write an essay on jaw suspensorium

Jaw Suspension In Vertebrates – Types, Structure, Functions, Example

What do you mean by jaw suspensorium.

Jaw suspension in vertebrates refers to the way the lower jaw is attached to the upper jaw or the skull, enabling efficient biting and chewing. This attachment is achieved through modifications in the visceral arches, which are part of the splanchnocranium in the vertebrate skull.

The mandibular arch consists of a dorsal palatopterygoquadrate bar, which forms the upper jaw, and a ventral Meckel’s cartilage, which forms the lower jaw. These structures provide the foundation for the jaws in gnathostomes, or jawed vertebrates.

The remaining arches in the splanchnocranium support the gills and are called branchial arches.

Overall, the splanchnocranium, particularly the mandibular and hyoid arches, plays a vital role in the formation of jaws in gnathostomes and their attachment or suspension with the chondrocranium, which is the cartilaginous part of the skull. This attachment or suspension mechanism is referred to as jaw suspension or suspensorium.

Types of Jaw Suspension In Vertebrates

By adapting and modifying the structures within the visceral arches, different vertebrates have evolved various types of jaw suspensions that suit their specific feeding habits and lifestyles. These adaptations have contributed to the incredible diversity of jaw structures and functions seen across vertebrate species. There are different types of suspensoria as follows:

1. Amphistylic

Components of amphistylic suspension, functional mechanism, 2. autodiastylic, components of autodiastylic suspension, 3. hyostylic.

Hyostylic jaw suspension is an advanced jaw structure mechanism observed in many elasmobranchs (such as modern sharks) and bony fishes. This system is characterized by the attachment of both the upper and lower jaws to the cranium primarily through the hyoid arch, offering increased mobility and support. Here is a detailed breakdown of its components and functions:

Components of Hyostylic Suspension

4. methystylic, components of methystylic suspension.

Comparison with Hyostylic Suspension

5. Autostylic

Components of autostylic suspension, 6. monimostylic.

Monimostylic jaw suspension represents an advanced modification of the autostylic suspension system, distinguished by its unique structural adaptations. This system involves specific changes to the jaw components, leading to a more rigid and fixed jaw mechanism. Below is a detailed explanation of its components and functions:

Components of Monimostylic Suspension

Comparison with other jaw suspensions, 7. holostylic, components of holostylic suspension, 8. craniostylic.

Craniostylic jaw suspension represents a highly specialized and advanced form of jaw articulation found primarily in mammals, including monotremes. This system exemplifies a significant evolutionary adaptation in jaw mechanics and skull structure.

Key Features of Craniostylic Suspension

Functional implications, 9. streptostylic.

Streptostylic jaw suspension is a distinct evolutionary adaptation observed in certain reptiles, including snakes and lizards, as well as in birds. This jaw suspension type is characterized by specific modifications that enhance jaw flexibility and function.

Key Features of Streptostylic Suspension

10. monimostylic, key features of monimostylic suspension, comparative account, which structure is responsible for the suspension of the jaw in vertebrates, what is jaw suspension, how many types of jaw suspension are found in vertebrates.

There are several types of jaw suspension found in vertebrates, including paleostylic, autodiastylic, amphistylic, hyostylic, holostylic, monimostylic, streptostylic, and craniostylic.

What is the difference between autodiastylic and amphistylic jaw suspension?

Which group of vertebrates exhibits hyostylic jaw suspension, what is the characteristic feature of holostylic jaw suspension.

Holostylic jaw suspension is found in lung fishes and Holocephali. In this type, the upper jaw is fused with the skull, and the lower jaw is directly attached to it. The hyoid arch remains independent and not attached to the skull.

What is monimostylic jaw suspension?

Which group of vertebrates exhibits streptostylic jaw suspension, what is craniostylic jaw suspension.

Craniostylic jaw suspension is found in mammals. In this type, the upper jaw fuses with the cranium, and the lower jaw is directly attached to the squamosal bone. The hyomandibular bone becomes the middle ear ossicle called the incus.

How does jaw suspension vary among different vertebrate groups?

How does jaw suspension relate to feeding behaviors in vertebrates, related posts, vertebra – definition, structure, development, vertebrata – definition, classification, characteristics, features, integument in vertebrates – structure, functions and derivatives., what is visceral arches, respiratory system of vertebrata – skin, gills, lungs and air sacs, circulatory system in vertebrates – components, structure, functions, nervous system of frog, respiratory system of frog, leave a comment cancel reply.

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• JAW SUSPENSION IN VERTEBRATES

Jaw suspension means attachment of the lower jaw with the upper jaw or the skull for efficient biting and chewing. There are different ways in which these attachments are attained depending upon the modifications in visceral arches in vertebrates.

  AMPHISTYLIC

In primitive elasmobranchs there is no modification of visceral arches and they are made of cartilage. Pterygoqadrate makes the upper jaw and meckel’s cartilage makes lower jaw and they are highly flexible. Hyoid arch is also unchanged. Lower jaw is attached to both pterygoqadrate and hyoid arch and hence it is called amphistylic.

 AUTODIASTYLIC

Upper jaw is attached with the skull and lower jaw is directly attached to the upper jaw. The second arch is a branchial arch and does not take part in jaw suspension.

  HYOSTYLIC

In modern sharks, lower jaw is attached to pterygoquadrate which is in turn attached to hyomandibular cartilage of the 2 nd arch. It is the hyoid arch which braces the jaw by ligament attachment and hence it is called hyostylic.

HYOSTYLIC (=METHYSTYLIC)

In bony fishes pterygoquadrate is broken into epipterygoid, metapterygoid and quadrate, which become part of the skull. Meckel’s cartilage is modified as articular bone of the lower jaw, through which the lower jaw articulates with quadrate and then with symplectic bone of the hyoid arch to the skull. This is a modified hyostylic jaw suspension that is more advanced.

AUTOSTYLIC (=AUTOSYSTYLIC)

Pterygoquadrate is modified to form epipterygoid and quadrate, the latter braces the lower jaw with the skull. Hyomandibular of the second arch transforms into columella bone of the middle ear cavity and hence not available for jaw suspension.

MONIMOSTYLIC

This type of suspension is a modification of autosystylic suspension in which quadrate is immovable and not flexible as in amphibia and many reptiles. Hyomandibular is modified as columella bone of the middle ear cavity.

STREPTOSTYLIC

This type is found in snakes, lizards and birds, in which quadrate bone is movable and flexible at both ends making the jaw highly flexible. Columella is single bone in the middle ear cavity and is sometimes called stapes.

HOLOSTYLIC type is found in lung fishes and Holocephali. Upper jaw is fused with the skull and the lower jaw is attached directly with it. Hyoid arch does not participate in jaw suspension and is a typical branchial arch. There is no columella bone.

AUTOSTYLIC (=CRANIOSTYLIC)

Found in mammals, in this type of jaw suspension, pterygoquadrate is transformed into alisphenoid and incus, while meckel’s cartilage is changed into malleus and not available for jaw suspension. Lower jaw is directly attached to the skull bone called squamosal. Monotremes also possess this type of jaw suspension.

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Morphology of the jaw, suspensorial, and opercle musculature of Beloniformes and related species (Teleostei: Acanthopterygii), with a special reference to the m. adductor mandibulae complex

Ingmar werneburg.

Museum für Naturkunde, Leibniz-Institut für Evolutions- & Biodiversitätsforschung an der Humboldt-Universität zu Berlin, Berlin, Germany

The taxon Beloniformes represents a heterogeneous group of teleost fishes that show an extraordinary diversity of jaw morphology. I present new anatomical descriptions of the jaw musculature in six selected beloniforms and four closely related species. A reduction of the external jaw adductor (A1) and a changed morphology of the intramandibular musculature were found in many Beloniformes. This might be correlated with the progressively reduced mobility of the upper and lower jaw bones. The needlefishes and sauries, which are characterised by extremely elongated and stiffened jaws, show several derived characters, which in combination enable the capture of fish at high velocity. The ricefishes are characterised by several derived and many plesiomorphic characters that make broad scale comparisons difficult. Soft tissue characters are highly diverse among hemiramphids and flying fishes reflecting the uncertainty about their phylogenetic position and interrelationship. The morphological findings presented herein may help to interpret future phylogenetic analyses using cranial musculature in Beloniformes.

Introduction

The m. adductor mandibulae complex belongs to one of the most intensively studied soft tissues in vertebrates. It primarily moves the skeletal elements associated to the mandibular arch and is the main head and the most powerful feeding musculature. The m. adductor mandibulae complex is highly adapted to different feeding strategies among vertebrate clades and, as such, experienced a large amount of diversification. Its anatomy is informative for different phylogenetic levels and a mutual evolution with jaw and skull anatomy can be observed (e.g., Gosline, 1986 ; Diogo, 2008 ; Diogo & Abdala, 2010 ; Datovo & Vari, 2013 ).

Among teleost fishes, the jaw anatomy of Beloniformes, the needlefishes and their allies, is very diverse. As such, they received reasonable attention in osteological, phylogenetic as well as ontogenetic analyses Rosen & Parenti, 1981 ; Boughton, Collette & McCune, 1991 ; Lovejoy & De Araujo, 2000 ; Lovejoy, Iranpour & Collette, 2004 . The taxon includes small, short-snouted and duckbilled ricefishes (Adrianichthyidae) ( Parenti, 1987 ), which live in flooded Asian rice fields. Halfbeaks (hemiramphids), another group, are characterised by an elongated lower jaw. The flying fishes (Exocoetidae) have short snouts; whereas the sauries (Scomberesocidae) and needlefishes (Belonidae), which are adapted to fast swimming and fish hunting, have elongated upper and lower jaws with extended teeth rows ( Nelson, 2006 ). Although the drastic ontogenetic changes of the jaws have been previously studied in their external shape ( Boughton, Collette & McCune, 1991 ; Lovejoy, Iranpour & Collette, 2004 ), the anatomy of the fully formed cranial musculature has received little attention.

Beloniformes belong to the Atherinomorpha ( Fig. 1 ), which are placed within the Acanthopterygii. The phylogenetic relationships among acanthopterygian groups, which also include taxa such as Perciformes and Mugilomorpha, are controversial (e.g., Stiassny, 1990 ; Johnson & Patterson, 1993 ; Parenti, 1993 ; Parenti & Grier, 2004 ; Rosen & Parenti, 1981 ; Wu & Shen, 2004 ; Nelson, 2006 ; Setiamarga et al., 2008 ; Near et al., 2013 ). Smegmamorpha, Mugilomorpha, or Paracanthopterygii have all been hypothesised to form the sister taxon to Atherinomorpha.

(A) Rosen (1964) , (B) Rosen & Parenti (1981) , (C) Lovejoy, Iranpour & Collette (2004) . Note the different arrangement of Cyprinodontea (6), Hemiramphidae, and the position of Scomberesocidae; corresponding taxa are highlighted. Numbers of non-terminal clades: 1, Atherinomorpha (1*: clade named as “Atheriniformes” by Rosen, 1964 ); 2, Cyprinodontoidei; 3, Exocoetoidei; 4, Exocoetoidea; 5, Scomberesocoidea; 6, Cyprinodontea; 7, Beloniformes, 8, N.N.

The monophyly of Atherinomorpha is currently accepted ( Nelson, 2006 ; Near et al., 2013 ). Atheriniformes form the sister group of Cyprinodontea, which comprises Cyprinodontiformes (killifishes and their allies) and Beloniformes ( Figs. 1B – 1C ). Recently, Li (2001) analysed osteological data of the hyobranchial apparatus and re-established the traditional hypotheses of Berg (1958) and Rosen (1964) of a closer relationship of Adrianichthyidae to Cyprinodontiformes ( Fig. 1A ; see also Temminck & Schlegel, 1846 : compared to Yamamoto, 1975 ). This hypothesis, however, was not based on a cladistic analysis and represents phenetic classifications. These classifications are in strong contrast to several morphological and molecular analyses, which result in a sister group relationship of Adrianichthyidae and Exocoetoidea, comprising the remaining Beloniformes ( Fig. 1 ), and Beloniformes as the sister group of Cyprinodontiformes ( Rosen & Parenti, 1981 ; Collette et al., 1984 ; White, Lavenberg & McGowen, 1984 ; Naruse et al., 1993 ; Dyer & Chernoff, 1996 ; Naruse, 1996 ; Hertwig, 2008 ).

The phylogenetic relationships within Beloniformes are still a matter of debate. Traditional studies ( Rosen, 1964 ; Rosen & Parenti, 1981 ) found two major clades within Beloniformes (excl. Adrianichthyidae), namely Exocoetoidea (flying fishes and halfbeaks) and Scomberesocoidea (sauries and needlefishes), together forming the Exocoetoidei ( Rosen, 1964 ; Parin & Astakhov, 1982 ; Collette et al., 1984 ; Figs. 1A – 1B ).

