anabantoidei, and
Pomacentridae. The question whether
pharyngognathous fishes are closely related has not been resolved {e.g., Giinther,
1862; Regan, 1913; Bertin and Arambourgh, 1958; Nelson, 1967). Functionally,
pharyngognathy is poorly understood, although numerous adaptive, evolutionary,
mechanical and ecological interpretations
have been published (e.g., Tarp, 1952;
Hiattand Strasburg, 1960; Quignard, 1962;
Nelson, 1967; De Martini, 1969; Chao,
1973; Rognes, 1973; Hobson, 1974; Sibbing, 1976; Yamaoka, 1978; Brett, 1979).
Pharyngognathy in Cichlidae
In all cichlids the upper pharyngeal jaws
are composed of the second, third and
fourth pharyngobranchials. Dorsally, the
third pharyngobranchial bears a prominent articular facet to form the basipharyngeal joint with the pharyngeal apophysis or process of the neurocranial base.
The upper pharyngeal jaws function as
one mechanical unit because of strong interconnections between the left and right,
PHARYNGOGNATH TELEOSTS
third pharyngobranchials. The lower
pharyngeal jaw is composed of fused
fifth ceratobranchials. The fourth levator
externus, and, in several taxa (e.g., Tylo-
91
(Liem, 1978). The functional consequence
of the insertion of the greater bulk of the
fourth levator externus and in many cichlids the levator posterior (Fig. 9 A: le4, lp)
chromis, many species of Cichlasoma, some on the muscular process of the lower pha^Decies of Haplochromis and Lamprologus), ryngeal jaw is that the latter has become
the levator posterior have split into lateral suspended in a muscular sling, part of
and medial components. The small lateral which can be kept in continuous tension
components insert on the dorsal aspect of because of the uninterrupted activity of
the fourth epibranchials, while the domi- the fourth levator externus muscle. Such
nant medial components bypass the dorsal an organization facilitates the control of
gill arch element to insert on the muscular protrusion, retrusion, and lateral translaprocess of the lower pharyngeal jaw (Fig. tion, as well as rotation about three axes,
5: le4; Fig. 9: le4, lp).
of the lower pharyngeal jaw. Within this
Biomechanically the pharyngognathous functional-morphological pattern the bitmechanism of cichlids exhibits a distinc- ing force can be greatly enhanced because
tively specialized triphasic pattern. The during power stroke 2 synchronous acfourth levator externus is dominant, being tions of the fourth levator externus and
active throughout the masticatory cycle, the pharyngocleithralis externus muscles
while the levator poSLerior is active syn- (Fig. 5: le4, pee) will result in a force couchronously with the fourth levator exter- ple. It is clear that pharyngognathy in cichnus during the last two phases of the tri- lids is characterized by specialized morphasic masticatory cycle (Fig. 5: le4, lp; Fig. phological and functional patterns.
4: Lobochilotes, LP, LEi). This pattern dif- At first (Liem, 1973) it was thought that
fers vastly from the alternating pattern of these specialized and complex patterns, inshort bursts of the two muscles in Anabas volving multiple morphological and funcand Pristolepis (Fig. 4) and Lepomis (Lau- tional characters, were unique to the Cichder, personal communication).
lidae and therefore indicative of
Cichlid pharyngognathy is further monophyly. However, as our knowledge
characterized by the triphasic pattern con- on pharynogognathy has expanded, we
sisting of two power strokes separated by find that the Cichlidae can no longer be
a "transitional stroke" (Figs. 4, 5: ps r , ps2, defined on the basis of the morphological
ts). Power stroke 1 is correlated with ac- and functional patterns of their pharyntions by the fourth levator externus, leva- geal jaws. As will be shown below, several
tores interni and geniohyoideus muscles other major acanthopterygian assemblages
(Fig. 5: le4, li, gh), and by protraction and seem to share this specialized pharyngorotation of both the lower and upper pha- gnathy with the cichlids.
