Ontogeny of the hyoid musculature in the African catfish, Clarias … · 1999-08-20 · r-br radius...

Zoological Journal of the Linnean Society (1997), 121: 105–128. With 9 figures

Ontogeny of the hyoid musculature in theAfrican catfish, Clarias gariepinus (Burchell, 1822)(Siluroidei: Clariidae)

DOMINIQUE ADRIAENS AND WALTER VERRAES

Institute of Zoology, University of Ghent, K.L. Ledeganckstraat 35, B-9000 Ghent, Belgium

Received December 1995; accepted for publication November 1996

Three ontogenetic stages of the African catfish Clarias gariepinus have been used to describeand discuss the ontogeny of the hyoid musculature. During ontogeny, an asynchrony in thedevelopment of the muscles is observed: the intermandibularis and protractor hyoidei arethe first to develop and which bear their insertions, followed by the hyohyoideus inferiorand the sternohyoideus. The hyohyoideus abductor and adductor muscles are the last of thehyoid muscles to develop. In the juvenile stage (136.2 mm SL specimen), the intermandibularisis still present. The protractor hyoidei is well developed, as it may play an important role inthe opening of the mouth, the elevation of the hyoid bars and, as a typical catfish feature,the displacement of the mandibular barbels. The protractor hyoidei arises as three pairs ofmuscle bundles (a pars ventralis, a pars lateralis and a pars dorsalis), of which the parsventralis and the pars lateralis become fused to each other. This fusion gives rise to fourdifferent fields of superficial fibres for the manipulation of the mandibular barbels. The parsdorsalis, with its tendinous insertion, may be of more importance for mouth opening and/or hyoid elevation. The hyohyoid muscle is well differentiated into an inferior, abductor andadductor muscles, acting on the hyoid bars, the branchiostegal rays and the opercular bone.

1997 The Linnean Society of London

ADDITIONAL KEY WORDS:—catfish – ontogeny – myology – hyoid – intermandibular– barbels.

CONTENTS

Introduction . . . . . . . . . . . . . . . . . . . . . . . 106Material and methods . . . . . . . . . . . . . . . . . . . 107Abbreviations . . . . . . . . . . . . . . . . . . . . . . 108Results . . . . . . . . . . . . . . . . . . . . . . . . 109

7.2 mm SL (7 days posthatching) . . . . . . . . . . . . . . 10946.8 mm SL (120 days posthatching) . . . . . . . . . . . . . 111136.2 mm SL (100 days posthatching) . . . . . . . . . . . . . 116

Discussion . . . . . . . . . . . . . . . . . . . . . . . 120Conclusions . . . . . . . . . . . . . . . . . . . . . . . 125Acknowledgements . . . . . . . . . . . . . . . . . . . . 125References . . . . . . . . . . . . . . . . . . . . . . . 126

Correspondence to: Dominique Adriaens. E-mail: [email protected]

1050024–4082/97/090105+24 $25.00/0/zj960086 1997 The Linnean Society of London

D. ADRIAENS AND W. VERRAES106

INTRODUCTION

In actinopterygians the hyoid bars are well known to play an important role inmechanisms like respiration and suction feeding. The depression and elevation ofthe hyoid bar control the required changes in volume of the orobranchial cavity(Schaeffer & Rosen, 1961; Osse, 1969; Anker, 1974; Lauder, 1981; Schaefer &Lauder, 1986; Westneat & Wainwright, 1989; Westneat, 1990; Aerts, 1991). Anadditional participation of the hyoid bars in the suction feeding mechanism isestablished through the hyoideo-mandibular connection (Liem, 1970; Verraes, 1977;Lauder, 1980a,b; Lauder & Liem, 1980). The morphology and the attachment ofdifferent muscles contribute to the great mobility and functional significance of thesebars.

During teleostean evolution, the hyoid arch has become differentiated into twofunctional units: a dorsal hyosymplectic and a ventral hyoid bar, interconnected byan interhyal. In generalized teleosts, the hyosymplectic articulates with the postero-lateral face of the neurocranium, at the level of the otic capsules. At its anterior andposterior face it bears a process, the pterygoid and the opercular process, respectively.In general, the hyosymplectic arises separately from the palatoquadrate of themandibular arch, which during ontogeny become sutured to each other, thus formingthe suspensorium. The ventral part consists of a hyoid bar, supporting severalbranchiostegal rays along the ventral margin. Both elements of the hyoid archarticulate with each other through an interhyal, which is believed to be a newelement in the hyoid arch in teleostean fishes (Daget, 1964; Jarvik, 1980), althoughit has been observed in crossopterygians as well (e.g. Latimeria chalumnae) (Lauder,1980b). The presence of the interhyal plays an important role for the efficiency ofhyoid depression (Anker, 1974; Lauder, 1980a). In some cases, secondary reductionshave occurred within both the dorsal part (e.g. symplectic bone in catfishes (Alexander,1965; Roberts, 1973; Fink & Fink, 1981; Arratia, 1992)), the interhyal (e.g. incatfishes (Arratia, 1990, 1992; Adriaens & Verraes, 1994)) and the ventral part (e.g.dorsal hypohyal in some catfishes or ventral hypohyal in most Osteoglossomorpha(Arratia & Schultze, 1990)).