Recently, Lovejoy (2000) and Lovejoy, Iranpour & Collette (2004) proposed the paraphyly of hemiramphids and nested Scomberesocidae inside “Belonidae” ( Fig. 1C ). The paraphyly of hemiramphids was also supported by Tibbetts (1991) and Aschliman, Tibbetts & Collette (2005) . The halfbeak Dermogenys (which is included in the present study) was found to be a member of the Zenarchopteridae, which comprise a subset of hemiramphids of the Indo-West-Pacific ( Anderson & Collette, 1991 ; Lovejoy, 2000 ; Meisner, 2001 ). Zenarchopteridae represents the sister taxon of the clade formed by needlefishes and sauries ( Lovejoy, Iranpour & Collette, 2004 ; Aschliman, Tibbetts & Collette, 2005 ). Other representatives of the traditionally recognized hemiramphids grouped with the Exocoetidae, or as the sister group to the clade Zenarchopteridae + “Belonidae” ( Fig. 1C ).

The complex jaw musculature of Beloniformes has only been studied in very few species so far, and most published descriptions of beloniform species are superficial and insufficiently illustrated, making broad scale phylogenetic comparisons impossible. That makes broad phylogenetic comparisons impossible. The aim of the present study was to illustrate and describe the morphological diversity of cranial musculature of six selected species of Beloniformes in great detail and to compare it to external jaw anatomy. By using manual dissections and histological slide sections I aim to provide a comprehensive anatomical basis for future researchers studying more species in a phylogenetic context.

In the present, purely anatomical study, the great diversity within beloniform subgroups or within non-beloniform groups could not be studied by maintaining the provided extent and detail of illustrations and descriptions. However, I present some considerations about the potential phylogenetic relevance of some characters that have to be tested in future studies. Therefore, four selected near related acanthopterygian species, which may serve as outgroup in future phylogenetic studies, are described. In addition to two atherinomorph species, I included the percomorph Perca fluviatilis , which was recently used to define the ancestral pattern of atherinomorph jaw musculature ( Hertwig, 2008 ), and the mugilomorph Rhinomugil corsula , which is possibly closer related to Atherinomorpha ( Stiassny, 1990 ; Setiamarga et al., 2008 ; Near et al., 2013 ). A preliminary character mapping is presented.

Materials and Techniques

Taxonomic sampling.

The cranial anatomy of ten acanthopterygian species was studied, including six species of Beloniformes ( Figs. 2 – 20 ). Specimens from the following collections were used: Phyletisches Museum der Friedrich Schiller Universität Jena, Germany (ISZE), Smithsonian Institution of the National Museum of Natural History Washington, USA (USNM), Naturhistorisches Museum der Burgergemeinde Bern, Switzerland (NMBE).

Skin is removed. Abbreviations of muscles (m., musculus) and selected bones: A1, external section of m. adductor mandibulae; A2/3, internal section of m. adductor mandibulae; AAP, m. adductor arcus palatini; den, dentary; DO, m. dilatator operculi; EA, epaxial musculature; lac, lacrimal; LAP, m. levator arcus palatini; LO, m. levator operculi; max, maxilla; op, opercle; PH, m. protractor hyoidei; pop, preopercle; T, m. trapezius. Drawings not to scale. For detailed labelling, scales, histological sections, and further illustrations see Figs. 5 – 20 .

(A–D) Histological sections in a juvenile specimen; compare to Fig. 19

(A–D) Manual dissections. Compare to Fig. 2A .

(A–D) Manual dissections; levels of histological sections ( Fig. 7 ) are indicated. Compare to Fig. 2B .

(A–D) Histological sections; compare to Fig. 6 .

(A–D) Manual dissections; levels of histological sections ( Fig. 9 ) are indicated. For one further manual dissection of this species see Fig. 12D . Compare to Fig. 2C .

(A–D) Histological sections; compare to Figs. 8 and 12D .

(A–C) Oryzias latipes ; levels of histological sections ( Fig. 13 ) are indicated. (A) and (C) modified from Werneburg & Hertwig (2009) . Compare to Fig. 2E . (D) Atherina boyeri ; for other dissections of this species see Fig. 8 , for histological sections see Fig. 9 . Compare to Fig. 2C .

(A–D) Manual dissections; levels of histological sections ( Fig. 11 ) are indicated. Compare to Fig. 2D .

(A–D) Histological sections; compare to Fig. 10 .

(A–D) Histological sections; compare to Fig. 12 . Modified from Werneburg & Hertwig (2009) .

Serial sections through the head. Slice thickness, 12 µm. Section numbers: (A) 14, (B) 170, (C) 206, (D) 268, (E) 340, (F) 440, (G) 450 (lenses redrawn), (H) 586, (I) 648, (J) 698. Bar scale provided for (A–J). Magnifications B’, D’, I’–J’ are not to scale. Compare to the other adrianichthyid studied herein, Oryzias latipes ( Figs. 2E , 12A – 12C and ​ and13 13 ).

(A–D) Manual dissections; levels of histological sections ( Fig. 15 ) are indicated. Compare to Fig. 2F .

(A–D) Histological sections; compare to Fig. 14 .

(A–C) Manual dissections; levels of histological sections ( Fig. 17 ) are indicated. Compare to Fig. 2G .

(A–D) Histological sections; compare to Fig. 16 .

(A–C) Manual dissections. Compare to Fig. 2H .

(A–D) Manual dissections in an adult specimen; approximate levels of histological sections of a juvenile ( Fig. 20 ) are indicated.

For a phylogenetic analysis, published information on further beloniform, namely hemiramphid species, Hyporhamphus unifasciatus (Ranzani, 1841), Nomorhamphus sp. aff. ravnaki (Brembach, 1991), and Hemirhamphodon phaiosoma (Bleeker, 1852), were included ( Table 1 , Fig. 4 ). According to the new findings of Werneburg & Hertwig (2009) , the data on O. latipes were modified when compared to Hertwig (2005) , Hertwig (2008) and Werneburg (2007) .

Arrangement of the species studied herein and those from the literature (*) used for the reconstruction of character evolution (character mapping); following Lovejoy, Iranpour & Collette ( 2004 ; compare to Fig. 1C ). Outlines indicate the species, which were manually dissected herein; not to scale (compare to Figs. 5 – 20 ).

For the phylogenetic arrangement of species see Fig. 4 .

Anatomical observations

Standard procedures for histology and manual dissection are those used by Werneburg (2007) and Werneburg & Hertwig (2009) .

For dissection, two or more specimens per species were used. In the first step of dissection (summarised in Fig. 2 ) the lateral view of the skinned head including all muscles in their unaltered place, including the jaw adductor musculature, opercle-, and suspensoric-related musculature, was documented. In the second step, the external section of m. adductor mandibulae (A1) was mostly removed and the course of the internal section of m. adductor mandibulae (A2/3) was depicted. Further steps of dissection did allow inspection of the symplectic in lateral view with the A2/3 completely or partly removed. Finally, the medial view of the jaw apparatus was documented with a focus on the musculature medial of the lower jaw, namely the intramandibular section of m. adductor mandibulae ( Aω ), the anterior part of m. protractor hyoidei, and m. intermandibularis.

Serial sections were prepared for all species (slice thickness = 12 µm), except for Pe. fluviatilis and B. belone due to the size of these species. The positions of the sections are indicated in the dissection figures ( Figs. 6 , ​ ,8, 8 , ​ ,10, 10 , ​ ,12, 12 , ​ ,14, 14 , ​ ,16 16 and ​ and19). 19 ). For S. saurus , a juvenile specimen was used for histological sectioning ( Fig. 20 ), whereas for manual dissections and character coding (as for all species), adult specimens were used ( Fig. 20 ).

Nomenclature

Osteological nomenclature follows Weitzman (1962) and Weitzman (1974) with modifications as summarised by Hertwig (2008) . Basic myological terminology is that of Werneburg (2011) . Fish muscle nomenclature mainly corresponds to that of Winterbottom (1974) . The homologisation of particular muscular portions follows Werneburg & Hertwig (2009) . The nomenclature of the nervous system refers to Holje, Hildebrand & Fried (1986) . For osteological and, if available, for myological comparisons, I relied on Osse (1969) for Perciformes; on Thomson (1954) for Mugilomorpha; on Kulkarni (1948) , Rosen (1964) , Karrer (1967) , Hertwig (2005) and Hertwig (2008) for Adrianichthyidae and Cyprinodontiformes; on Clemen, Wanninger & Greven (1997) , Greven, Wanninger & Clemen (1997) , Meisner (2001) , and Shakhovskoi (2002) for hemiramphids; on Khachaturov (1983) and Shakhovskoi (2004) for Exocoetidae; and on Chapman (1943) for Scomberesocidae.

Character evolution

Using PAUP* ( Swofford, 2003 ), a character mapping was performed. Therefore, the topology of Lovejoy, Iranpour & Collette (2004) was used as template to arrange the phylogeny of the beloniform species studied herein and of three additional hemiramphid species ( Fig. 4 ; cf. Fig. 1C ). For the interrelationship of major acanthopterygian groups, the present study follows the findings of Stiassny (1990) , Setiamarga et al. (2008) , and Near et al. (2013) . Therein, Percomorpha form the sister taxon to Ovalentaria. Consequently a polarisation of characters is given. The topology for the character mapping was drawn using the move branch function in Mesquite 2.01 ( Maddison & Maddison, 2011 ).

Results and Discussion

Characters and character mapping.

In total, 37 soft tissue characters are described and discussed below. The character matrix can be found in Table 1 . The results of the character mapping are listed in Table 2 . Therein, the consensus of Acctran and Deltran optimizations are documented. Due to the particular focus on the morphological descriptions and illustration of this study, the taxonomic sampling is limited. Also the available data from the literature record is limited. As such, I avoid discussing the character changes in detail. They should serve as summary of character distribution of the species studied herein. The phylogenetic relevance of the characters should be subject of evaluation and discussion in future, more quantitative analyses of the cranial musculature of Beloniformes. Those studies may also consider more closely related species for the comparison with Atherinomorpha.

External section of the m. adductor mandibulae complex (A1)

The m. adductor mandibulae is differentiated into different muscle sections in teleost fishes, representing a complex of individual muscles, each having a separated origin, course, and insertion ( Diogo, 2008 ; Diogo & Abdala, 2010 ). The external section of m. adductor mandibulae complex, A1, is the lateral-most jaw muscle. If present, it originates posteriorly on the suspensorium and/or on the preopercle, it runs rostrad, and has a tendinous insertion to the upper or lower jaw (i.e., Allis, 1897 ).

General appearance. An A1 is present in Perca fluviatilis ( Figs. 2A and ​ and5), 5 ), Rhinomugil corsula ( Figs. 2B , ​ ,6 6 and ​ and7), 7 ), Atherina boyeri ( Figs. 2C , ​ ,8, 8 , ​ ,9 9 and 12D ), Aplocheilus lineatus ( Figs. 2D , ​ ,10 10 and ​ and11), 11 ), Oryzias latipes ( Figs. 2E , 12A – 12C and ​ and13), 13 ), and Xenopoecilus oophorus ( Fig. 3 ) [character state 0] but is absent in all other species studied herein, namely Dermogenys pussila , Parexocoetus brachypterus , Belone belone , and Scomberesox saurus [state 1].

In O. latipes , Hertwig (2008) and Werneburg & Hertwig (2009) described a lateral muscle of the adductor complex with an insertion to the lower jaw. It could be interpreted in two different ways: First, it could represent A1, the possession of which is plesiomorphic; A1 is present in all non-beloniform fishes studied and in O. latipes , it autapomorphically would have shifted its insertion to the lower jaw. Second, A1 could be reduced in O. latipes ( Hertwig, 2005 ). In that case, one additional step of transformation would be needed, as the internal section of m. adductor mandibulae (A2/3) would be modified secondarily. Hertwig (2005) followed the principle of parsimony and opted for the first explanation. Werneburg (2007) interpreted an insertion of A1 to the maxilla and homologised the muscle to the A1 of the outgroup representatives. After reanalysing, this finding was revised and A1 actually inserts on the posterior edge of the dentary at two-thirds of its height below the coronoid process of this bone and has contact via connective tissue to the lig. maxillo-mandibulare in this species ( Werneburg & Hertwig, 2009 ). Previously, the latter connection was misinterpreted as an upper jaw insertion ( Werneburg, 2007 ).