ryngeal jaws, which move toward each other. The transitional stroke is accompanied Embiotocidae-Cichlidae resemblances
by activity in the fourth levator externus,
With respect to pharyngeal jaw anatolevator posterior, retractor dorsalis, and my, all members of the surfperch family
pharyngohyoideus (Fig. 5: le4, lp, rd, ph) Embiotocidae possess specializations which
and involves retraction and rotation of the are identical to those of the Cichlidae. The
lower and upper pharyngeal jaws, which fifth ceratobranchials are united into a sinnow move apart slightly. Power stroke 2 is gle lower pharyngeal jaw (Nelson, 1967;
characterized by high amplitude actions of Fig. 6, Ditrema) with posterodorsally dithe fourth levator externus, levator pos- rected, prominent muscular processes.
terior, retractor dorsalis, pharyngocleith- Each upper pharyngeal jaw is composed of
ralis externus and internus, and sternohy- the third pharyngobranchial, which is
oideus (Fig. 5: le4, lp, rd, pee, pci, sh), either fused or united with the fourth upcausing strong rotation of both the upper per pharyngeal toothplate (Nelson, 1967).
and lower pharyngeal jaws so that their The upper pharyngeal jaw articulates with
posterior ends approximate each other the skull base via an apophysis on a pha-
92
K. F. LIEM AND P. H. GREENWOOD
DITREMA
uh
ph
FIG. 6. Lateral view of branchial apparatus and muscles after removal of opercular, suspensory apparatus,
gills, gill rakers, and mucous membrane of Ditrema (Embiotocidae), Labrus (Labridae), Scarus (Scaridae), and
Odax (Odacidae). ad, adductor branchials; ad5, fifth adductor; ao, adductor operculi; cb,_s, first-fifth ceratobranchial; cb 5 , lower pharyngeal jaw; cl, cleithrum; eb, epibranchial; eb,_4, first-fourth epibranchial; es,
esophagus; 1, ligament between cleithrum and lower pharyngeal jaw; lei_3, first—third levator externus; le4,
fourth levator externus; li, levator internus; lp, levator posterior; od, obliquus dorsalis; pee, pharyngocleithralis externus; pci, pharyngocleithralis internus; pej, pharyngocleithral joint; ph, pharyngohyoideus; rab,
retractor arcus branchialis (retractor dorsalis); rd, retractor dorsalis (retractor arcus branchialis); sh, sternohyoideus; sph, sphenotic; uh, urohyal.
ryngeal process of the parasphenoid (Mor- and the muscular processes of the lower
ris and Gaudin, 1976) and an articular pharyngeal jaw (Figs. 6, 7: le4, lp). As in
apophysis on the dorsal aspect of the third cichlids, the fourth levator externus muspharyngobranchial (Fig. 7: apu). Both the cle is always the larger of the two, in refourth levator externus and levator pos- spect to both its volume and cross-sectional
terior muscles are differentiated into small area. Morphologically and topographically
lateral and large medial heads, inserting the pharyngocleithralis externus and inrespectively on the fourth epibranchials ternus, and the pharyngohyoideus muscles
PHARYNGOGNATH TELEOSTS
93
EMBIOTICA
apu
Fie. 7. Dorsal view of dissected and isolated branchial apparatus of Embiotoca (Embiotocidae), Centrolabrus
(Labridae), Odax (Odacidae) and Scarus (Scaridae). ad, adductor branchialis; ad,. 3 , first-third adductor; apu,
articular apophysis of the upper pharyngeal jaw; cb, ceratobranchial; cb!_5, first-fifth ceratobranchial; eb,_4,
first-fourth levator externus; li, levator internus; lp, levator posterior; od, obliquus dorsalis; pb, pharyngobranchial; rd, retractor dorsalis; tda, transversus dorsalis anterior; tdp, transversus dorsalis posterior.
of embiotocids are identical to those of
cichlids (Figs. 6, 8A: pee, pci, ph).
Based on the morphological data of the
pharyngeal jaw apparatus in embiotocids,
and the functional evidence from cichlids,
the following activity hypothesis is proposed: Prior to swallowing, prey or food
caught between the occlusal surfaces of the
toothed lower and upper pharyngeal jaws
can be crushed, triturated, macerated,
compacted or in other ways prepared depending on the nature of the pharyngeal
dentition. Because the dominant medial
heads of the fourth levator externus and
levator posterior are inserted on the muscular process of the lower pharyngeal jaw
94
K. F. LIEM AND P. H. GREENWOOD
"e.