Ontogenetically three major muscles primordia can be distinguished which playan important role in formation of the hyoid musculature: (1) the intermandibularis,(2) the interhyoideus, and (3) the sternohyoideus (Takahasi, 1925; Munshi &Singh, 1967; Greenwood, 1971; Winterbottom, 1974; Jarvik, 1980; Surlemont &Vandewalle, 1991). The intermandibularis is derived from the intermandibularispart of the mandibular muscle plate. Early during ontogeny, this muscle becomessubdivided into an intermandibularis anterior and posterior. As is the case for allthe mandibular arch muscles, these muscles are innervated by the ramus mandibularisof the trigeminal nerve. The interhyoideus develops out of the muscle plate of thehyoid arch. The ventral part of the hyoid muscle plate, the constrictor hyoideusventralis becomes subdivided into an interhyoideus anterior and an interhyoideusposterior. All the muscles derived from the hyoid arch muscle plate are innervated bythe ramus hyomandibularis of the nervus facialis (ramus hyohyoideus in Greenwood(1971)). The third muscle, the sternohyoideus, is a differentiation of the hypobranchialmuscle plate of the first spinal myomeres which grows forward to the hyoid bars.Innervation occurs through the branches of the occipito-spinal nerves. Furtherdifferentiations of these three primary muscles, both by fusions and additionalsubdivision, give rise to the formation of the functional muscles of the hyoid bars.

ONTOGENY OF HYOID MUSCULATURE IN CLARIAS GARIEPINUS 107

Generally, six major muscles can be distinguished: (1) the intermandibularis, whichis homologous with the early intermandibularis anterior (Greenwood, 1971; Win-terbottom, 1974). This muscle becomes extended between the left and right man-dibular ramus, close to the symphysis. The intermandibularis posterior, however,generally fuses with the interhyoideus anterior, thereby forming (2) the protractorhyoidei. This fusion has led to a wide range of forms of the protractor hyoidei,thereby sometimes creating some uncertainties concerning the nomenclature (Green-wood, 1971; Winterbottom, 1974). In most teleosts, this muscle, frequently andincorrectly referred to as the geniohyoideus, connects the lower jaw with the hyoidbars (Anker, 1974; Winterbottom, 1974; Elshoud, 1978; Lauder & Liem, 1980;Lauder, 1979, 1981; Liem, 1984; Westneat, 1990). According to Greenwood (1971),however, “it is clear that on grounds of homology and ontogeny the muscle shouldnot be called a geniohyoideus in teleost fishes”. It has been shown that “the teleostean‘geniohyoideus’ is in no way homologous to that of the tetrapods, from which thename has been taken” (Winterbottom, 1974). However, some functional shifts haveoccurred in Ostariophysi, as will be discussed later. The interhyoideus posterior willgive rise to the hyohyoideus, which generally becomes subdivided into three functionalmuscles. (3) The hyohyoideus inferior connects the ipsi-lateral hyoid bars, therebyinserting medially on an aponeurosis. (4) The hyohyoideus abductor connects theanteriormost branchiostegal ray to the rostral tip of the hyoid bar. (5) The largerhyohyoidei adductores are spread over and between the branchiostegal rays, up tothe medial face of the opercular bone. (6) The sternohyoideus forms the muscularconnection between the pectoral girdle and the hyoid bars, as will be discussed later.In siluroids, certain specializations of the hyoid musculature can be related to thepresence of mandibular barbels (Greenwood, 1971).

In this paper, three ontogenetic stages of the above mentioned hyoid muscles inClarias gariepinus (Burchell, 1822) (Clariidae) are described. Some considerations aregiven concerning the functional-morphological structure of the muscles, as well assome typical catfish adaptations of the protractor hyoidei. Discussion on the functionof the different muscles is based on anatomical evidence only. No cinematographicalor electromyographical analyses have been done. In this paper, interpretations ofpossible functions of a certain muscle are based on morphological configurations,indicating that the muscle can be functional as it bears both its insertions.

MATERIAL AND METHODS

Specimens of Clarias gariepinus of three ontogenetic stages (7.2 mm SL, 46.8 mmSL and 136.2 mm SL) were used to describe the myology of the skull. Fertilizedeggs were obtained from the Laboratory of Ecology and Aquaculture (CatholicUniversity of Leuven, Belgium) and were raised at a temperature of 25°C. Atdifferent moments (7 days and 120 days after hatching) specimens were sedated inMS 222. A 7.2 mm SL specimen (TL=7.8 mm, PAL=3.8 mm, 7 days posthatching)(SL=standard length, TL=total length, PAL=preanal length) was fixed in aparaformaldehyde-glutaraldehyde solution. The 46.8 mm SL specimen (TL=50.2 mm, PAL=23.9 mm, 120 days posthatching) was fixed in a buffered 4%formaldehyde solution. Both were used for serial sectioning, embedded in Epon andParaplast, resp. Epon sections of 2 lm thick were stained with toluidine, Paraplast


sections of 5 lm thick were stained with an improved trichrome staining (Mangakiset al., 1964).

Other juvenile specimens were used for dissections and clearing and staining intoto, according to Hanken & Wassersug (1981). These were commercially raisedspecimens with an age of approximately 100 days, obtained from Mr Fleure(Someren, the Netherlands). One specimen was used for drawing (TL=154.1 mm,SL=136.2 mm, PAL=71.3 mm), other specimens were used for further observations(TL=149.9 mm, SL=132.5 mm, PAL=68.2 mm) (TL=166.9 mm, SL=144.5 mm, PAL=78.3 mm) (TL=163.5 mm, SL=142.8 mm, PAL=75.7 mm)(TL=144.9 mm, SL=125.5 mm, PAL=67.1 mm).

Serial sections were studied and drawn using a Leitz Diaplan light microscope,equipped with a camera lucida. Three-dimensional reconstructions were made usinga commercial software package. A WILD M5 stereo-microscope with camera lucidawas used for studying the dissections, as well as the cleared and stained specimens.