Wu & Shen (2004) mentioned a small ventrolateral portion of A1, their A1-VL, in two flying fish species. As Hertwig ( 2005 : 39) already pointed out, the homologisations of those authors remain unclear. Moreover, the illustration of that portion is lacking. It appears that Wu & Shen (2004) may have confused this portion with the lateral subdivision of A2/3. Hertwig ( 2008 , 149) wrote: ‘In an extensive comparative study of the m. adductor mandibulae in teleostean fishes, [the authors], however, did not mention a subdivision of A2/3 either in the Mugilomorpha or in the Atherinomorpha, but this is probably down to their limited taxon sample, which comprised only three species of the latter.’ If Wu & Shen (2004) actually identified the remainder of A1 as their A1-VL (supported by the fact that an insertion of A1-VL to the maxilla is present), a high interspecific variability may be hypothesised for the flying fishes.

Starks (1916) dissected a belonid species, Tylosurus acus , in which he described an A1-muscle. Following the present homologisation, however, that muscle clearly represents the lateral head of the muscle A2/3, which has a similar anatomy as found in B. belone (see also below) and S. saurus ( Figs. 2H and ​ and18 18 – 20 ).

Orientation. The spatial orientation of A1 to the more medial, internal section of m. adductor mandibulae (A2/3) is different among species. In R. corsula ( Figs. 2B , ​ ,6 6 and ​ and7), 7 ), the A1 is situated ventrolaterally to the lateral head of A2/3 and three-fourths of this head are still visible in lateral view [state 0]. In Pe. fluviatilis , the muscle is situated dorsolateral to the internal section and the complete lateral head (A2/3, lateral) is not covered in lateral view ( Figs. 2A and ​ and5) 5 ) [state 1]. A1 is situated completely lateral to the intermedial head of the internal section of m. adductor mandibulae (A2/3, intermedial) in Ap. lineatus ( Figs. 2D , ​ ,10 10 and ​ and11), 11 ), O. latipes ( Figs. 2E , 12A – 12C and ​ and13; 13 ; see also Werneburg & Hertwig, 2009 ), and X. oophorus ( Fig. 3 ) and the lateral head (A2/3, lateral) is only covered in its anterior region [2(2)]. Laterally in At. boyeri ( Figs. 2C , ​ ,8, 8 , ​ ,9 9 and 12D ), the A1 completely covers the internal section of m. adductor mandibulae (A2/3) [state 3].

For the ground pattern of Atherinomorpha, Hertwig (2005) proposed that the external (A1) and internal (A2/3) sections are situated next to each other in a horizontal plane. As an outgroup of Atherinomorpha, the author used Pe. fluviatilis , in which the A2/3-portions are situated above each other in a horizontal plane ( Figs. 2A and ​ and5). 5 ). In the present study, R. corsula was dissected as an additional, potential outgroup species, which is closely related to Atherinomorpha. Similar to Atherinomorpha ( sensu Hertwig, 2008 ), the A1 of that species also has to be interpreted to be lateral to the A2/3 in a horizontal plane. As such, that character has to be withdrawn as an autapomorphy of Atherinomorpha. More detailed observation among Percomorpha could identify the orientation of A1 to A2/3 in Pe. fluviatilis ( Figs. 2A and ​ and5) 5 ) as autapomorphy of Percomorpha or only of that species. In the latter case, the ‘A1 in horizontal plane to A2/3’ would need to be interpreted as plesiomorphic among Acanthopterygii. Observations among Mugilomorpha could identify the orientation of A1–A2/3 as a homoplastic character of R. corsula and Atherinomorpha. If all members of Mugilomorpha had an A1 lateral to A2/3, and when following the phylogenetic hypothesis of Stiassny (1990) , that spatial orientation would need to be interpreted as a synapomorphy of Mugilomorpha + Atherinomorpha.

Insertion. The tendon of A1 inserts on the lateral face of the anterior part of the maxilla in Pe. fluviatilis ( Figs. 2A and ​ and5) 5 ) [state 0], to the medial face of the middle region of the maxilla in R. corsula ( Figs. 2B , ​ ,6 6 and ​ and7) 7 ) and X. oophorus ( Fig. 3 ) [state 1], and to the posterior edge of the dentary in O. latipes ( Figs. 2E , 12A – 12C and ​ and13) 13 ) [state 2]. With three tendons, A1 inserts on the processus primordialis (anguloarticularis), to the medial side of the lacrimal, and medially to the anterodorsal tip of the maxilla in At. boyeri ( Figs. 2C , ​ ,8, 8 , ​ ,9 9 and 12D ) [state 3]. The A1 inserts with two tendons to the lateral face of the medial part of the maxilla and to the medial face of the lacrimal in Ap. lineatus ( Figs. 2D , ​ ,10 10 and ​ and11) 11 ) [state 4].

The insertion of A1 to the jaws is different in all species studied. A definition of homology (e.g., A1 inserts laterally to the maxilla) was not made, because the differences of A1 were too large. Hertwig (2008) observed several atherinomorph species and defined the insertion of A1 at the lateral face of the maxilla to be present in Pe. fluviatilis and “Aplocheilidae”. In contrast to Pe. fluviatilis ( Figs. 2A and ​ and5), 5 ), however, the A1 inserts on the other end of the maxilla in Ap. lineatus ( Figs. 2D , ​ ,10 10 and ​ and11). 11 ). The latter species has an additional tendon to the medial face of the lacrimal, a character which was found by Hertwig (2008) to be present in the ground pattern of Atherinomorpha (compare to Alexander, 1967 ; Parenti, 1993 ; Stiassny, 1990 ). For Cyprinodontiformes (incl. Aplocheilus ), Hertwig (2005) was not able to define an unambiguous constellation of the insertion of A1. However, he argued that the insertion of A1 shifted based on the rotation of the maxilla in this taxon. As such, the insertion of A1 to the lateral face of the maxilla could be interpreted as being plesiomorphic among Atherinomorpha.

Internal section of the m. adductor mandibulae complex (A2/3)

The A2/3 usually originates with two or three muscle heads on the suspensoric and on the preopercle and inserts as a consistent muscle to the lower jaw. Muscle heads are defined as partial differentiations of a muscle. They have separated origins or insertions ( Werneburg, 2007 ; Werneburg, 2011 ). Muscle heads gain a descriptive nomenclature herein; their position of origin (or insertion) and the spatial orientation were considered. This nomenclature differs from Winterbottom (1974) , because that one is not applicable for muscle heads herein.

A2/3 can have an intramandibular portion. A muscle portion is defined as having a separate origin, course, and insertion, but as having some intertwining fibres or a shared tendon with another muscle portion of the same ontogenetic and/or phylogenetic origin ( Werneburg, 2007 ; Werneburg, 2011 ).

Origin. In Pe. fluviatilis ( Figs. 2A and ​ and5), 5 ), Pa. brachypterus ( Figs. 2F , ​ ,14 14 and ​ and15), 15 ), and D. pussila ( Figs. 2G , ​ ,16 16 and ​ and17), 17 ), the A2/3 has two muscle heads (A2/3, lateral; A2/3, medial) in its origin [state 0]. A2/3 originates with three muscle heads (A2/3, lateral; A2/3, medial; A2/3, intermedial) in R. corsula ( Figs. 2B , ​ ,6 6 and ​ and7), 7 ), Ap. lineatus ( Figs. 2D , ​ ,10 10 and ​ and11), 11 ), O. latipes ( Figs. 2E , 12A – 12C and ​ and13), 13 ), X. oophorus ( Fig. 3 ), B. belone ( Figs. 2H and ​ and18), 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 1].

The cyprinodontiform species Ap. lineatus ( Figs. 10 and ​ and11) 11 ) was found to have three muscle heads at its origin. This corresponds to the findings of Hertwig (2008) . To confirm his findings, Hertwig (2008) used histological sections, which permit a much higher accuracy when distinguishing between minute muscle heads. I have seen many of the sections and used some herein, and can confirm his observations.

Jourdain (1878) described a specimen of B. belone (“ vulgaris ”), in which A2/3 was not separated. I dissected several specimens of that species and always found a separation, although I have to note that the differentiation of the lateral and the medial head were difficult. Also, apparently, Jourdain (1878) did not remove the lateral head of A2/3 as he expected A2/3 to represent an undifferentiated muscle mass and hence did not discover the intermedial head of A2/3.

The lateral head. The lateral head of A2/3 originates almost overall at the vertical aspect of preopercle, at the posterior part of the horizontal aspect of the preopercle, as well as on the processus lateralis hyomandibularis in R. corsula ( Figs. 2B , ​ ,6 6 and ​ and7), 7 ), Ap. lineatus ( Figs. 2D , ​ ,10 10 and ​ and11), 11 ), B. belone ( Figs. 2H and ​ and18), 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 0]. It originates at the vertical aspect of the preopercle (but does not reach its dorsal most tip) and at more than half of the horizontal aspect of the preopercle in D. pussila ( Figs. 2G , ​ ,16 16 and ​ and17) 17 ) [state 1]. In Pe. fluviatilis ( Figs. 3A and ​ and5) 5 ) and Pa. brachypterus ( Figs. 2F , ​ ,14 14 and ​ and15), 15 ), the lateral head originates ventrally at the processus lateralis hyomandibularis, at the ventral third of the vertical aspect of the preopercle, as well as on the processus caudalis quadrati [state 2]. With a narrow attachment, it only originates on the ventral third of the vertical aspect of the preopercle in O. latipes ( Figs. 2E , 12A – 12C and ​ and13) 13 ) and X. oophorus ( Fig. 3 ) [state 3].

Medial head. In Pe. fluviatilis , the medial head of A2/3 originates from the hyomandibular, the metapterygoid, and the symplectic, as well as from processus lateralis hyomandibularis ( Fig. 5 ) [state 0]. It originates from the hyomandibular and from the metapterygoid in R. corsula ( Figs. 6 and ​ and7) 7 ) [state 1] or only from the metapterygoid in Ap. lineatus ( Figs. 10 and ​ and11) 11 ) and Pa. brachypterus ( Figs. 2F , ​ ,14 14 and ​ and15) 15 ) [state 2]. It arises from the lateral faces of the quadrate, the symplectic, and the cartilaginous interspaces of the hyopalatine arch, and from the tendon of the m. adductor arcus palatini quadrati in O. latipes ( Figs. 12A – 12C and ​ and13) 13 ) and X. oophorus ( Fig. 3 ) [state 3]. The medial head of A2/3 originates ventrally at the sphenotic, laterally at the hyomandibular, and dorsally at the metapterygoid in D. pussila ( Figs. 16 and ​ and17), 17 ), B. belone ( Figs. 2H and ​ and18), 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 4].

Similar to the present study, Hertwig (2005) and Hertwig (2008) found the origin of the medial head of A2/3 to be highly variable. In addition to an adult specimen of S. saurus , a juvenile was studied ( Figs. 9E – 9H ). In this specimen, a different orientation of the A2/3-heads was found ( Werneburg, 2007 ). One could hypothesise that the medial head of A2/3 in the juvenile shifts its origin to a dorsal position and the intermedial head of A2/3 could shift its origin to a more ventral position (two transformation steps). Alternatively, the origin of the medial A2/3-head of the juvenile could shift ventrolaterally to the intermedial head of A2/3 and would be homologous to the intermedial head of A2/3 in the adult. Hence, the intermedial head of A2/3 in the juvenile (then the medial head of the adult) would keep its origin at the sphenotic (one transformation step). Those scenarios are very speculative because they are derived from only one observation. No final answer can be presented, because the variability of that character within S. saurus cannot be estimated. The species D. pussila , B. belone , and S. saurus show a very drastic ontogenetic elongation of the lower jaw (Hemiramphidae) or of both jaws (Belonidae, Scomberesocidae) ( Boughton, Collette & McCune, 1991 ; Lovejoy, 2000 ; Lovejoy, Iranpour & Collette, 2004 ). It would be valuable to study if, correlated to the elongation of jaws, changes in the anatomy of the jaw musculature occur (origin, volume, course, insertion). Comparative ontogenetic and electromyographic studies ( Focant, Jacob & Huriaux, 1981 ; Osse, 1969 ) could help to interpret the specific case mentioned herein. Ontogenetic changes in the anatomy of the jaw musculature were already observed by Hertwig (2005) in representatives of Goodeidae (Cyprinodontiformes: Crenichthys ). Nanichthys (Scomberesocidae) is often not accepted as a ‘genus’ in a taxonomic sense and is often referred to as a dwarf morphotype of Scomberesox ( Collette, 2004 ; Collette et al., 1984 ). However, if the juvenile specimen of S. saurus studied herein would actually represent a member of a valid genus Nanichthys , the arrangement of the A2/3-musculature may serve as a criterion to distinguish both species taxonomically.