FIG. 8. Lateral view of branchial apparatus and muscles after removal of opercular apparatus, suspensorium,
gills, gill rakers and mucous membrane of A, Lamprologus tretocephalus (Cichlidae, molluscivorous); B, Nexitarius
taunts (Pomacentridae); C, Anabas testudineus (Anabantidae, dorsal part of the labyrinthine first epibranchial
had been removed); D, Girella tricuspidata (Girellidae); E, Pogonias chromis (Sciaenidae). ad,_5, first-fifth
adductor branchialis; ao, adductor operculi; cb,_5, first-fifth ceratobranchial; cl, cleithrum; eb,_4, first-fourth
epibranchial; eel, epibranchial-ceratobranchial ligament; 1, ligament between cleithrum and lower pharyngeal
PHARYNGOGNATH TELEOSTS
(Fig. 6: le4, lp) it is mechanically possible
for the latter to perform a wide range of
actions (Fig. 8). Potentially the embiotocid
lower pharyngeal jaw can produce not
only a strong bite, but also numerous other
•finely controlled movements since it is suspended in a muscular sling (Figs. 6, 8),
part of which can be kept in continuous
and varying tensions.
Preliminary comparative and functional
studies have revealed that the embiotocidcichlid resemblances are not restricted to
the basic functional design of the pharyngeal jaw apparatus but include the myological and osteological modifications accompanying such trophic specializations as
molluscivory and piscivory (Brett, 1979).
The embiotocid-cichlid resemblances involve all morphological specializations of
the multiple components making up the
pharyngeal jaw apparatus. The only differences are found in the first two gill
arches, which do not contribute to the upper pharyngeal jaw apparatus, and in the
transversus dorsalis anterior muscle not
being subdivided to the extent it is in cichlids (Fig. 7: tda; Anker, 1978). In embiotocids the second pharyngobranchial is
toothless (Nelson, 1967).
The labrold pharyngeal jaw apparatus
The labroids (Labridae, Odacidae and
Scaridae) have a very specialized pharyngeal jaw apparatus, which resembles that
of the embiotocids and cichlids in several
salient aspects: (1) The fifth ceratobranchials are united into a single lower pharyngeal jaw with posterodorsally directed,
prominent muscular processes (Nelson,
1967; Fig. 6: cb5; Fig. 9); (2) Each upper
pharyngeal jaw is composed of the third
pharyngobranchial and the fourth upper
pharyngeal toothplate (Nelson, 1967); (3)
The upper pharyngeal jaws articulate with
the skull base by means of articular apophyses on the dorsal aspect of the third
95
pharyngobranchials (Yamaoka, 1978; Figs.
8, 9: apu); (4) Both the fourth levator externus and levator posterior are differentiated into small lateral and large medial
components inserting, respectively, on the
fourth epibranchial and the muscular process of the lower pharyngeal jaw (Yamaoka, 1978; Figs. 6, 7, 9: le4) lp). However,
in the labroid pharyngeal jaw apparatus
the levator posterior is the dominant muscle (Yamaoka, 1978; Figs. 6, 7, 9: lp), and
the lower pharyngeal jaw is no longer a
free-floating element. In labroids, the lower pharyngeal jaw articulates with a distinct articular process on the cleithrum
(Figs. 6, 9: pcj). This joint, characteristic
for labroids, will be called the pharyngocleithral joint. Mechanically, the pharyngocleithral joint serves as the fulcrum of
the lower pharyngeal jaw, which has become transformed into a lever (Fig. 9: pcj).
Because the levator posterior and the
pharyngocleithralis externus muscles exert
forces in opposite directions around a fulcrum provided by the pharyngocleithral
joint, we are dealing with a force couple
(Fig. 9: lp, pee, pcj). The pharyngocleithral
joint is a synovial joint enhancing loading,
smoothness of movement and lubrication
without any tendency to jamming, even
under very variable conditions (Liem,
1977, pp. 192-193).