ABBREVIATIONS

bb-I basibranchiale Ic-eth cartilago ethmoideumc-Meck cartilago Meckelicb-I ceratobranchiale Icb-V ceratobranchiale Vch ceratohyalecor coracoideumfr-l foramen fila olfactoriahembr hemibranchiahh hypohyaleih interhyalel-an-ch ligamentum angulo-ceratohyalel-an-iop ligamentum angulo-interopercularel-uh-hh ligamentum urohyalo-hypohyalelm-on lamina orbitonasalis, sensu latu

m-ad-ap musculus adductor arcus palatinim-ad-mnd musculus adductor mandibulaem-ad-op musculus adductor operculim-dil-op musculus dilatator operculim-hh-ab musculus hyohyoideus abductorm-hh-ab-ad undifferentiated musculi hyohyoidei abductores and adductoresm-hh-ad musculi hyohyoidei adductoresm-hh-inf musculus hyohyoideus inferiorm-intm musculus intermandibularism-l-ap musculus levator arcus palatinim-l-op musculus levator operculim-obl-inf musculus obliquus inferiorism-phcl-ex musculus pharyngoclavicularis externusm-pr-h musculus protractor hyoideim-pr-h-d musculus protractor hyoidei pars dorsalis


m-pr-h-l musculus protractor hyoidei pars lateralism-pr-h-v musculus protractor hyoidei pars ventralism-pr-h-v-l fused musculus protractor hyoidei pars ventralis and pars lateralism-sh musculus sternohyoideusmnd mandibulamnd-b mandibular barbelmnd-b-b mandibular barbel basemnd-b-ex external mandibular barbelmnd-b-in internal mandibular barbelmx-b maxillary barbelo-ch-a os ceratohyale anterioro-ch-p os ceratohyale posterioro-cl os cleithrumo-den os dentaleo-den-c os dento-splenio-mentomeckelium complexo-den-mm os dento-mentomeckeliumo-hh-v os hypohyale ventraleo-iop os interoperculareo-mmeck os mentomeckeliumo-mx os maxillareo-op os operculareo-prmx os praemaxillareo-uh os urohyaleo-uh-l os urohyale, lateral processo-uh-m os urohyale, medial processot-cap otic capsulepal palatinumpns-ep pons epiphysialisprc-co processus coronoideus of Meckel’s cartilager-br radius branchiostegust-hh-ab tendon of the m. hyohyoideus abductort-pr-h-d tendon of the m. protractor hyoidei pars dorsalistn-m-p taenia marginalis posteriorvm-tpl vomeral tooth plate

RESULTS

The nomenclature used for the muscles described follows Winterbottom (1974).

7.2 mm SL (7 days posthatching)

In this larva, most of the muscles in question can be distinguished: (1) theintermandibularis, (2) the protractor hyoidei, (3) the hyohyoideus inferior, (4) the


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Figure 1. Graphical 3D reconstruction of the skull of larval Clarias gariepinus (7.2 mm SL): A, obliquefronto-lateral view; B, oblique ventro-lateral view (not all skeletal and muscular elements are drawn)(black indicates bone).

complex of the undifferentiated hyohyoideus ab- and adductor muscles and (5) thesternohyoideus (Fig. 1).

The intermandibularis lies at the ventro-posterior margin of the rostral tip of the


lower jaw, close to its symphysis (Figs 2A,B, 3). The mandibula in this larvalstage is formed by Meckel’s cartilage, which already bears a rostral perichondralossification, the mentomeckelian bone, and the dermal dentary. Anteriorly, themuscle fibres are attached to the ventro-medial face of the mentomeckelian, whilethe posterior fibres originate at the ventro-medial margin of the dentary (Fig. 4A).The caudalmost fibres seem to be still continuous with the rostral fibres of theprotractor hyoidei.

The protractor hyoidei is the largest of the hyoid muscles (Fig. 1B). It covers theventral face of the anterior part of the ceratohyals, thereby surrounding the basesof the mandibular barbels (Figs 1B, 2). Both the external and the internal mandibularbarbel bases seem to penetrate the muscle completely, as on the dorsal face of theprotractor muscle, two pairs of mandibular barbel extensions can be observed (Fig.3A,B). The muscle originates on the ventro-lateral face of the anterior ossificationof the hyoid bar, the anterior ceratohyal. The site of origin is located caudallyagainst the attachment site of the hyohyoideus inferior (Figs 1B, 2A,B). From thereon, the protractor muscle fibres run lateral against the hyohyoideus inferior, up tothe bases of the mandibular barbels and the dentary, where they insert. Some ofthe ventral fibres do not reach the dentary but meet the ipsi-lateral fibres at amedian aponeurosis (Figs 1, 2A,B). The attachment of the fibres to the dental issituated at the ventro-medial margin, posterior against the caudal fibres of theintermandibularis.

The hyohyoideus inferior is a small muscle bundle which runs along the ventralsurface of the ceratohyal (Figs 1B, 2A,B, 3A). Caudally the fibres originate on theventro-lateral side of the ceratohyal, medial to the protractor hyoidei. This attachmentsite is situated caudally to the articulation between the second branchiostegal rayand the hyoid bar. From there, the fibres run anteriorly to a median aponeurosis,which is not attached to any skeletal element (Fig. 2A,B).

In the muscle complex, constituting the hyohyoidei ab- and adductor, no distinctioncan be made yet between the abductor part and the adductor part. The rostral,conical part of the muscle lies at the medial face of the hyohyoideus inferior. It isattached through a very indistinct tendon to the hyoid bar. Caudally, the musclebecomes sheet-like, lying in the margin of the branchiostegal membrane. Althoughpresent, the muscle cannot be functional at this stage, as no insertion is observedto branchiostegal rays.

The sternohyoideus is already well developed. The slender muscle connects the pectoralgirdle with the rostral tip of the hyoid bars (Figs 1B, 2A, 3A,B). Caudally, all thefibres originate on a horizontal crest of the cleithrum, lateral to the attachment of thepharyngoclavicularis externus (Fig. 4C). No fibres seem to originate from a myoseptum,separating the sternohyoideus from the obliquus inferioris. Caudally, the left and rightmuscle bundles are separated from each other, as the conus arteriosus lies in betweenthem. The muscle runs between the ventrally situated ab- and adductor complex ofthe hyohyoideus muscle, and the dorsally lying branchial arches (Fig. 1). Anteriorlythe ipsi-lateral bundles converge, until they meet, thereby enclosing the ventral aorta.Rostrally, the insertion of both muscles is separated and situated at the posterior surfaceof the cartilaginous hyoid bar. The urohyal is not formed yet.