Intermedial head. The intermedial head of A2/3 is situated between the lateral and the medial head. It originates only on the horizontal aspect of the preopercular in R. corsula ( Figs. 6 and ​ and7) 7 ) [state 0]. It takes its origin from the horizontal aspect of the preopercle and at the processus caudalis quadrati in Ap. lineatus ( Figs. 10 and ​ and11), 11 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 1] and originates only on the processus caudalis quadrati in O. latipes ( Figs. 12A – 12C and ​ and13) 13 ) and X. oophorus ( Fig. 3 ) [state 2]. An intermedial head is not present in Pe. fluviatilis , At. boyeri , Pa. brachypterus , and D. pussila .

Muscle portions. Unlike in all other species [state 0], A2/3 is laterally separated into two portions (by definition; see above and Werneburg, 2011 ) in At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ) [state 1]. The muscle portions of A2/3 have separated origins lateral at the posterior part of the suspensoric as well as separated insertions medial to the lower jaw. The medial portion of A2/3 is differentiated into two heads at its origin. The lateral portion of its A2/3 is not separated into heads. Among the species studied herein, and indeed, considering data from Hertwig (2008) regarding several other atherinid species, this condition has to be declared autapomorphic for At. boyeri (Atheriniformes).

Orientation of muscle heads. The spatial orientations of the medial and the lateral head of A2/3 are different among species. In Pe. fluviatilis ( Figs. 2A and ​ and5), 5 ), Ap. lineatus ( Figs. 10 and ​ and11), 11 ), D. pussila ( Figs. 2G , ​ ,16 16 and ​ and17), 17 ), X. oophorus ( Fig. 3 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20), 20 ), the medial head of A2/3 is situated dorsally to the lateral head or is at least clearly visible in lateral view [state 0]. The medial head of A2/3 is situated ventrally to the lateral head in At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ) [state 1]. The lateral head is situated laterally to the medial head and can cover it completely in R. corsula ( Figs. 6 and ​ and7), 7 ), O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), and Pa. brachypterus ( Figs. 2F , ​ ,14 14 and ​ and15) 15 ) [state 2].

Relative size of muscle heads. The medial and the lateral heads of A2/3 have about the same size in Pe. fluviatilis ( Fig. 5 ) and D. pussila ( Figs. 16 and ​ and17) 17 ) [state 0]. The medial head is relatively narrow when compared to the lateral head in Pa. brachypterus ( Figs. 14 and ​ and15) 15 ) [state 1]. The lateral head is quite widespread when compared to the medial head in R. corsula ( Figs. 6 and ​ and7) 7 ) and Ap. lineatus ( Figs. 10 and ​ and11) 11 ) [state 2]. The medial head is larger than the lateral head in O. latipes ( Figs. 2E , 12A – 12C and ​ and13), 13 ), X. oophorus ( Fig. 3 ), B. belone ( Figs. 2H and ​ and18), 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 3].

Insertion. Except for B. belone ( Figs. 2H and ​ and18) 18 ) and S. saurus ( Figs. 19 and ​ and20), 20 ), A2/3 only inserts on the medial side of the lower jaw [state 0]. In the former species, it also inserts on the coronomeckelian bone [state 1], which is only found in these two species. It represents a bone, which is posterodorsally fused with the border of processus primordialis anguloarticularis. Both bones are separated from each other by a clear suture ( Werneburg, 2007 ).

Intramandibular portion. An intramandibular portion of A2/3 is lacking in all Beloniformes [state 0]. It is present in R. corsula ( Figs. 6 and ​ and7) 7 ) and has a narrow insertion on the medial face of processus coronoideus dentalis [state 1]. In Ap. lineatus ( Figs. 10 and ​ and11), 11 ), it has broad insertions to the processus coronoideus dentalis, to cartilago Meckeli, and to the anguloarticular [state 2]. It inserts medially to the dentary in At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ) [state 3] and has a narrow insertion medially to the anguloarticular in Pe. fluviatilis ( Fig. 5 ) [state 4].

The configuration of the intramandibular portion of A2/3 is different among non-beloniforms species studied here. As the criterion of homology, the intramandibular portion is defined to originate from an A2/3-associated aponeurosis or tendon herein. Hertwig (2008) , who observed few species of Beloniformes ( O. latipes and some hemiramphids), argued for an autapomorphic reduction of an intramandibular portion of A2/3 within Beloniformes, which I can confirm herein.

Intramandibular muscles possibly act in positioning the jaw ( Karrer, 1967 : “Stellbewegung”). Hertwig (2005) and Hertwig (2008) mentioned the reduction of intramandibular muscles and found a correlation between the loss of those muscles and a reduced mobility of particular bone elements. For Empetrichthys latos (Cyprinodontiformes), he noticed an ontogenetic reduction of intramandibular muscles. The movement of upper jaw bones in Beloniformes may be coupled to the movement of the lower jaw (see above) and hence they may underlie large mechanical stresses in fish hunting species. To withstand those forces, the bones of the lower jaw may have a higher degree of fusion resulting in the tendency to reduce intramandibular musculature.

Like Hertwig (2008) , I defined an intramandibular portion of A2/3 as present in Pe. fluviatilis . However, the configuration of the intramandibular musculature of Pe. fluviatilis could be interpreted differently. In the present study, two intramandibular muscles were differentiated. First, an intramandibular portion of A2/3 is described as originating from the tendon of A2/3 by only a few muscle fibres. It narrowly inserts on the medial face of the anguloarticulare. Second, an intramandibular m. adductor mandibulae ( Aω ) is described, which is tendinously originating from the preopercular and the quadrate. That muscle has a flat insertion medially to the dentary, to cartilago Meckeli, and to the anguloarticular.

In contrast, Osse (1969) only described one intramandibular muscle for Pe. fluviatilis . That muscle, “ Aω ” in Osse (1969) , has one origin at the tendon of A2/3. This “ Aω ” also has a narrow attachment to the anguloarticular, one tendinous attachment to the prearticular/quadrate and one flat insertion to the medial face of the lower jaw. Osse (1969) combined the Aω and the intramandibular portion of A2/3 of the present study as his “ Aω .” Therefore, he did not differentiate the course of muscle fibres and other associated structures. The fibres of the intramandibular portion of A2/3 of the present study run anteroventrad. The fibres of the Aω were found to originate as a double fibred muscle from the tendon originating from the prearticular/quadrate. However, some fibres also originate from the tendon of A2/3, which is only partly fused with the tendon of Aω . While both tendons fuse, the course of the Aω -tendon is still separable ( Fig. 5D ). The fusion of the tendons and the origin of some Aω -fibres at the A2/3-tendon may have persuaded Osse (1969) to define only one intramandibular muscle.

One additional interpretation of intramandibular muscle configuration is possible. If a tendinous insertion of A2/3 to the tendon of Aω is hypothesised, the origin of some Aω -fibres may have been shifted to the tendon of A2/3. In that case, no intramandibular portion of A2/3 would exist in Pe. fluviatilis . If this configuration is a plesiomorphic condition of Acanthopterygii, the character should also be interpreted as a reversal within Beloniformes. In contrast, if one hypothesises the intramandibular portion of A2/3 to be independently reduced in Pe. fluviatilis , the character should be considered as homoplastic in Pe. fluviatilis (Percomorpha) and Beloniformes. To clarify that controversy, additional species of Percomorpha and Acanthopterygii need to be observed in great detail, but this was outside the scope of the present study.

Intramandibular section of the m. adductor mandibulae complex ( Aω )

The intramandibular section of the m. adductor mandibulae complex ( Aω ) connects the suspensoric with the medial face of the lower jaw.

Origin. It originates with a tendon anteriorly at the medial face of the symplectic in Pa. brachypterus ( Figs. 14 and ​ and15) 15 ) and D. pussila ( Figs. 16 and ​ and17) 17 ) [state 0]. It originates directly at the ventral and the anterior edge of the quadrate in O. latipes ( Figs. 12A – 12C and ​ and13) 13 ) [state 1]. In R. corsula ( Figs. 6 and ​ and7), 7 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20), 20 ), Aω originates broadly on the medial face of the quadrate and a part of the muscle can have a tendinous origin [state 2]. It attaches with a tendon anteroventrally to the medial face of the quadrate in At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ) and Ap. lineatus ( Figs. 10 and ​ and11) 11 ) [state 3]; and in Pe. fluviatilis ( Fig. 5 ), it originates with a tendon anteriorly at the medial face of the horizontal aspect of the preopercular and to a small amount medially at the middle area of processus caudalis quadrati [state 4]. The Aω is absent in X. oophorus [state 5].

Hertwig (2005) defined as a common character of hemiramphids: The origin of the flat tendon of Aω is situated at a part of the symplectic, which points rostrad. He studied species of Hyporhamphus , Nomorhamphus , and Hemiramphodon . Due to the diverging observation in D. pussila herein ( Figs. 16 and ​ and17), 17 ), this character on the origin of Aω cannot be confirmed to be diagnostic for all hemiramphids. However, as that character was also found in Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), a potential synapomorphic character of (Exocoetidae + Hemiramphidae) is identified and a possible monophyly of Hemiramphidae could be indicated ( Rosen, 1964 ; Rosen & Parenti, 1981 ; Collette et al., 1984 ). This would contradict the works of Lovejoy, Iranpour & Collette (2004) and Aschliman, Tibbetts & Collette (2005) , who found “Hemiramphidae” paraphyletic. In the work of Lovejoy, Iranpour & Collette (2004) , the Zenarchopteridae (among others Dermogenys , Hemiramphodon , Nomorhamphus ) oppose the paraphyletic “Belonidae” (incl. Scomberesocidae) and Hyporhamphus belongs to a group, which opposes (Zenarchopteridae + “Belonidae”). Several species of “Hemiramphidae” that are closely related to Exocoetidae in the work of Lovejoy, Iranpour & Collette (2004) , as well as several other species of the remaining groups of Beloniformes need to be observed to gain a better understanding on how that character is distributed. The absence of Aω was documented for some atherinomorph species by Hertwig (2008) and the reduction must have occurred several times independently.

Shape. In R. corsula ( Figs. 6 and ​ and7), 7 ), Aω is separated into two heads at the level of the quadrate. The lateral head inserts broadly to the medial face of the dentary and cartilago Meckeli. The medial head of Aω inserts ventrally to the medial face of the dentary and anteriorly to the medial face of the anguloarticular [state 0]. The Aω represents a double-feathered muscle in Pe. fluviatilis ( Fig. 5 ), At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), D. pussila ( Figs. 16 and ​ and17), 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20), 20 ), in which one of the muscle parts may project to a far caudad direction [state 1]. The Aω is a parallel fibred muscle in O. latipes ( Figs. 12A – 12C and ​ and13) 13 ) and Pa. brachypterus ( Figs. 14 and ​ and15) 15 ) [state 2] and a simple feathered muscle in Ap. lineatus ( Figs. 10 and ​ and11) 11 ) [state 3].

Insertion. On the medial face of the lower jaw, the Aω (when not differentiated into heads) inserts broadly to the dentary, cartilago Meckeli and/or to the anguloarticular in Pe. fluviatilis ( Fig. 5 ), At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), and D. pussila ( Figs. 16 and ​ and17) 17 ) [state 0]. It inserts broadly to the dentary, to the anguloarticular, and to the cartilago Meckeli, whereby a ventral part in feathered muscles inserts far anteriorly to the medial face of the dentary in B. belone ( Fig. 18 ) and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 1]. It inserts to the ventral part of the dentary in Ap. lineatus ( Figs. 10 and ​ and11) 11 ) [state 2] and posteriorly to the dentary and medially at the cartilago Meckeli in O. latipes ( Figs. 12A – 12C and ​ and13) 13 ) [state 3].

Hertwig (2005) and Hertwig (2008) has shown that the configuration of Aω is highly variable among Cyprinodontiformes. In comparison, this can also be concluded for the species observed herein.

M. intermandibularis

Cross section. M. intermandibularis connects the contralateral dentaries at their medial faces. The cross-section of m. intermandibularis is +/− round in At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ) [state 0]. It is big-bellied oval in Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and ​ and7), 7 ), O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), and X. oophorus ( Fig. 3 ); i.e., it is at its maximum twice as broad as high [state 1]. It is elongated oval in Ap. lineatus ( Figs. 10 and ​ and11), 11 ), Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), D. pussila ( Figs. 16 and ​ and17), 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20); 20 ); i.e., it is (mostly much) more than twice as broad as high [state 2].