The activity hypothesis for the labroid
pharyngeal jaw apparatus proposed here
is derived from comparative morphological data and preliminary functional observations. Functionally and morphologically,
labroid pharyngognathy seems only to be
a variation on the basic functional design
seen in embiotocids and cichlids. The levator posterior and fourth levator externus appear to act on the lower pharyngeal
jaw in the same way as in the cichlids and
embiotocids (Fig. 9: lp, le4). The basic difference is that with the appearance of a
pharyngocleithral joint the labroid lower
jaw, le!_4, first-fourth levator externus; Ii, levator internus; lp, levator posterior; pee, pharyngocleithralis
externus; pci, pharyngocleithralis internus; pcj, pharyngocleithral joint; ph, pharyngohyoideus; pp, protractor
pectoralis; rab, retractor arcus branchialis (retractor dorsalis); rd, retractor dorsalis (retractor arcus branchialis); sh, sternohyoideus; tv, transversus ventralis; uh, urohyal.
96
K. F. LIEM AND P. H. GREENWOOD
CICHLID
A
FIG. 9. Diagrammatic representation of the principal components of the pharyngeal jaw apparatus of cichlids, embiotocids, labrids and scarids. Shaded elements are the upper and lower pharyngeal jaws. The neurocranium and first vertebra are drawn as complete structures. In each diagram the dorsal half of the cleithrum has been eliminated. In the cichlid and embiotocid the hyoid is indicated in a simplified form, while in
the labrid and scarid the hyoid has been omitted. The muscles are represented as lines and the principal
direction of force has been indicated by arrows. Anatomical and functional dominance is indicated by a
heavier line. In the cichlid-embiotocid the non-articulated lower pharyngeal jaw is suspended in a muscular
sling, of which the fourth levator externus (le() is dominant. In the labrid and scarid, lower pharyngeal jaw
articulates with the cleithrum, and the dominant levator posterior (Ip) in conjunction with the pharyngocleithralis externus (pee) form a force couple. le4, fourth levator externus; li, levator internus; Ip, levator
posterior; pee, pharyngocleithralis externus; pci, pharyngocleithralis internus; ph, pharyngohyoideus; rd,
retractor dorsalis.
pharyngeal jaw is not suspended from a
muscular sling as it is in cichlids and embiotocids. Of course a pharyngocleithral
joint does impose limitations on movements in some directions, but it also provides a fulcrum, which offers mechanical
advantages where power is required in the
bite. In the Scaridae, additional specializa-
tions can be seen (Figs. 6, 7, 9), all leading
to a mechanically favorable pharyngognathous system enhancing the biting
force. Thus the fourth levator externus,
levator posterior, fifth and fourth adductors, pharyngocleithralis externus and internus, the pharyngeal jaws themselves,
and both the basipharyngeal and pharyn-
PHARYNGOGNATH TELEOSTS
gocleithral joints are greatly hypertrophied (Figs. 6, 7, 9).
The supposed kinematic profile of labroid pharyngognathy presented here is
based on experimental data from cichlids
wnd detailed comparative myology, arthrology and osteology of all pharyngognathous taxa. Experimental studies testing the
hypothesis that labroid, embiotocid and
cichlid pharyngognathy share not only
morphological but also functional resemblances are currently being performed.
Other pharyngognathous acanthopterygians
(Pomacentridae, Anabantoidei,
Sciaenidae, Girellidae)
Pharyngognathy in all other acanthopterygians differs both morphologically and
functionally from that encountered in the
Cichlidae-Embiotocidae-Labroidei type.
In the Pomacentridae (e.g., Fig. 8B: le,
lp) the fourth levator externus and levator
posterior insert on the dorsal aspect of the
fourth epibranchial. The lower pharyngeal jaw is acted upon by the ventral gill
arch muscles only i.e., pharyngocleithralis
externus and internus, pharyngohyoideus
and fifth adductor (Fig. 8B: pee, pci, ph,
ad). Thus, kinematically, the pharyngeal
jaws of pomacentrids resemble those of
more generalized acanthopterygians, even
though the left and right fifth ceratobranchials are united to form a single lower
pharyngeal jaw, and the upper pharyngeal
jaws articulate with the skull base by means
of basipharyngeal joints. In pomacentrids
feeding habitually on hard foods, the fifth
adductor, the pharyngohyoideus and
pharyngocleithralis externus are hypertrophied, indicating their dominant role in
operating the lower pharyngeal jaw, while
both dorsal muscles (the levator posterior
and fourth levator externus) remain relatively unmodified.