The intermandibularis is now completely separated from the protractor hyoidei, asan interconnection between the left and right internal mandibular barbel bases lies


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Figure 2. Graphical 3D reconstruction of the hyoid and intermandibularis musculature of larvalClarias gariepinus (7.2 mm SL) (ventro-frontal view): A, all muscles drawn; B, protractor hyoidei,hyohyoideus abductor and adductor muscles removed; C, intermandibularis and hyohyoideus inferiorremoved (black indicates bone, anterior ceratohyal bone not shown).


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Figure 3. Graphical 3D reconstruction of the hyoid and intermandibularis musculature of larvalClarias gariepinus (7.2 mm SL) (caudal view): A, all muscles drawn; B, hyohyoideus inferior andsternohyoideus removed; C, protractor hyoidei, hyohyoideus abductor and adductor muscles removed(black indicates bone, anterior ceratohyal bone not shown).


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in-between the two muscles (Fig. 5A). The fibres originate on the ventral side of themandibula, at the mentomeckelian and dentary (at this stage the latter bone hasalready fused with the splenial bone). The muscle connects left and right lower jaw,close to the symphysis.

The protractor hyoidei is well developed in this stage. Caudally the fibres originateon the ventro-lateral surface of the anterior ceratohyal, lateral to the attachment ofthe hyohyoideus inferior. As the fibres run rostrally and pass the bases of themandibular barbels, the fibres become subdivided into three distinct, ipsi-lateralpairs of muscle bundles (Fig. 5B). The ventral bundle pair (=protractor hyoideipars ventralis) inserts on the medial face of the bases of the internal mandibularbarbels, whereas the lateral pair (=protractor hyoidei pars lateralis) inserts on themedial face of the bases of the external mandibular barbels. The dorsal bundle pair(=protractor hyoidei pars dorsalis) is elongated rostrally into a tendon, whichattaches to the ventral face of the dentary. This tendon originates from the latero-dorsal fibres of the muscle bundles. Caudally, where no subdivisions can bedistinguished, the tendon lies on the dorsal surface of the protractor hyoidei, untilit continues into muscle fibres. As already mentioned, the protractor hyoidei hasbecome completely separated anteriorly from the intermandibularis (Fig. 5A).

The hyohyoideus inferior takes origin along the ventral surface of the anteriorceratohyal and ventral hypohyal bones. In serial sections, the fibres of the muscleseem to be directed in different trajectories (Fig. 5C). The ventral fibres runtransversally between the left and right hyoid bars, meeting in a median aponeurosis.The dorsal fibres, however, are directed more longitudinally. In between the twomuscle parts, two tendons can be distinguished which are elongated into the adjacenthyohyoidei abductores (see below).

The hyohyoideus abductor has become a distinct muscle, connecting the first branchio-stegal ray to the rostral tip of the hyoid bar. The muscle originates through a longand narrow tendon on the ventral surface of the ventral hypohyal bone. This tendonis elongated into a flat muscle sheet which inserts on the first branchiostegal ray ofthe opposite side. Consequently a crossing over of the ipsi-lateral tendons is notedat the level of the urohyal bone. Anterior to the crossing over, the tendons arecovered both dorsally and ventrally by fibres of the hyohyoideus inferior. Theinsertion site of the muscle on the rostral margin of the first branchiostegal ray isspread over the complete length of the ray, whereas the lateral margin of the muscleextends into the lateral margin of the branchiostegal membrane. The lateral fibresdo not insert on the branchiostegal ray, but are attached to a myoseptum separatingthe muscle from the first hyohyoideus adductor.

The hyohyoidei adductores form a continuous muscle sheet between the first branchio-stegal ray up to the medial face of the opercular bone, thereby enclosing all therays lying in between. The muscles inserting on the branchiostegal rays attach tothe latter along the whole length. The lateral fibres lie lateral to the rays, as theyinsert on the myocommata separating the different muscles.

At this ontogenetic stage the sternohyoideus is enlarged caudally to a great extent,as can be seen in the 136.2 mm SL specimen as well (Fig. 8C). The muscle isattached to both the ventral and the dorsal surface of the cleithrum. Caudally, thefibres lying dorsal to the horizontal limb of the cleithrum, are separated completelyfrom the fibres attached to the ventral surface of the bone. More anteriorly, thelateral fibres of these muscle divisions are fused, thereby covering the latero-rostralmargin of the cleithral bone. The left and right muscle bundles are separated from


each other by a vertical myoseptum. The hemibranchia in the branchial cavitycover the dorsal surface of these muscle bundles. Anteriorly, the fibres enclose thethree caudal processes of the urohyal bone, on which they insert. The medial processof the urohyal bone lies in the same plane as the myoseptum separating the ipsi-lateral muscle bundles. At the level of these three processes, the fibres are concentratedinto four distinct bundles: two of them are attached to the ventral surface of themedial process, the other two are attached to the dorsal surface (Fig. 5D). Both theventral and the dorsal bundles insert laterally on the medial face of the lateralprocesses of the urohyal bone. A broad sheet of connective tissue can be distinguished,connecting the lateral processes and the ventral bundles to the underlying hyohyoideusinferior.


The intermandibularis in this specimen is comparable to the situation in the 46.8 mmSL specimen. In a ventral view, the separation of the muscle from the anterior fibresof the protractor hyoidei can be observed (Fig. 6A). The muscle connects the leftand right mandibles. The insertion is spread over the ventral face of the men-tomeckelian part and the anterior part of the dento-splenial component, close tothe mandibular symphysis (Fig. 6B).