In each species studied, several specimens were observed and a tendency of a rounder cross-section of the muscle was found in At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ). In addition, the assignment to big-bellied or elongated oval has to be understood as a tendency in the variability of the specimens observed.

Shape. The m. intermandibularis is parallel fibred and has no tendinous origin at the dentary in Pe. fluviatilis ( Fig. 5 ), At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), D. pussila ( Figs. 16 and ​ and17), 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 0]. However, it is spindle-shaped and has a tendinous origin at the dentary in R. corsula ( Figs. 6 and ​ and7), 7 ), Ap. lineatus ( Figs. 10 and ​ and11), 11 ), O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), and X. oophorus ( Fig. 3 ) [state 1].

M. protractor hyoidei

Origin. The m. protractor hyoidei connects the branchial apparatus with the lower jaw. It originates laterally at the ceratohyal in Pe. fluviatilis ( Fig. 5 ), Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), and D. pussila ( Figs. 16 and ​ and17) 17 ) [state 0], with two heads ventrally and laterally at the ceratohyal and at the anterior tips of the branchiostegal rays in O. latipes ( Figs. 12A – 12C and ​ and13) 13 ) [state 1], ventrally to the ceratohyal in R. corsula ( Figs. 6 and ​ and7), 7 ), At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), Ap. lineatus ( Figs. 10 and ​ and11), 11 ), and X. oophorus ( Fig. 3 ) [state 2] and medially to the ceratohyal in B. belone ( Fig. 18 ) and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 3].

Course. A fusion with the contralateral m. protractor hyoidei occurs at the level of the jaws or suspensoric and united, they travel rostrad in R. corsula ( Figs. 6 and ​ and7), 7 ), Ap. lineatus , O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), X. oophorus ( Fig. 3 ) (in relation to the jaw joint, the protractor fuses more anteriorly in X. oophorus when compared to O. latipes ), Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), and D. pussila ( Figs. 16 and ​ and17) 17 ) and anteroventrally at the fused mm. protractor hyoidei a tendon can be formed on each side [state 0]. Such a fusion does not occur in Pe. fluviatilis ( Fig. 5 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 1]. In At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), at the level of the anguloarticular, the muscles fuse only in their ventral regions; they separate on the level of the dentary in order to insert independently of the contralateral muscle to the dentary [state 2].

Anterior part. When reaching m. intermandibularis, m. protractor hyoidei has a flat shape in Ap. lineatus ( Figs. 10 and ​ and11), 11 ), O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), and X. oophorus ( Fig. 3 ) [state 0], or it is about as broad as high in Pe. fluviatilis ( Fig. 5 ), At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), D. pussila ( Figs. 16 and ​ and17), 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 1]. At this level, m. protractor hyoidei already differentiated into two heads. The dorsal head is flat and the ventral head is as high as broad in R. corsula ( Figs. 6 and ​ and7) 7 ) [state 2].

When reaching the dentary, the flat shape of the muscle in Ap. lineatus ( Figs. 10 and ​ and11) 11 ) and O. latipes could be hypothesized as being an autapomorphic character of Cyprinodontoidei sensu Rosen (1964) ( Fig. 1A ).

Insertion. M. protractor hyoidei inserts dorsally to the insertion of m. intermandibularis at the dentary and covers at least the posterodorsal area of the latter muscle in Ap. lineatus ( Figs. 10 and ​ and11), 11 ), Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 0]. In Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and ​ and7), 7 ), O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), D. pussila ( Figs. 16 and ​ and17), 17 ), and B. belone ( Fig. 18 ), it inserts ventrally to the m. intermandibularis at the dentary [state 1]. It inserts dorsally as well as ventrally of m. intermandibularis to the dentary in X. oophorus ( Fig. 3 ) [state 2].

Insertion tendon. The ventral part of m. protractor hyoidei extends into a long tendon, which reaches the anterior tip of the lower jaw in D. pussila ( Figs. 16 and ​ and17) 17 ) and B. belone ( Fig. 18 ) [state 0]. It does not extend into a long tendon to reach the anterior tip of the lower jaw in Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and ​ and7), 7 ), At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), and X. oophorus ( Fig. 3 ) [state 1].

The anteroventral elongation of musculature in the region of the dentary seems to be associated with the elongated lower jaw within Beloniformes. In D. pussila ( Figs. 16 and ​ and17) 17 ) and B. belone ( Fig. 18 ), also a ventral insertion of m. adductor mandibulae ( Aω ) to the anterior tip of the lower jaw can be recognised. Besides the latter muscle, m. intermandibularis is also extended far rostrad in S. saurus ( Figs. 19 and ​ and20), 20 ), however, in this species m. protractor hyoidei does not reach the anterior tip of the lower jaw. Referring to Haszprunar (1998) , one could argue that the elongation of a muscle within the lower jaw is simply an adaptation correlated to food ingestion and hence would not have a value for phylogenetic questions. However, as noted by de Pinna (1991) and Haas (2003) , such adaptations can be informative at particular hierarchical levels.

M. adductor arcus palatini

Origin and insertion. The anterior portion of m. adductor arcus palatini, the only portion of this muscle studied herein, originates along the whole parasphenoid and inserts dorsally along the entire suspensoric in R. corsula ( Figs. 6 and ​ and7), 7 ), Ap. lineatus ( Figs. 10 and ​ and11), 11 ), O. latipes ( Figs. 2E , 12A – 12C and ​ and13), 13 ), X. oophorus ( Fig. 3 ), and D. pussila ( Figs. 2G , ​ ,16 16 and ​ and17) 17 ) (in addition to other small attachments) [state 0]. In contrast, it originates on the posterior part of the parasphenoid and inserts on the posterior region of the suspensoric in Pe. fluviatilis ( Figs. 2A and ​ and5), 5 ), At. boyeri ( Figs. 2C , ​ ,8, 8 , ​ ,9 9 and 12D ), Pa. brachypterus ( Figs. 2F , ​ ,14 14 and ​ and15), 15 ), B. belone ( Figs. 2H and ​ and18), 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 1].

M. levator arcus palatini

M. levator arcus palatine originates on the skull roof behind the eye, runs ventrally, and inserts dorsally to the posterior part of the suspensoric.

Origin. It originates broadly on the sphenotic in Pa. brachypterus ( Figs. 2F , ​ ,14 14 and ​ and15) 15 ) and D. pussila ( Figs. 2G , ​ ,16 16 and ​ and17) 17 ) [state 0]. In R. corsula ( Figs. 2B , ​ ,6 6 and ​ and7), 7 ), B. belone ( Figs. 2H and ​ and18), 18 ), and S. saurus ( Figs. 19 and ​ and20), 20 ), it originates on a ridge of the sphenotic, the processus sphenoticus, and some fibres originate directly on the sphenotic [state 1]. The muscle arises via a short tendon from the ventral edge of the transverse process of the sphenotic and runs ventrad along the posterior margin of the orbit, dorsally from the hyomandibular, and with few fibres from the sphenotic in O. latipes ( Figs. 2E , Figs. 12A – 12C and ​ and13) 13 ) and X. oophorus ( Fig. 3 ) [state 2]. It originates ventrally at the dermosphenotic in At. boyeri ( Figs. 2C , ​ ,8, 8 , ​ ,9 9 and 12D ) [state 3] and from the autosphenotic and with some fibres at the sphenotic in Pe. fluviatilis ( Figs. 2A and ​ and5) 5 ) and Ap. lineatus ( Figs. 2D , ​ ,10 10 and ​ and11) 11 ) [state 4].

The m. levator arcus palatini plesiomorphically originates at the autosphenotic and with some fibres at the sphenotic. This condition is also visible in Ap. lineatus ( Figs. 10 and ​ and11) 11 ) and could be assumed as being plesiomorphic for all Cyprinodontiformes (compare to Hertwig, 2005 ; Karrer, 1967 ).

Course. During its course from origin to insertion, the thickness of m. adductor arcus palatini hardly changes in R. corsula ( Figs. 2B , ​ ,6 6 and ​ and7), 7 ), O. latipes ( Figs. 2E , 12A – 12C and ​ and13), 13 ), and X. oophorus ( Fig. 3 ) [state 0], whereas in all other species it becomes more than twice as thick [state 1].

Relation to other muscles. M. levator arcus palatini runs dorsally of the medial and lateral head of A2/3 and does not run between both heads heads in Pe. fluviatilis ( Figs. 2A and ​ and5), 5 ), R. corsula ( Figs. 2B , ​ ,6 6 and ​ and7), 7 ), Ap. lineatus ( Figs. 10 and ​ and11), 11 ), O. latipes ( Figs. 2E , 12A – 12C and ​ and13), 13 ), X. oophorus ( Fig. 3 ), and Pa. brachypterus ( Figs. 2F , ​ ,14 14 and ​ and15) 15 ) [state 0]. It is clearly situated between the lateral and the medial head of A2/3 in D. pussila ( Figs. 16 and ​ and17) 17 ) [state 1] or it is only partly surrounded by the lateral and by the medial head of A2/3 in B. belone ( Figs. 2H and ​ and18) 18 ) and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 2].

Insertion. On the lateral face of the suspensoric of Pe. fluviatilis ( Fig. 5 ), Ap. lineatus ( Figs. 10 and ​ and11), 11 ), Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), D. pussila ( Figs. 16 and ​ and17), 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20), 20 ), m. levator arcus palatini inserts onto the hyomandibular and to the metapterygoid and with some fibres, it also can attach anteriorly to the processus lateralis hyomandibularis [state 0]. In O. latipes ( Figs. 12A – 12C and ​ and13) 13 ) and X. oophorus ( Fig. 3 ), it inserts on the broad face of the praeopercular and posterodorsally to the symplectic [state 1]. In R. corsula ( Figs. 6 and ​ and7) 7 ) and At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), it inserts on the hyomandibular, anteriorly to the processus lateralis hyomandibularis, to the metapterygoid, and to the broad face of the preopercular [state 2].

Kulkarni (1948) identified the metapterygoid as being reduced within Adrianichthyidae. This suggestion was only based on his observations in Horaichthys setnai and O. melastigma . Werneburg & Hertwig (2009) identified a horizontal suture in the ‘symplectic’ ( sensu Kulkarni, 1948 ) of O. latipes , which could represent the border of the metapterygoid. In histological sections and hence in 3D reconstructions ( Werneburg & Hertwig, 2009 ), such a differentiation of bones was not visible. As such, the situation remains unclear.

M. dilatator operculi

Origin. M. dilatator operculi connects the opercle with the skull roof. It originates ventrally at the lateral face of the sphenotic in Pa. brachypterus ( Figs. 2F , ​ ,14 14 and ​ and15), 15 ), X. oophorus ( Fig. 3 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 0]. It originates laterally at the sphenotic, at the autosphenotic, and with some fibres possibly at the anteroventral area of the pterotic in Pe. fluviatilis ( Figs. 2A and ​ and5), 5 ), At. boyeri ( Figs. 2C , ​ ,8, 8 , ​ ,9 9 and 12D ), and Ap. lineatus ( Figs. 2D , ​ ,10 10 and ​ and11) 11 ) [state 1]. In R. corsula ( Figs. 2A , ​ ,6 6 and ​ and7), 7 ), O. latipes ( Figs. 2E , 12A – 12C and ​ and13), 13 ), D. pussila ( Figs. 2G , ​ ,16 16 and ​ and17), 17 ), and B. belone ( Figs. 2H and ​ and18), 18 ), it originates laterally at the sphenotic and anteriorly at the lateral face of the pterotic [state 2].

Shape. Anteriorly, m. dilatator operculi extends almost to the eye and lies dorsally to m. levator arcus palatini in R. corsula ( Figs. 2A , ​ ,6 6 and ​ and7), 7 ), At. boyeri ( Figs. 2C , ​ ,8, 8 , ​ ,9 9 and 12D ), Ap. lineatus ( Figs. 2D , ​ ,10 10 and ​ and11), 11 ), and O. latipes ( Figs. 2E , 12A – 12C and ​ and13) 13 ) [state 0]. It does not reach the eye region in Pe. fluviatilis ( Figs. 2A and ​ and5), 5 ), X. oophorus ( Fig. 3 ), Pa. brachypterus ( Figs. 2F , ​ ,14 14 and ​ and15), 15 ), D. pussila ( Figs. 2G , ​ ,16 16 and ​ and17), 17 ), B. belone ( Figs. 2H and ​ and18), 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 1].

M. levator operculi

Origin. The m. levator operculi connects the opercle with the skull roof. It is an undivided muscle with an origin ventrally at the lateral face of the pterotic in all taxa studied [state 0], except for Pe. fluviatilis . In this species is a bipartite muscle with a large anterior origin ventrally at the lateral face of the pterotic and a small posterior origin ventrally at the ventral situated extrascapula ( Figs. 2A and ​ and5) 5 ) [state 1].