From these comparative morphological
data we may conclude that in pomacentrids the lower pharyngeal jaw can occlude
against the upper pharyngeal jaws by the
actions of the fifth adductor and pharyngocleithralis externus muscles, while at the
same time the upper pharyngeal jaws can
undergo translational movements through
97
the actions of the fourth levator externus
and levator posterior muscles. The pomacentrid kinematic pattern of pharyngognathy, although well suited for crushing, trituration and shearing, differs drastically
from that of cichlids-embiotocids-labroids,
because it is based on an entirely different
morphological pattern in which the dorsal
gill arch musculature remains independent from that of the lower pharyngeal
jaw.
Although the Anabantoidei possesses a
single lower pharyngeal jaw formed by
united fifth ceratobranchials (Fig. 1, 8C),
the electromyographic and kinematic patterns are uniquely specialized, differing
significantly from those of the cichlid-embiotocid-labroid type (compare Anabas and
Lobochilotes in Fig. 4). The fourth levator
externus and levator posterior muscles
play a dominant role in executing the lower pharyngeal jaw-parasphenoid bite (Fig.
4: LP, LE4). Anatomically the stout epibranchial-ceratobranchial ligament (Fig.
8B: eel) plays a key role in transferring the
forces generated by the fourth levator externus and levator posterior from the
fourth epibranchial (Fig. 8: eh,) to the lower pharyngeal jaw (cb5). Thus pharyngognathy in the Anabantoidei represents a
uniquely specialized character complex
both functionally and morphologically.
Among sciaenids, Pogonias chromis has
very robust pharyngeal jaws with molariform teeth. Crushing movements of the
lower against the upper pharyngeal jaws
in Pogonias result from the actions of the
greatly hypertrophied pharyngohyoideus,
pharyngocleithralis externus and internus
and fifth adductor muscles (Fig. 8E: ph,
pee, pci, ad5). The specialized and prominent ventral processes on the lower pharyngeal jaw serve not only as enlarged insertion sites but also enhance the
mechanical efficiency of the three massive
ventral muscles. In Pogonias the generation of biting force is restricted to the lower pharyngeal jaw while the upper jaw,
with its generalized musculature, does not
actively participate in the bite, except as a
well supported foundation against which
a forceful bite can be executed. From this
morphological pattern we may postulate
98
K. F. LIEM AND P. H. GREENWOOD
that occlusion takes place by rotation of the
lower pharyngeal jaw so that its posterior
corner moves anterodorsally against the
fixed upper pharyngeal jaw.
Finally, in the Girellidae pharyngognathy is probably the least specialized (Fig.
8D). The upper pharyngeal jaws are freefloating as in generalized percoids. The
united fifth ceratobranchials form a distinct lower pharyngeal jaw, which is associated with relatively elongate ventral muscles
(pharyngohyoideus, pharyngocleithralis externus and internus) in a configuration
reminiscent of that in generalized percoids
(Fig. 8D: pee, pci, ph, cb5). Besides the
single lower pharyngeal jaw, the only specialized feature in the pharyngeal jaw apparatus of Girella is the loss of the levator
posterior muscle (Fig. 8D). It is clear that
the morphological pattern and its functional correlates make pharyngognathy of
Girella different in all basic features from
that in the cichlid-embiotocid-labroid lineage.
The morphological and tunctional data
on pomacentrids, girellids, anabantoids,
and Pogonias have revealed that pharyngognathy, when viewed comprehensively
as a major, integrated pattern, can be subdivided into four distinct categories, each
having its own and unique functional and
anatomical specializations.
The Cichlidae-Embiotocidae-Labroidei as a
monophyletic assemblage
We propose the hypothesis that the
Cichlidae, Embiotocidae, Labridae, Odacidae, and Scaridae are more closely related to each other than to any other teleostean group, because they share a uniquely
specialized pharyngognathy. The two key
specializations (Fig. 10: 1, 2) are: (1) The
major component of the fourth levator externus inserts invariably on the lower pharyngeal jaw, which is formed by united
fifth ceratobranchials. Except in some cichlids, the levator posterior also possesses a
major component inserting on the muscular process of the lower pharyngeal jaw
(Fig. 9; Hoogerhoud and Barel, 1978); (2)
The pharyngeal bite proceeds by coordinated movements of the lower and upper
pharyngeal jaws in such a way that the
fourth levator externus together with the
levator posterior and the pharyngocleithralis externus form the two components of
a force couple acting on the lower pharyngeal jaw (Figs. 5, 9; Liem, 1978). The
fourth levator externus and levator po.^
terior are functionally and morphologically the dominant muscles of the lower pharyngeal jaw (Figs. 4-6, 9). Kinematically
the bite occurs when the posterior ends of
both the upper and lower pharyngeal jaws
move anterodorsally and toward each other (Liem, 1978). These specialized character complexes are not shared by any other teleostean group.