The protractor hyoidei is a solid and large muscle, connecting the hyoid bars to boththe lower jaw and the mandibular barbels (Fig. 6). The origin of the muscle isspread over the anterior ceratohyal, up to the anterior margin of the non-ossifiedarea between the anterior and the posterior ceratohyal bone (Fig. 8). The origin ofthe protractor hyoidei lies lateral to the origin of the hyohyoideus inferior, whichinserts on the anterior ceratohyal as well. From there on, the superficial fibres runanteriorly up to different insertion sites, resulting in four distinct superficial musclefields (Fig. 7). The lateral fibres insert on the posterior and lateral margin of thebases of the external mandibular barbels (field P1) (nomenclature of the fieldsfollowing Ghiot et al. (1984)). The medial fibres run up to a median aponeurosis,thereby interconnecting the left and right protractor muscles (field P7). Superficialfibres originate from the bases of the mandibular barbels as well. Muscle fibres wereobserved running from the medial face of the base of the external mandibularbarbel, up to the lateral face of the base of the internal mandibular barbel (field P3).Other fibres connect the medial face of the base of the internal mandibular barbelto the structure interconnecting the ipsi-lateral internal mandibular barbels (fieldP4). These superficial fibres correspond to the pars ventralis and lateralis, as wasobserved in the 46.8 mm SL specimen (Fig. 5B). The tendon of the pars dorsalis,as was observed in the 46.8 mm SL C. gariepinus, originates from its ventral fibresand inserts on the ventral face of the dentary. The dorsal fibres insert on the caudalmargin of the lower jaw and run medially where they meet the ipsi-lateral fibres ata median aponeurosis (Fig. 6B).

The hyohyoideus inferior is a solid muscle covering the ventral face of the anteriorceratohyal and the ventral hypohyal (Figs 6, 8A). The origin of the muscle is spreadover the whole ventral surface of those two bones. Anteriorly, the anteriorly directedfibres curve medially as they insert on a median aponeurosis.

The morphology of the hyohyoideus abductor is comparable to the situation in the46.8 mm SL specimen. The crossing over of the tendons of the muscles can clearly


5 mm

mnd-b-in

m-hh-abmnd

m-pr-h-d

m-intm

o-mx

m-hh-inf m-hh-ab m-ad-mnd r-br-VII

B

5 mm

m-hh-adm-pr-h-v-l mnd

mx-b

o-prmx

A

mnd-b-ex

t-pr-h-d

m-intm

m-hh-inf l-an-iop l-an-ch

m-ad-mnd

Figure 6. Ventral view of juvenile Clarias gariepinus (136.2 mm SL): A, skin removed; B, pars ventralisand pars lateralis of the protractor hyoidei removed.

be distinguished as they run from the ventral face of the urohyal bone up to theventral hypohyals (Fig. 9).

The hyohyoidei adductores form a strong muscular sheet between the first branch-iostegal ray and the opercular bone, into which the other branchiostegal rays areembedded. The developmental state is comparable to the 46.8 mm specimen. Themarginal muscle fibres correspond with the margin of the branchiostegal membrane,which covers the pectoral girdle.

The sternohyoideus has become a very solid muscle, triangular in shape. The origin


5 mm

P4

P7

P3

P1

Figure 7. Ventral view of the protractor hyoidei in juvenile Clarias gariepinus (136.2 mm SL), showingthe different fields of the superficial fibres (for abbreviations, see text).

of the muscle is spread along the whole rostral margin of the ventral limb of thecleithral bone (Fig. 8C). The cleithrum bears a thin, rostral crest for the attachmentof the sternohyoideus fibres, both at its ventral and its dorsal face. The fibres of thesternohyoideus are completely separated from the hypaxial muscles. Caudally, leftand right sternohyoideus meet one another entirely in the midline. Rostrally themuscle fits into the fork formed by the caudal processes of the urohyal bone. It isstated that the latter bone is derived from a paired ossification of the tendons of theleft and right tendon of the sternohyoideus (parurohyale in Arratia & Schultze,1990). The urohyal is connected to the ventral hypohyals through two stout ligaments(ligamenta urohyalo-hypohyalia). The sternohyoideus consists of three myomeres,divided by two myocommata (Fig. 8C). The medial fibres of the middle myomereoriginate on the cleithral bone, whereas the major part of the fibres are attached tothe caudal myocomma.

DISCUSSION

Not all the described hyoid muscles develop simultaneously in C. gariepinus (seeTable 1). The intermandibularis, the protractor hyoidei and the hyohyoideus inferiorare present already in 4.7 mm fry, although no insertion was observed (Surlemont


5 mm

o-prmx

hembrmnd

mnd

m-hh-ab o-iopB

5 mm

m-hh-ad

vm-tpl

A

m-hh-inf

m-ad-mndl-an-iop

o-hh-v

m-ad-mnd

m-hh-ab

o-ch-a o-ch-p r-br-VIII

o-op

5 mm

o-uh

o-hh-v

l-uh-hh

t-hh-ab

l-an-ch

o-ch-a m-sh o-ch-p o-cl

C

o-mx

o-uh

o-prmx

o-hh-v

vm-tpl

Figure 8. Ventral view of juvenile Clarias gariepinus (136.2 mm SL): A, protractor hyoidei, in-termandibularis and part of the hyohyoideus inferior removed; B, hyohyoideus inferior removedcompletely; C, hyohyoideus abductor and adductor muscles, together with the branchiostegal rays,removed (small circles indicate cartilage).


m-hh-ad

B

A

vm-tpl

l-uh-hh m-hh-ab

1 mm o-ch-a

5 mm

t-hh-ab

o-hh-v

o-uh r-br-l

Figure 9. Ventral view of juvenile Clarias gariepinus (136.2 mm SL): A, overview; B, detail of the tendonsof the hyohyoideus abductor (small circles indicate cartilage).

et al., 1989). In the 5.2 mm fry, the sternohyoideus is developed, lying at the ventralface of the branchial basket. The muscle reaches from the pectoral region tothe posterior margin of the hyohyoideus inferior, but does not insert yet. Theintermandibularis and protractor hyoidei, however, are already provided with boththeir insertions at this level (Surlemont & Vandewalle, 1991). It is only in the 6.8 mmlarva that the hyohyoideus inferior and the sternohyoideus attach to the hyoid bars(Surlemont et al., 1989). In the 7.2 mm larva, the hyohyoideus abductor and adductormuscles can be observed, inserting through an indistinct tendon onto the rostralpart of the hyoid bar. These muscles, however, which cannot be distinguished fromeach other at this stage, do not yet insert on the branchiostegal rays. The insertionwas observed in the 46.8 mm SL juveniles.