Insertion. M. levator operculi inserts dorsally to the medial face of the opercle and has a continuous horizontal level of insertion in Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and ​ and7), 7 ), Ap. lineatus ( Figs. 10 and ​ and11), 11 ), O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), X. oophorus ( Fig. 3 ) , Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), and D. pussila ( Figs. 16 and ​ and17) 17 ) [state 0]. It also inserts dorsally at the medial face of the opercle in B. belone ( Fig. 18 ) and S. saurus ( Figs. 19 and ​ and20), 20 ), but it attaches more ventrally to the anterior region of the medial face of the opercle [state 1]. The muscle inserts dorsally to the medial face and dorsally to the lateral face of the opercle in At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ) [state 2].

Truncus maxillaris infraorbitalis trigemini. The truncus maxillaris infraorbitalis trigemini branches into the ramus mandibularis trigemini and ramus maxillaris trigemini short before or after leaving the neurocranium in Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and ​ and7), 7 ), At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), and Ap. lineatus ( Figs. 10 and ​ and11)—and 11 )—and dorsally to the suspensoric, the ramus mandibularis trigemini covers the ramus maxillaris trigemini laterally [state 0]. Contrary, in O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), X. oophorus ( Fig. 3 ) , Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), and D. pussila ( Figs. 16 and ​ and17), 17 ), it first branches at the level of the eye [state 1]. In B. belone ( Fig. 18 ) and S. saurus ( Figs. 19 and ​ and20), 20 ), it branches already within the neurocranium. Afterwards, the ramus maxillaris trigemini splits into two branches. Dorsally to the posterior part of the suspensoric, the branches align laterally and medially along the course of ramus mandibularis trigemini. On the level of the jaw joint, the branches of ramus maxillaris trigemini change their course into an anterodorsad direction and enter the upper jaw. Ramus mandibularis trigemini travels anteroventrad to the lower jaw [state 2].

Ramus mandibularis facialis. The ramus mandibularis facialis branches after leaving the hyomandibular laterally to the suspensoric in order to run with two branches to the medial side of the suspensoric in At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), Ap. lineatus ( Figs. 10 and ​ and11), 11 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 0]. In Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and ​ and7), 7 ), O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), Pa. brachypterus ( Figs. 14 and ​ and15), 15 ), and D. pussila ( Figs. 16 and ​ and17) 17 ) it branches differently [state 1]. The course of that nerve could not be followed in X. oophorus ( Fig. 3 ).

Lig. premaxillo-maxilla. This ligaments spans broadly between premaxilla and maxilla in B. belone ( Fig. 18 ) and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 0] and between the proximal ends of the premaxilla and the maxilla in all other species [state 1].

Hertwig (2008) argued for the absence of the ligament in Beloniformes and mentioned an extensive area of connective tissue instead. Based on arguments of Werneburg (2013b) , I homologise this tissue with the broad ligament found in other taxa.

Primordial ligament. This ligament is present as a lig. maxillo-anguloarticulare between the maxilla and the anguloarticular in Pe. fluviatilis ( Figs. 2A and ​ and5) 5 ) and At. boyeri ( Figs. 2C , ​ ,8, 8 , ​ ,9 9 and 12D ) [state 0]. The ligament is absent in all other species [state 1].

Upper jaw/palatine ligament. A ligament, which connects the palatine and the upper jaw, is present as lig. palato-maxilla between palatine and maxilla in At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), Ap. lineatus ( Figs. 10 and ​ and11), 11 ), O. latipes ( Figs. 12A – 12C and ​ and13), 13 ), X. oophorus ( Fig. 3 ), and Pa. brachypterus ( Figs. 14 and ​ and15) 15 ) [state 0]. It is present as lig. palato-premaxilla between palatine and premaxilla in Pe. fluviatilis ( Fig. 5 ) [state 1] or is absent in R. corsula ( Figs. 6 and ​ and7), 7 ), D. pussila ( Figs. 16 and ​ and17), 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 2].

An autapomorphy in the ground pattern of Atherinomorpha may be the presence of a lig. palato-maxilla. The absence of the ligament in R. corsula ( Figs. 6 and ​ and7) 7 ) and a different attachment of the ligament in Pe. fluviatilis makes it impossible to reconstruct the ground pattern.

Lig. parasphenoido-suspensorium. This ligament is present in Pe. fluviatilis ( Fig. 5 ), At. boyeri ( Figs. 8 , ​ ,9 9 and 12D ), and S. saurus ( Figs. 19 and ​ and20) 20 ) [state 0]. It is absent in all other species [state 1].

For Pe. fluviatilis , Osse (1969) described two ligaments (his No. XVII and XVIII) that originate from the parasphenoid and insert to the dorsal edge of the suspensoric. This differentiation of the ligament could not be identified in the manual dissections performed for the present study.

Conclusions

In the present study, the variety of jaw, suspensoric, and opercle muscles was described for several acanthopterygian fishes with a focus on Beloniformes. The diversity of jaw muscles within Beloniformes corresponds to the external differences in their jaw morphology. As such, long beaked forms and species with protractible mouths show remarkable differences in their jaw musculature that may be correlated to stiffening or high mobility of the jaws.

Most important anatomical differences detected in this study exist in the external jaw musculature of Beloniformes. The jaw adductors belong to the most intensely studied muscles in vertebrates due to their prominent size and variation in the head and their importance for feeding mechanisms ( Haas, 2001 ; Diogo, 2008 ; Diogo & Abdala, 2010 ; Daza et al., 2011 ; Konstantinidis & Harris, 2011 ; Werneburg, 2013a ; Werneburg, 2013b ; Datovo & Vari, 2013 ; Datovo & Vari, 2014 ). Among Acanthopterygii, the external section of m. adductor mandibulae (A1) experienced comprehensive diversifications ( Wu & Shen, 2004 ), and among Beloniformes, it can either be present or absent.

The A1 lowers the upper jaw in most fishes. As an autapomorphy of Beloniformes, Mickoleit (2004) mentioned the reduced mobility of bones related to the upper jaw. Hertwig (2005) hypothesised that the reduced mobility of those bones might be correlated with the reduction of A1 within Beloniformes or the displacement of the A1-insertion apart from the upper jaw. In the present study, such a replacement of A1 was discovered in O. latipes ( Fig. 2E ; see also Werneburg & Hertwig, 2009 ). This species can still move its upper jaw during feeding (I Werneburg, pers. obs., 2006), which questions the possibility of a functional correlation of the character pair mentioned by Hertwig (2005) and Hertwig (2008) , namely ‘A1 no longer attached to upper jaw’ and ‘non-moveable upper jaw bones’.

Moreover, in the flying fish Pa. brachypterus , which has no A1 ( Fig. 2F ), a protrusible jaw was discovered herein. Therefore, the upper jaw bones are moveable against each other ( Figs. 14 and ​ and15 15 ).

The hemiramphid Dermogenys pusilla , which hunts at the surface of the water ( Meisner, 2001 ), is able to easily move its short upper jaw, although the species has no A1 ( Fig. 2G ). Hence, coupled by ligament attachments, the lifting of the upper jaw appears to be indirectly performed by lowering the lower jaw. A deep coupling of those structures can be hypothesised for most other A1-lacking Beloniformes. In addition, the mobility of the protrusible upper jaw of Pa. brachypterus suggests a strong ligament-bone interaction ( Figs. 14 and ​ and15 15 ).

Among hemiramphids, whose phylogenetic relationship is debated, A1 can be absent (this study: Dermogenys pussila ; Hertwig, 2008 : Hyporhamphus unifasciatus ) or can be present ( Hertwig, 2008 : Nomorhamphus sp., Hemiramphodon phaiosoma ; Rosen, 1964 : Arrhamphus brevis ). Also Exocoetidae seem to have members with an A1 ( Wu & Shen, 2004 : Cypselurus cyanopterus , Parexocoetus mento ; but see comments in the Results section) and members without an A1 (this study: Pa. brachypterus ). The phylogenetic significance of those conditions can first be adequately estimated when more species are observed and more clarity exists about phylogenetic interrelationship. But this requires further detailed and comprehensive observations.

At least for B. belone ( Fig. 2H ) and S. saurus ( Figs. 19 and ​ and20), 20 ), one may hypothesise that the loss of the A1 could be related to a strong fixation of the upper jaw to the cranium, realised by lig. premaxillo-frontale. Whether the upper jaw of both species is still moveable in vivo is not known so far, but is not expected.

As seen in hemiramphids, an elongated lower jaw not necessarily involves the reduction of A1. Xenopoecilus oophoris , an adrianichthyid with duckbill-like jaws, also has an A1 ( Fig. 3 ), which is attached to the upper jaw. This indicates that also an elongated upper jaw, which possibly was present in the ground pattern of Beloniformes already ( Parenti, 1987 ), not necessarily implies the loss of A1. Only the derived condition of two species, B. belone and S. saurus , which possess a stiffened upper jaw, may be clearly correlated to the loss of A1. As such, it can be expected that another belonid, Potamorrhamphis eigenmannii ( Miranda Ribeiro, 1915 ), which has a moveable upper jaw in vivo (I Werneburg, pers. obs., 2006), could have an A1, but this hypothesis needs further observation. The present study shows that the loss of A1 must not be interpreted only in correlation to elongated jaws. Other biomechanical requirements must be considered.

The studied selection of non-beloniform species must be handled with care when choosing them as potential outgroup species (as example see Hertwig, 2008 ). Compared to the insufficient documentation of the cranial musculature of most acathopterygian groups, the species dissected herein appear to show several derived characters. E.g., Rh. corsula has three main components of A2/3. Most mugiliform taxa, however, are reported to have a different arrangement of that muscle ( Gosline, 1993 : Agonostomus ; Van Dobben, 1935 : Mugil ; Wu & Shen, 2004 : Chelon , Crenimugil ; Starks, 1916 : Mugil ; Eaton, 1935 : Mugil ). As the authors of these studies did not observe histological sections, these findings could represent artefacts caused by the lower resolution of manual dissection.

As representative of the potential sister group to all remaining Beloniformes, the adrianichthyids Oryzias latipes and Xenopoecilus oophorus were studied herein. Hertwig (2005) , Hertwig (2008) and Werneburg & Hertwig (2009) already diagnosed several derived characters for O. latipes that could be affirmed herein and together with X. oophorus , it shares several derived characters. Due to the distinctive morphology of Adrianichthyidae, problems could arise when reconstructing the jaw muscle configuration in the ground pattern of Beloniformes. In addition to several derived characters, the taxon seems to display several plesiomorphic characters shared with Cyprinodontiformes. This finding persuaded Rosen (1964) and Li (2001) to postulate a sister group relationship of Adrianichthyidae + Cyprinodontiformes, named as Cyprinodontoidei ( Fig. 1A ). The present study highlights which characters are most variable among near related species and may assist taxon and character selection in future phylogenetic studies.

The differing external jaw morphology of diverse beloniform fishes is nicely reflected in the anatomy of their jaw musculature. Apparent changes concern the absence or presence of the A1 and arrangements of the intramandibular musculature. Both muscles are coupled to the upper or lower jaw, which are connected by ligaments themselves. The strong attachment of the upper jaw to the neurocranium, as visible in needlefishes and sauries, involves complex rearrangements of the soft tissue of the jaw apparatus.

Acknowledgments

I am grateful to Stefan T. Hertwig for discussion and advice (but I am of course responsible for any remaining mistakes). I thank Lynne Parenti, Rolf Beutel, Stefan T. Hertwig, and Manfred Schartl for kindly providing specimens. Janine M. Ziermann, Martin Fischer, Lennart Olsson, and Torsten M. Scheyer are thanked for discussion. Rommy Peterson and Katja Felbel helped with laboratory concerns. Julio Mario Hoyos, Janine M. Ziermann, Laura A.B. Wilson, and anonymous reviewers gave constructive critics to former versions of the manuscript. I am most grateful to Marcelo R. Sánchez-Villagra and Walter G. Joyce to for their generous support of my research.

Funding Statement

The author was funded by SNF Advanced Postdoc Mobility Grant P300P3_158526. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Additional Information and Declarations

The author declares there are no competing interests.

Ingmar Werneburg conceived and designed the experiments, performed the experiments, analyzed the data, wrote the paper, prepared figures and/or tables.

The following information was supplied relating to ethical approvals (i.e., approving body and any reference numbers):

No permission was required. The vertebrate animals used in this study were manually dissected. The specimens were ethanol preserved and stem from scientific collections as indicated in the methods section of the manuscript.