Our hypothesis that cichlids, embiotocids and labroids are members of a monophyletic assemblage assumes that it is highly improbable that the morphological
(basipharyngeal joint, united fifth ceratobranchials, major components of the
fourth levator externus and levator posterior inserting on the lower pharyngeal
jaw) and functional specializations (mastication by 2 power strokes, occlusion by the
anterodorsal movements of the posterior
ends of both the lower and upper pharyngeal jaws, the fourth levator externus together with the levator posterior, sternohyoideus, and pharyngocleithralis play a
dominant role in the kinematics of the lower pharyngeal jaw, and the neuronal circuitry governing the firing patterns of the
pharyngeal muscles) have arisen independently in phyletically unrelated lineages.
Because they have specialized drastically
along very different morphological and
functional lines, we reject the hypothesis
that any of the other pharyngognathous
acanthopterygians are related to this lineage.
Within this monophyletic assemblage we
can recognize two lineages containing respectively the cichlids-embiotocids and the
labrids-odacids-scarids. The lineage containing the Cichlidae and Embiotocidae
possesses a lower pharyngeal jaw that is
suspended in a muscular sling with the
fourth levator externus being dominant
both morphologically and functionally
(Fig. 9A, B; Fig. 10). Other components of
the muscular sling are the pharyngohyoideus, pharyngocleithralis externus and in-
99
PHARYNGOGNATH TELEOSTS
ternus and the fifth adductor muscles. The
anatomical and functional dominance of
the fourth levator externus in this lineage
(Fig. 10: 3) is correlated with the muscular
sling mechanism, which enables the lower
^bharyngeal jaw to rotate around three axes
and undergo protraction and retraction.
Extensive overlap in the firing sequences
of the component muscles of the muscular
sling enhances the versatility, precision
and control of the movements of the lower
pharyngeal jaw (e.g., Greenwood, 1973,
1974; Liem, 1973; Liem and Osse, 1975;
Hoogerhoud and Barel, 1978). The dominance of the fourth levator externus and
the muscular sling can be considered a
unique, specialized complex characterizing
the Cichlidae-Embiotocidae lineage.
In the labroid lineage (Fig. 10), the levator posterior is dominant (Fig. 9C, D;
Fig. 10: 4) and the lower pharyngeal jaw
articulates with the cleithrum by means of
a pharyngocleithral joint (Fig. 10: 5; Fig.
9C, D: pcj). Labroid pharyngognathy is
mechanically specialized by the development of a force couple acting on the lower
pharyngeal jaw. Dominance of the levator
posterior and pharyngocleithralis externus
muscles in labroids reflects the importance
of the two forces of the couple, while the
pharyngocleithral joint represents the fulcrum around which the two forces work.
In the labroid lineage the lower pharyngeal jaw is stabilized by the pharyngocleithral joint. Although such a construction is
conducive to mechanical strength and the
force of the pharyngeal bite, labroid pharyngognathy does not possess the functional versatility so characteristic of the
pharyngeal muscular sling in the cichlidembiotocid lineage. Monophyly of the labroid lineage is further supported by the
reduction or loss of the first pharyngobranchial (Fig. 10: 6) and hypertrophy of
the adductor muscles of the branchial
arches (Fig. 10: 7; Figs. 6, 7: ad).
Within our proposed phylogenetic
scheme, the Labridae, Odacidae and Scaridae are depicted as an unresolved trichotomy, since our data on pharyngognathy are
insufficient to propose the relationships
more precisely.