Looking at the ontogeny of the skeletal elements of the suspensorium, four majorstages can be distinguished. Initially, the suspensorium, Meckel’s cartilage and thehyoid bars form one single cartilaginous unit, as can be observed in the 4.7 mmand 5.2 mm larvae (Surlemont et al., 1989; Surlemont & Vandewalle, 1991). Secondly,the cartilaginous connection between the lower jaw and the quadrate part of thesuspensorium is lost, and a real articulation is formed in the 6.8 mm larva (Surlemont& Vandewalle, 1991). Thirdly, the cartilaginous connection between the hyoid barsand the suspensorium, constituted by the cartilaginous interhyal is lost, as theinterhyal becomes a separate structure articulating with both the suspensorium andthe hyoid bars (in the 46.8 mm SL specimen). Fourthly, the interhyal becomescompletely reduced and a ligamentous connection is present between the hyoid barsand the suspensorium (in the 136.2 mm SL specimen) (Adriaens & Verraes, 1994).


T 1. Data on the presence of the cranial muscles during ontogeny in C. gariepinus (−=not yetpresent, ±=present but no insertion, +=present and inserting) (∗ the insertion of the muscles is noton the opercular bone but on the opercular process of the hyosymplectic) (∗ following Surlemont et

al., 1989; † following Surlemont & Vandewalle, 1991)

Muscle 4.2 mm† 4.7 mm† 5.2 mm∗ 6.8 mm† 7.2 mm 46.8 mm 144.90 mm

intermandibularis − ± + + + + +protractor hyoidei − ± + + + + +hyohyoideus inferior − ± ± + + + +hyohyoideus abductor − − − − + + +hyohyoidei adductores − − − − ± + +sternohyoideus − − ± + + + +adductor mandibulae − ± + + + + +levator arcus palatini − ± + + + + +adductor arcus palatini − ± + + + + +extensor tentaculi − − − + + + +retractor tentaculi − − − + + + +levator operculi − − ± + + + +adductor operculi − − ±∗ ±∗ ±∗ + +dilatator operculi − − ±∗ ± + + +

As already mentioned, the intermandibularis in the juvenile C. gariepinus correspondsto the anterior portion of the primordium of this muscle, as the posterior part hasfused with the interhyoideus anterior. This seems to be the case in most teleosts.However, in two groups of Osteoglossomorpha (Notopteridae: Osteoglossiformesand Mormyridae: Mormyriformes), the two muscles (posterior intermandibularisand anterior interhyoideus) remain separated (Greenwood, 1971). In the latter paperthe interhyoideus seems to correspond to the interhyoideus anterior. A reduction ofthe anterior intermandibularis is noted in those species where a fusion has occurredbetween the two mandibular rami, as the muscle normally contributes to theadduction of the two rami, and consequently the adduction of the suspensoria(Anker, 1974). Within the ostariophysan fishes, the muscle is well developed inCobitidae (but not in the other Cypriniformes) and in Siluroidei.

The morphology of the protractor hyoidei has frequently become a complex structure,in which the basic configuration of the subdivisions can only be discerned fromontogenetic studies. Generally the protractor hyoidei is recognized only when afusion between the posterior intermandibular and anterior interhyoideus muscle hasoccurred. Generally, this protractor then connects the medial face of the mandibula,close to the symphysis, with the hyoid bars at the level of the hypohyals, and theanterior and posterior ceratohyals (Winterbottom, 1974). Expansion of insertionshave been observed in several teleosts, where the protractor becomes attached tothe branchiostegal rays (e.g. in Osteoglossidae, Pantodontidae (Greenwood, 1971),Cyprinidae (Takahasi, 1925)) (Winterbottom, 1974). The rostral attachment of themuscle to the dentary seems to be constant, although additional insertions on theangular occur (Liem, 1967). In several cases, the protractor hyoidei has a typical‘X’-shape, bearing two separate bundles anteriorly and posteriorly, fused to eachother in the middle (Takahasi, 1925; Saxena & Chandy, 1966; Lauder, 1980a, 1981;Lauder & Liem, 1980), although other shapes are frequent (e.g. Y-shape in Epibulusinsidator (Perciformes: Labridae)) (Westneat & Wainwright, 1989). The secondarysubdivision of the protractor muscle in a superficial part and a deeper part, as isobserved in C. gariepinus, seems to be a general feature for siluroid fishes. Takahasi


(1925) referred to a ‘geniohyoideus inferior’, corresponding to the protractor hyoideipars ventralis and lateralis, and a ‘geniohyoideus superior’, corresponding to theprotractor hyoidei pars dorsalis. In Mormyridae, where the posterior inter-mandibularis and the anterior interhyoideus remain separated from each other, thelatter muscle consists of two pairs of muscle bundles: a medial (or inner) divisionand a lateral division (Greenwood, 1971). The position of the lateral division, andespecially the fact that it inserts through a tendon onto the anterior half of themandibula, may suggest a correspondence with the tendinously inserting protractorhyoidei pars dorsalis. The deeper fibres of this pars dorsalis, covering the tendinouspart, may then correspond to the inner division (Fig. 6B). When comparing theposition of the posterior intermandibularis in Mormyridae with C. gariepinus, thismuscle may then correspond to the protractor hyoidei pars lateralis and ventralisof C. gariepinus, into which the mandibular barbels have become embedded. However,some additional ontogenetic evidence, as well as comparative material would berequired to elucidate such homologies. Several authors refer to a ‘geniohyoideusanterior’ and a ‘geniohyoideus posterior’ (Osse, 1969; Anker, 1974; Lauder & Liem,1980; Westneat, 1990). It has been demonstrated that these two muscles contractedindependently from each other (Osse, 1969; Lauder & Liem, 1980). This anteriorpart presumably corresponds to the intermandibularis posterior, whereas the posteriorpart corresponds to the interhyoideus anterior. As these two muscles are innervatedby two different nerves, an independent contraction of those two muscles could beexplained (Verraes, 1973). In those ostariophysan fishes where no subdivisions canbe found, it is presumed to be the result of a secondary fusion between the superficialand the deeper part. Exceptionally, the protractor hyoidei can be reduced completely,as is observed in Liobagrus (Amblycipitidae) (Takahasi, 1925). The activity of theprotractor hyoidei muscle can even differ interspecifically, as was observed in severalcharacids (Lauder, 1981).