Morphology of the jaw, suspensorial, and opercle musculature of Beloniformes and related species (Teleostei: Acanthopterygii), with a special reference to the m. adductor mandibulae complex

The taxon Beloniformes represents a heterogeneous group of teleost fishes that show an extraordinary diversity of jaw morphology. I present new anatomical descriptions of the jaw musculature in six selected beloniforms and four closely related species. A reduction of the external jaw adductor (A1) and a changed morphology of the intramandibular musculature were found in many Beloniformes. This might be correlated with the progressively reduced mobility of the upper and lower jaw bones. The needlefishes and sauries, which are characterised by extremely elongated and stiffened jaws, show several derived characters, which in combination enable the capture of fish at high velocity. The ricefishes are characterised by several derived and many plesiomorphic characters that make broad scale comparisons difficult. Soft tissue characters are highly diverse among hemiramphids and flying fishes reflecting the uncertainty about their phylogenetic position and interrelationship. The morphological findings presented herein may help to interpret future phylogenetic analyses using cranial musculature in Beloniformes.

Introduction

The m. adductor mandibulae complex belongs to one of the most intensively studied soft tissues in vertebrates. It primarily moves the skeletal elements associated to the mandibular arch and is the main head and the most powerful feeding musculature. The m. adductor mandibulae complex is highly adapted to different feeding strategies among vertebrate clades and, as such, experienced a large amount of diversification. Its anatomy is informative for different phylogenetic levels and a mutual evolution with jaw and skull anatomy can be observed (e.g., Gosline, 1986 ; Diogo, 2008 ; Diogo & Abdala, 2010 ; Datovo & Vari, 2013 ).

Among teleost fishes, the jaw anatomy of Beloniformes, the needlefishes and their allies, is very diverse. As such, they received reasonable attention in osteological, phylogenetic as well as ontogenetic analyses Rosen & Parenti, 1981 ; Boughton, Collette & McCune, 1991 ; Lovejoy & De Araujo, 2000 ; Lovejoy, Iranpour & Collette, 2004 . The taxon includes small, short-snouted and duckbilled ricefishes (Adrianichthyidae) ( Parenti, 1987 ), which live in flooded Asian rice fields. Halfbeaks (hemiramphids), another group, are characterised by an elongated lower jaw. The flying fishes (Exocoetidae) have short snouts; whereas the sauries (Scomberesocidae) and needlefishes (Belonidae), which are adapted to fast swimming and fish hunting, have elongated upper and lower jaws with extended teeth rows ( Nelson, 2006 ). Although the drastic ontogenetic changes of the jaws have been previously studied in their external shape ( Boughton, Collette & McCune, 1991 ; Lovejoy, Iranpour & Collette, 2004 ), the anatomy of the fully formed cranial musculature has received little attention.

Beloniformes belong to the Atherinomorpha ( Fig. 1 ), which are placed within the Acanthopterygii. The phylogenetic relationships among acanthopterygian groups, which also include taxa such as Perciformes and Mugilomorpha, are controversial (e.g., Stiassny, 1990 ; Johnson & Patterson, 1993 ; Parenti, 1993 ; Parenti & Grier, 2004 ; Rosen & Parenti, 1981 ; Wu & Shen, 2004 ; Nelson, 2006 ; Setiamarga et al., 2008 ; Near et al., 2013 ). Smegmamorpha, Mugilomorpha, or Paracanthopterygii have all been hypothesised to form the sister taxon to Atherinomorpha.

Figure 1: Alternative topologies for atherinomorph interrelationship as referred in the literature.

The monophyly of Atherinomorpha is currently accepted ( Nelson, 2006 ; Near et al., 2013 ). Atheriniformes form the sister group of Cyprinodontea, which comprises Cyprinodontiformes (killifishes and their allies) and Beloniformes ( Figs. 1B – 1C ). Recently, Li (2001) analysed osteological data of the hyobranchial apparatus and re-established the traditional hypotheses of Berg (1958) and Rosen (1964) of a closer relationship of Adrianichthyidae to Cyprinodontiformes ( Fig. 1A ; see also Temminck & Schlegel, 1846 : compared to Yamamoto, 1975 ). This hypothesis, however, was not based on a cladistic analysis and represents phenetic classifications. These classifications are in strong contrast to several morphological and molecular analyses, which result in a sister group relationship of Adrianichthyidae and Exocoetoidea, comprising the remaining Beloniformes ( Fig. 1 ), and Beloniformes as the sister group of Cyprinodontiformes ( Rosen & Parenti, 1981 ; Collette et al., 1984 ; White, Lavenberg & McGowen, 1984 ; Naruse et al., 1993 ; Dyer & Chernoff, 1996 ; Naruse, 1996 ; Hertwig, 2008 ).

The phylogenetic relationships within Beloniformes are still a matter of debate. Traditional studies ( Rosen, 1964 ; Rosen & Parenti, 1981 ) found two major clades within Beloniformes (excl. Adrianichthyidae), namely Exocoetoidea (flying fishes and halfbeaks) and Scomberesocoidea (sauries and needlefishes), together forming the Exocoetoidei ( Rosen, 1964 ; Parin & Astakhov, 1982 ; Collette et al., 1984 ; Figs. 1A – 1B ).

Recently, Lovejoy (2000) and Lovejoy, Iranpour & Collette (2004) proposed the paraphyly of hemiramphids and nested Scomberesocidae inside “Belonidae” ( Fig. 1C ). The paraphyly of hemiramphids was also supported by Tibbetts (1991) and Aschliman, Tibbetts & Collette (2005) . The halfbeak Dermogenys (which is included in the present study) was found to be a member of the Zenarchopteridae, which comprise a subset of hemiramphids of the Indo-West-Pacific ( Anderson & Collette, 1991 ; Lovejoy, 2000 ; Meisner, 2001 ). Zenarchopteridae represents the sister taxon of the clade formed by needlefishes and sauries ( Lovejoy, Iranpour & Collette, 2004 ; Aschliman, Tibbetts & Collette, 2005 ). Other representatives of the traditionally recognized hemiramphids grouped with the Exocoetidae, or as the sister group to the clade Zenarchopteridae + “Belonidae” ( Fig. 1C ).

The complex jaw musculature of Beloniformes has only been studied in very few species so far, and most published descriptions of beloniform species are superficial and insufficiently illustrated, making broad scale phylogenetic comparisons impossible. That makes broad phylogenetic comparisons impossible. The aim of the present study was to illustrate and describe the morphological diversity of cranial musculature of six selected species of Beloniformes in great detail and to compare it to external jaw anatomy. By using manual dissections and histological slide sections I aim to provide a comprehensive anatomical basis for future researchers studying more species in a phylogenetic context.

In the present, purely anatomical study, the great diversity within beloniform subgroups or within non-beloniform groups could not be studied by maintaining the provided extent and detail of illustrations and descriptions. However, I present some considerations about the potential phylogenetic relevance of some characters that have to be tested in future studies. Therefore, four selected near related acanthopterygian species, which may serve as outgroup in future phylogenetic studies, are described. In addition to two atherinomorph species, I included the percomorph Perca fluviatilis , which was recently used to define the ancestral pattern of atherinomorph jaw musculature ( Hertwig, 2008 ), and the mugilomorph Rhinomugil corsula , which is possibly closer related to Atherinomorpha ( Stiassny, 1990 ; Setiamarga et al., 2008 ; Near et al., 2013 ). A preliminary character mapping is presented.

Materials and Techniques

Taxonomic sampling.

The cranial anatomy of ten acanthopterygian species was studied, including six species of Beloniformes ( Figs. 2 – 20 ). Specimens from the following collections were used: Phyletisches Museum der Friedrich Schiller Universität Jena, Germany (ISZE), Smithsonian Institution of the National Museum of Natural History Washington, USA (USNM), Naturhistorisches Museum der Burgergemeinde Bern, Switzerland (NMBE).

Perciformes, Perca fluviatilis (Linnaeus, 1758) (ISZE) ( Figs. 2A and 5 );

Mugilomorpha, Rhinomugil corsula (Hamilton, 1822) (NMBE) ( Figs. 2B , 6 and 7 );

Atheriniformes, Atherina boyeri (Risso, 1810) (NMBE) ( Figs. 2C , 8 , 9 and 12D );

Cyprinodontiformes, Aplocheilus lineatus (Valenciennes, 1846) (NMBE) ( Figs. 2D , 10 and 11 );

Beloniformes, Adrianichthyidae, Oryzias latipes ( Temminck & Schlegel, 1846 ) (NMBE) ( Figs. 2E , 12A – 12C , 13 );

Beloniformes, Adrianichthyidae, Xenopoecilus oophorus (Kottelat 1990) (NMBE) ( Fig. 3 );

Beloniformes, Exocoetidae, Parexocoetus brachypterus (Richardson, 1846) (USNM 299385) ( Figs. 2F , 14 and 15 );

Beloniformes, Hemiramphidae, Dermogenys pusilla (Kuhl and Van Hasselt, 1823) (NMBE) ( Figs. 2G , 16 and 17 );

Beloniformes, Belonidae, Belone belone (Linnaeus, 1761) (NMBE) ( Figs. 2H and 18 );

Beloniformes, Scomberesocidae, Scomberesox saurus (Walbaum, 1782) (ISZE) ( Figs. 19 and 20 ).

Figure 2: Overview on the cranial anatomy in the eight species manually dissected in this study.

Figure 3: The duckbilled ricefish Xenopoecilus oophorus (Beloniformes, Adrianichthyidae).

Figure 4: Phylogenetic framework.

Figure 5: Perca fluviatilis .

Figure 6: Rhinomugil corsula .

Figure 7: Rhinomugil corsula .

Figure 8: Atherina boyeri .

Figure 9: Atherina boyeri .

Figure 10: Aplocheilus lineatus.

Figure 11: Aplocheilus lineatus.

Figure 12: Manual dissections.

Figure 13: Oryzias latipes .

Figure 14: Parexocoetus lineatus .

Figure 15: Parexocoetus lineatus.

Figure 16: Dermogenys pussila .

Figure 17: Dermogenys pussila.

Figure 18: Belone belone .

Figure 19: Scomberesox saurus .

Figure 20: Scomberesox saurus .

For a phylogenetic analysis, published information on further beloniform, namely hemiramphid species, Hyporhamphus unifasciatus (Ranzani, 1841), Nomorhamphus sp. aff. ravnaki (Brembach, 1991), and Hemirhamphodon phaiosoma (Bleeker, 1852), were included ( Table 1 , Fig. 4 ). According to the new findings of Werneburg & Hertwig (2009) , the data on O. latipes were modified when compared to Hertwig (2005) , Hertwig (2008) and Werneburg (2007) .

not applicable

Anatomical observations

Standard procedures for histology and manual dissection are those used by Werneburg (2007) and Werneburg & Hertwig (2009) .

For dissection, two or more specimens per species were used. In the first step of dissection (summarised in Fig. 2 ) the lateral view of the skinned head including all muscles in their unaltered place, including the jaw adductor musculature, opercle-, and suspensoric-related musculature, was documented. In the second step, the external section of m. adductor mandibulae (A1) was mostly removed and the course of the internal section of m. adductor mandibulae (A2/3) was depicted. Further steps of dissection did allow inspection of the symplectic in lateral view with the A2/3 completely or partly removed. Finally, the medial view of the jaw apparatus was documented with a focus on the musculature medial of the lower jaw, namely the intramandibular section of m. adductor mandibulae ( Aω ), the anterior part of m. protractor hyoidei, and m. intermandibularis.

Serial sections were prepared for all species (slice thickness = 12 µm), except for Pe. fluviatilis and B. belone due to the size of these species. The positions of the sections are indicated in the dissection figures ( Figs. 6 , 8 , 10 , 12 , 14 , 16 and 19 ). For S. saurus , a juvenile specimen was used for histological sectioning ( Fig. 20 ), whereas for manual dissections and character coding (as for all species), adult specimens were used ( Fig. 20 ).

Nomenclature

Osteological nomenclature follows Weitzman (1962) and Weitzman (1974) with modifications as summarised by Hertwig (2008) . Basic myological terminology is that of Werneburg (2011) . Fish muscle nomenclature mainly corresponds to that of Winterbottom (1974) . The homologisation of particular muscular portions follows Werneburg & Hertwig (2009) . The nomenclature of the nervous system refers to Holje, Hildebrand & Fried (1986) . For osteological and, if available, for myological comparisons, I relied on Osse (1969) for Perciformes; on Thomson (1954) for Mugilomorpha; on Kulkarni (1948) , Rosen (1964) , Karrer (1967) , Hertwig (2005) and Hertwig (2008) for Adrianichthyidae and Cyprinodontiformes; on Clemen, Wanninger & Greven (1997) , Greven, Wanninger & Clemen (1997) , Meisner (2001) , and Shakhovskoi (2002) for hemiramphids; on Khachaturov (1983) and Shakhovskoi (2004) for Exocoetidae; and on Chapman (1943) for Scomberesocidae.