The Cichlidae can be distinguished by a
CICHLIDAE
EMBOTOCIDAE
LABRIDAE
ODAQDAE
SCAR1DAE
FIG. 10. Proposed hypothesis of the phylogenetic
relationships of pharyngognathous acanthopterygians, primarily based on functional morphological
data. Various characters are indicated by a black bar
at the appropriate level. The characters are: 1, fourth
levator externus and levator posterior insert on muscular process of lower pharyngeal jaw, composed of
united fifth ceratobranchials; 2, the pharyngeal bite
occurs when the posterior ends of both the upper
and lower pharyngeal jaws move anterodorsally and
toward each other by coordinated actions of associated muscles which are active throughout the masticatory cycle; 3, lower pharyngeal jaw is suspended in
a muscular sling of which the fourth levator externus
is dominant both morphologically and functionally;
4, the levator posterior is the dominant muscle of the
lower pharyngeal jaw forming a force couple together with the pharyngocleithralis externus muscle; 5,
the lower pharyngeal jaw articulates with the cleithrum by means of pharyngocleithral joint; 6, loss or
reduction of the first pharyngobranchial; 7, hypertrophy of the adductor branchialis muscles; 8, the
transversus dorsalis anterior muscle is subdivided
into four parts; 9, single nostril on each side; 10, loss
of teeth of the second pharyngobranchial; 11, viviparous mode of reproduction.
very highly differentiated and complexly
subdivided transversus dorsalis anterior
muscle (Fig. 10: 8; Anker, 1978). It is composed of four parts: Part 1 (pars dorsalis
of the transversus epibranchialis 2, sensu
Anker, 1978) runs from the dorsal face of
the second epibranchial towards a median
flat aponeurotic band; Part 2 arises from
the caudal face of the second pharyngobranchial to attach on the same flat aponeurotic band as part 1; Part 3 connects
the rostral face of the left and right second
pharyngobranchials; Part 4 runs between
the 2nd pharyngobranchial and the neu-
100
K. F. LIEM AND P. H. GREENWOOD
rocranium. Such a specialized quadripartite transversus dorsalis anterior muscle
does not occur in pomacentrids and generalized percoids. Monophyly of the cichlid lineage is further supported by the single nostril on each side (Fig. 10: 9).
The Embiotocidae cannot be defined on
the basis of a specialized feature of the
branchial apparatus except for the loss of
teeth on the second pharyngobranchial
(Fig. 10: 10; Nelson, 1967). However, the
group can be characterized by its specialized viviparous reproductive mechanism
(Fig. 10: 11).
CONCLUSION
phology to phylogenetic studies is that it
can serve as a new appraoch to test and
formulate hypotheses on phyletic relationships. Of course, most other major goals
of functional morphology can best be
achieved within a well founded phylogd^
netic context so that historical factors can
be included in the explanation of animal
form.
ACKNOWLEDGMENTS
This research was supported in part by
a fellowship from the John Simon Guggenheim Memorial Foundation, New York,
and NSF grant DEB 79-00955 to KFL. We
are greatly indebted to both foundations.
We are especially grateful to Dr. David M.
Gardiner of Occidental College for supplying us with embiotocids. KFL has benefited from discussions with John E. Randall, George Losey, W. MacFarland, William
and Sara Fink. George V. Lauder, Jr. has
improved the manuscript and offered
valuable assistance in the completion of
this study. Karsten Hartel, Gordon Howes,
James Chambers, and Christine Fox have
contributed their knowledge and skills
making it possible to bring this study to a
successful end. This study is based on collections of the Museum of Comparative
Zoology and the British Museum (Natural
History). Finally, we would like to thank
the New England Aquarium and Mr. L.
Garibaldi for their cooperation.
In this case study we have tried to demonstrate that functional morphology can
be used as a tool to test phylogenetic hypotheses. Functional morphology, by focussing on the nature of the mutual influences, interdependence and interacting
constraints existing between structural elements, can put purely morphological characters, previously viewed in isolation, into
a more precise and informative context. As
a result of our functional studies several
phylogenetic hypotheses have to be rejected. During our functional studies on pharyngognathy in acanthopterygians, our attention has been directed to several
specialized character complexes with distinct patterns that yielded important phylogenetic information. On the basis of
functionally integrated patterns of characters a new hypothesis of phyletic relaREFERENCES
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PHARYNGOGNATH TELEOSTS
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