The hyohyoideus is derived from the interhyoideus posterior (Winterbottom, 1974).An undifferentiated hyohyoideus muscle can still be found in some living teleosts,where the muscle runs from the medial face of the opercular bones, passingalong the branchiostegal rays up to the medial face of the hyoid bar (e.g. inOsteoglossomorpha, Salmonidae, Cobitidae) (Takahasi, 1925; Greenwood, 1971;Verraes, 1973; Lauder & Liem, 1980). Although only one muscle can be observedin Cobitidae, two rostral insertion sites can be distinguished, corresponding to theinsertion sites of two subdivisions of the hyohyoideus observed in most Cypriniformesand all Siluroidei (Takahasi, 1925). The latter author then refers to an ‘inferiorhyohyoideus muscle’, inserting on the hyoid bar, and a ‘superior hyohyoideusmuscle’, attaching onto the branchiostegal rays. The inferior part corresponds tothe hyohyoideus inferior used in this paper, whereas the superior part correspondsto both the hyohyoideus abductor and adductor muscles (Takahasi, 1925; Munshi& Singh, 1967; Singh, 1967; Osse, 1969; Anker, 1974).

This hyohyoideus inferior generally covers the anterior ventral portion of the hyoidbars, onto which it inserts. The muscle fibres then run medially, as they insert ona median aponeurosis, thereby covering the urohyal bone. In some cases, the muscleinserts on the latter bone as well, in which case no median aponeurosis is present(Winterbottom, 1974).

The hyohyoideus abductor is responsible for the expansion of the branchiostegalmembrane. In general the muscle connects the first branchiostegal rays with therostral tip of the hyoid bars. However, some morphological modifications concerning


the insertions of the tendons have been noted, as the tendon of the abductor,attached to the branchiostegal ray on one side of the hyoid bar, runs up to thehyoid bar of the same side, of the opposite side or of both sides. In C. gariepinus itis observed that the tendons cross over each other, as they pass through thehyohyoideus inferior (Fig. 9). In Gasterosteus aculeatus, a single tendon, which is forkedanteriorly, connects the muscle with ipsi-lateral rostral tips of the hyoid bar (Anker,1974). In those cases where the abductor muscle is not present, a caudal shift of thefibres of the hyohyoideus inferior or the protractor hyoidei can be observed, whichthen insert on the first branchiostegal rays (Winterbottom, 1974). As a result, thecontraction will generate an abduction of the branchiostegal rays as well.

In general the hyohyoidei adductores form the sometimes continuous muscle sheetbetween the first branchiostegal ray and the opercular, although insertions are foundon the subopercular or the interopercular bones as well (Munshi & Singh, 1967; Osse,1969; Winterbottom, 1974). Contraction of the muscles results in the constriction ofthe branchiostegal membrane. In C. gariepinus the caudal insertion is restricted tothe opercular bone. Nawar (1955) made a further nomenclatural subdivision as hereferred to the ‘interbranchiostegales’, indicating the muscles interconnecting thebranchiostegal rays, and the ‘opercular branchiostegalis’, being the muscle runningfrom the last branchiostegal ray up to the medial face of the opercular bone.

The sternohyoideus configuration in teleosts is rather constant (Greenwood, 1971;Winterbottom, 1974). In most cases this muscle runs from the horizontal limb ofthe cleithrum up to the urohyal bone, which is believed to be a sesamoid ossificationof the sternohyoideus tendon (de Beer, 1937; Devillers, 1958; Arratia & Schultze,1990). As in most teleosts, some fibres are connected to an aponeurosis with theinferior obliquus hypaxial muscle, it is not the case in C. gariepinus. The insertion ofthe sternohyoideus in the latter species is, however, spread over the plate-likehorizontal limb, both along its dorsal and ventral margin. In most teleosts, thesternohyoideus plays a crucial role in mouth opening, suspensorial abductions andhyoid depressions (Lauder, 1980c; Lauder & Liem, 1980; Aerts, 1991). In C. gariepinusthe sternohyoideus is a solid but short muscle, which may influence the depressioncapacities during hyoid depression (Adriaens & Verraes, 1994).

The principal function of the hyoid bar is to act as a lever for the expansion ofthe orobranchial cavity (Schaeffer & Rosen, 1961). Such expansions, however, aregenerated through a whole set of mechanisms in which the neurocranium, the lowerjaw, the maxillary bones, the suspensorium, the branchiostegal rays, the opercularbones and the gill arches are involved (Alexander, 1967, 1969; Gosline, 1971; Anker,1974; Lauder & Liem, 1980; Lauder, 1980a,c, 1981; Liem, 1984; Muller, 1987;Westneat, 1990; Aerts, 1991). The effect of suspensorial abduction will be of greaterimportance in those fishes with a laterally depressed skull, where the suspensoriaare high, compared to dorso-ventrally flattened skulls, with short suspensoria. Inthose teleosts having a dorso-ventrally depressed head, like most catfishes do, theelevation of the skull and the depression of the hyoid bar will play a more importantrole (Alexander, 1965; Gosline, 1973). In siluroids, however, the neurocranialmovements are believed to be obstructed by the strongly fused anterior vertebraein the complex weberian apparatus, but mainly in the lateral way (Gosline, 1977).In fishes, with dorso-ventrally flattened skulls, it can be suggested that an extensivehyoid depression can be infavourable (Adriaens & Verraes, 1994). In general, thehead of catfishes is dorso-ventrally flattened, being an adaptation to a benthic lifestyle(Alexander, 1965). Consequently, the floor of the orobranchial cavity is relatively


broad, which implicates that only a slight depression of the hyoid bars will result ina substantial volume increase (Adriaens & Verraes, in press). Furthermore, Hughes(1970) argued that in bottom-living fishes, the suction pump system, enabled throughan abduction of the opercular bone, is far more important for aquatic respirationthan the pressure pump system, in which a depression of hyoid bar and adductionof suspensoria induces the water flow. In C. gariepinus, an adaptation to an improvedopercular abduction has been observed, as a shift of the insertion site of the adductoroperculi resulted in an abduction action of the latter muscle, and thus being aprotagonist of the well developed dilatator operculi (Adriaens & Verraes, 1997).

One typical catfish specialization, in hyoid musculature, is related to the presenceof the mandibular barbels. In several catfishes, the function of the protractor hyoideiis not restricted to jaw opening or hyoid elevation. As the bases of the mandibularbarbels are embedded into the superficial fibres of the protractor muscle, contractionsof the muscle will control the orientation of these barbels. In some catfishes a totalof up to seven of these different fields could be recognized: (1) P1 connecting thehyoid bar with the basal process of the external mandibular barbel, (2) P2 betweenthe plate, interconnecting the bases of the internal and external barbel, and theexternal mandibular barbel base, (3) P3 between the bases of the internal and theexternal barbels, (4) P4 between the internal barbel base and the median aponeurosis,(5) P5 between the caudal tip of the external mandibular barbel base and the medianaponeurosis, (6) P6 between the base of the internal mandibular barbel and thehyoid bar and (7) P7 running from the hyoid bar up to the median aponeurosis(Ghiot, 1978; Ghiot et al., 1984). In C. gariepinus, four of these fields were observed(Fig. 7). The largest field, the P7, connects the ipsi-lateral hyoid bars to each other.As the fibres of this field do not insert on the bases of mandibular barbels, they willprobably have little effect on the displacement of the barbels. A medial displacementcan be generated for the internal and external barbels independently: contractionof the P1 field will retract the base of the external mandibular barbel, which canresult in the medial displacement of the distal part of the barbel, whereas a combinedcontraction of the P1 and the P3 field can have the same effect on the internalbarbel. The opposite displacement, in a lateral direction, can be generated as follows:contraction of the P4 for the internal barbels, P3 for the external barbels and bothfor the displacement of the internal and external barbels. Singh (1967) used termslike ‘retractor tentaculi’ and ‘protractor tentaculi’ to indicate the differentiatedprotractor hyoidei attached to the bases of the mandibular barbels.

Another specialization, within the Ostariophysi, as an adaptation to a benthiclifestyle has been observed in some hill stream cyprinids, like Garra mullya andCrossocheilus latius punjabensis (Cypriniformes: Cyprinidae) (Saxena & Chandy, 1966).These species have developed a mental suctorial disc, which enables them to attachthemselves to the substrate in order to withstand strong currents. A vacuum is createdand sustained into these discs through contraction of a modified intermandibularis andprotractor hyoidei.

In the Clariidae, the hyoid bars play an additional important role in the respiratorymechanism, as the members of this catfish family are able to perform aerialrespiration, due to the presence of a suprabranchial organ (Willem, 1951; Munshi,1961). During this kind of respiration, an air bubble is swallowed at the watersurface, and transported from the oral cavity, along the branchial cavity into thesuprabranchial cavity (Hellin & Chardon, 1981; Vandewalle & Chardon, 1991).The air bubble is pushed from the oral cavity into the branchial cavity through the


lifting of the hyoid bar, generated through the contraction of the protractor hyoidei.It was observed in an abnormal specimen, lacking any mobility in the hyoid bars,that the transport of the air bubble to the suprabranchial organ was impossible(Vandewalle & Chardon, 1991).

CONCLUSIONS

In C. gariepinus, the hyoid muscles investigated, develop and attach themselves toskeletal elements in a non-synchronous way. Ontogenetically, the intermandibularis,the protractor hyoidei and the hyohyoideus inferior are the first to develop, followedby the sternohyoideus. The last of the six muscles to become functional are thehyohyoideus abductor and adductor muscles. This time difference in functionality,coupled to an ontogenetic asynchrony in the skeletal development, may result forexample in a shift and sequence in mouth opening and respiratory mechanisms.

The myology of the juvenile C. gariepinus reveals some structural adaptations. Thesuperficial fibres of the protractor hyoidei are arranged into four fields, based onthe place of origin and insertion. Several of these fields may generate a displacementof the internal and external mandibular barbels. A detailed morphological studyreveals a subdivision of this muscle in pars lateralis, pars ventralis and pars dorsalis.The hyohyoid muscle is well developed and differentiated in the inferior, theabductor and the several adductor muscles. The sternohyoideus is broad but rathershort, probably due to the need of a restricted hyoid depression during respirationand feeding.

ACKNOWLEDGEMENTS

We wish to thank Prof. Dr F. Ollevier and Prof. Dr F. Volckaert of the Laboratoryof Ecology and Aquaculture (Catholic University of Leuven) and Mr Fleure (Someren,the Netherlands) for providing the specimens of C. gariepinus. Also we wish to thankD. Vandenbroeck and G. De Wever for making the serial sections of C. gariepinus.Research was funded by the Institute for Science and Technology (D.A.) and theNational Funds for Scientific Research (W.V.).

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