Character evolution

Using PAUP* ( Swofford, 2003 ), a character mapping was performed. Therefore, the topology of Lovejoy, Iranpour & Collette (2004) was used as template to arrange the phylogeny of the beloniform species studied herein and of three additional hemiramphid species ( Fig. 4 ; cf. Fig. 1C ). For the interrelationship of major acanthopterygian groups, the present study follows the findings of Stiassny (1990) , Setiamarga et al. (2008) , and Near et al. (2013) . Therein, Percomorpha form the sister taxon to Ovalentaria. Consequently a polarisation of characters is given. The topology for the character mapping was drawn using the move branch function in Mesquite 2.01 ( Maddison & Maddison, 2011 ).

Results and Discussion

Characters and character mapping.

In total, 37 soft tissue characters are described and discussed below. The character matrix can be found in Table 1 . The results of the character mapping are listed in Table 2 . Therein, the consensus of Acctran and Deltran optimizations are documented. Due to the particular focus on the morphological descriptions and illustration of this study, the taxonomic sampling is limited. Also the available data from the literature record is limited. As such, I avoid discussing the character changes in detail. They should serve as summary of character distribution of the species studied herein. The phylogenetic relevance of the characters should be subject of evaluation and discussion in future, more quantitative analyses of the cranial musculature of Beloniformes. Those studies may also consider more closely related species for the comparison with Atherinomorpha.

direction of character change from taxon 1 to taxon 2

unambiguous character change

ambiguous character change

External section of the m. adductor mandibulae complex (A1)

The m. adductor mandibulae is differentiated into different muscle sections in teleost fishes, representing a complex of individual muscles, each having a separated origin, course, and insertion ( Diogo, 2008 ; Diogo & Abdala, 2010 ). The external section of m. adductor mandibulae complex, A1, is the lateral-most jaw muscle. If present, it originates posteriorly on the suspensorium and/or on the preopercle, it runs rostrad, and has a tendinous insertion to the upper or lower jaw (i.e., Allis, 1897 ).

General appearance. An A1 is present in Perca fluviatilis ( Figs. 2A and 5 ), Rhinomugil corsula ( Figs. 2B , 6 and 7 ), Atherina boyeri ( Figs. 2C , 8 , 9 and 12D ), Aplocheilus lineatus ( Figs. 2D , 10 and 11 ), Oryzias latipes ( Figs. 2E , 12A – 12C and 13 ), and Xenopoecilus oophorus ( Fig. 3 ) [character state 0] but is absent in all other species studied herein, namely Dermogenys pussila , Parexocoetus brachypterus , Belone belone , and Scomberesox saurus [state 1].

In O. latipes , Hertwig (2008) and Werneburg & Hertwig (2009) described a lateral muscle of the adductor complex with an insertion to the lower jaw. It could be interpreted in two different ways: First, it could represent A1, the possession of which is plesiomorphic; A1 is present in all non-beloniform fishes studied and in O. latipes , it autapomorphically would have shifted its insertion to the lower jaw. Second, A1 could be reduced in O. latipes ( Hertwig, 2005 ). In that case, one additional step of transformation would be needed, as the internal section of m. adductor mandibulae (A2/3) would be modified secondarily. Hertwig (2005) followed the principle of parsimony and opted for the first explanation. Werneburg (2007) interpreted an insertion of A1 to the maxilla and homologised the muscle to the A1 of the outgroup representatives. After reanalysing, this finding was revised and A1 actually inserts on the posterior edge of the dentary at two-thirds of its height below the coronoid process of this bone and has contact via connective tissue to the lig. maxillo-mandibulare in this species ( Werneburg & Hertwig, 2009 ). Previously, the latter connection was misinterpreted as an upper jaw insertion ( Werneburg, 2007 ).

Wu & Shen (2004) mentioned a small ventrolateral portion of A1, their A1-VL, in two flying fish species. As Hertwig ( 2005 : 39) already pointed out, the homologisations of those authors remain unclear. Moreover, the illustration of that portion is lacking. It appears that Wu & Shen (2004) may have confused this portion with the lateral subdivision of A2/3. Hertwig ( 2008 , 149) wrote: ‘In an extensive comparative study of the m. adductor mandibulae in teleostean fishes, [the authors], however, did not mention a subdivision of A2/3 either in the Mugilomorpha or in the Atherinomorpha, but this is probably down to their limited taxon sample, which comprised only three species of the latter.’ If Wu & Shen (2004) actually identified the remainder of A1 as their A1-VL (supported by the fact that an insertion of A1-VL to the maxilla is present), a high interspecific variability may be hypothesised for the flying fishes.

Starks (1916) dissected a belonid species, Tylosurus acus , in which he described an A1-muscle. Following the present homologisation, however, that muscle clearly represents the lateral head of the muscle A2/3, which has a similar anatomy as found in B. belone (see also below) and S. saurus ( Figs. 2H and 18 – 20 ).

Orientation. The spatial orientation of A1 to the more medial, internal section of m. adductor mandibulae (A2/3) is different among species. In R. corsula ( Figs. 2B , 6 and 7 ), the A1 is situated ventrolaterally to the lateral head of A2/3 and three-fourths of this head are still visible in lateral view [state 0]. In Pe. fluviatilis , the muscle is situated dorsolateral to the internal section and the complete lateral head (A2/3, lateral) is not covered in lateral view ( Figs. 2A and 5 ) [state 1]. A1 is situated completely lateral to the intermedial head of the internal section of m. adductor mandibulae (A2/3, intermedial) in Ap. lineatus ( Figs. 2D , 10 and 11 ), O. latipes ( Figs. 2E , 12A – 12C and 13 ; see also Werneburg & Hertwig, 2009 ), and X. oophorus ( Fig. 3 ) and the lateral head (A2/3, lateral) is only covered in its anterior region [2(2)]. Laterally in At. boyeri ( Figs. 2C , 8 , 9 and 12D ), the A1 completely covers the internal section of m. adductor mandibulae (A2/3) [state 3].

For the ground pattern of Atherinomorpha, Hertwig (2005) proposed that the external (A1) and internal (A2/3) sections are situated next to each other in a horizontal plane. As an outgroup of Atherinomorpha, the author used Pe. fluviatilis , in which the A2/3-portions are situated above each other in a horizontal plane ( Figs. 2A and 5 ). In the present study, R. corsula was dissected as an additional, potential outgroup species, which is closely related to Atherinomorpha. Similar to Atherinomorpha ( sensu Hertwig, 2008 ), the A1 of that species also has to be interpreted to be lateral to the A2/3 in a horizontal plane. As such, that character has to be withdrawn as an autapomorphy of Atherinomorpha. More detailed observation among Percomorpha could identify the orientation of A1 to A2/3 in Pe. fluviatilis ( Figs. 2A and 5 ) as autapomorphy of Percomorpha or only of that species. In the latter case, the ‘A1 in horizontal plane to A2/3’ would need to be interpreted as plesiomorphic among Acanthopterygii. Observations among Mugilomorpha could identify the orientation of A1–A2/3 as a homoplastic character of R. corsula and Atherinomorpha. If all members of Mugilomorpha had an A1 lateral to A2/3, and when following the phylogenetic hypothesis of Stiassny (1990) , that spatial orientation would need to be interpreted as a synapomorphy of Mugilomorpha + Atherinomorpha.

Insertion. The tendon of A1 inserts on the lateral face of the anterior part of the maxilla in Pe. fluviatilis ( Figs. 2A and 5 ) [state 0], to the medial face of the middle region of the maxilla in R. corsula ( Figs. 2B , 6 and 7 ) and X. oophorus ( Fig. 3 ) [state 1], and to the posterior edge of the dentary in O. latipes ( Figs. 2E , 12A – 12C and 13 ) [state 2]. With three tendons, A1 inserts on the processus primordialis (anguloarticularis), to the medial side of the lacrimal, and medially to the anterodorsal tip of the maxilla in At. boyeri ( Figs. 2C , 8 , 9 and 12D ) [state 3]. The A1 inserts with two tendons to the lateral face of the medial part of the maxilla and to the medial face of the lacrimal in Ap. lineatus ( Figs. 2D , 10 and 11 ) [state 4].

The insertion of A1 to the jaws is different in all species studied. A definition of homology (e.g., A1 inserts laterally to the maxilla) was not made, because the differences of A1 were too large. Hertwig (2008) observed several atherinomorph species and defined the insertion of A1 at the lateral face of the maxilla to be present in Pe. fluviatilis and “Aplocheilidae”. In contrast to Pe. fluviatilis ( Figs. 2A and 5 ), however, the A1 inserts on the other end of the maxilla in Ap. lineatus ( Figs. 2D , 10 and 11 ). The latter species has an additional tendon to the medial face of the lacrimal, a character which was found by Hertwig (2008) to be present in the ground pattern of Atherinomorpha (compare to Alexander, 1967 ; Parenti, 1993 ; Stiassny, 1990 ). For Cyprinodontiformes (incl. Aplocheilus ), Hertwig (2005) was not able to define an unambiguous constellation of the insertion of A1. However, he argued that the insertion of A1 shifted based on the rotation of the maxilla in this taxon. As such, the insertion of A1 to the lateral face of the maxilla could be interpreted as being plesiomorphic among Atherinomorpha.

Internal section of the m. adductor mandibulae complex (A2/3)

The A2/3 usually originates with two or three muscle heads on the suspensoric and on the preopercle and inserts as a consistent muscle to the lower jaw. Muscle heads are defined as partial differentiations of a muscle. They have separated origins or insertions ( Werneburg, 2007 ; Werneburg, 2011 ). Muscle heads gain a descriptive nomenclature herein; their position of origin (or insertion) and the spatial orientation were considered. This nomenclature differs from Winterbottom (1974) , because that one is not applicable for muscle heads herein.

A2/3 can have an intramandibular portion. A muscle portion is defined as having a separate origin, course, and insertion, but as having some intertwining fibres or a shared tendon with another muscle portion of the same ontogenetic and/or phylogenetic origin ( Werneburg, 2007 ; Werneburg, 2011 ).

Origin. In Pe. fluviatilis ( Figs. 2A and 5 ), Pa. brachypterus ( Figs. 2F , 14 and 15 ), and D. pussila ( Figs. 2G , 16 and 17 ), the A2/3 has two muscle heads (A2/3, lateral; A2/3, medial) in its origin [state 0]. A2/3 originates with three muscle heads (A2/3, lateral; A2/3, medial; A2/3, intermedial) in R. corsula ( Figs. 2B , 6 and 7 ), Ap. lineatus ( Figs. 2D , 10 and 11 ), O. latipes ( Figs. 2E , 12A – 12C and 13 ), X. oophorus ( Fig. 3 ), B. belone ( Figs. 2H and 18 ), and S. saurus ( Figs. 19 and 20 ) [state 1].

The cyprinodontiform species Ap. lineatus ( Figs. 10 and 11 ) was found to have three muscle heads at its origin. This corresponds to the findings of Hertwig (2008) . To confirm his findings, Hertwig (2008) used histological sections, which permit a much higher accuracy when distinguishing between minute muscle heads. I have seen many of the sections and used some herein, and can confirm his observations.

Jourdain (1878) described a specimen of B. belone (“ vulgaris ”), in which A2/3 was not separated. I dissected several specimens of that species and always found a separation, although I have to note that the differentiation of the lateral and the medial head were difficult. Also, apparently, Jourdain (1878) did not remove the lateral head of A2/3 as he expected A2/3 to represent an undifferentiated muscle mass and hence did not discover the intermedial head of A2/3.

The lateral head. The lateral head of A2/3 originates almost overall at the vertical aspect of preopercle, at the posterior part of the horizontal aspect of the preopercle, as well as on the processus lateralis hyomandibularis in R. corsula ( Figs. 2B , 6 and 7 ), Ap. lineatus ( Figs. 2D , 10 and 11 ), B. belone ( Figs. 2H and 18 ), and S. saurus ( Figs. 19 and 20 ) [state 0]. It originates at the vertical aspect of the preopercle (but does not reach its dorsal most tip) and at more than half of the horizontal aspect of the preopercle in D. pussila ( Figs. 2G , 16 and 17 ) [state 1]. In Pe. fluviatilis ( Figs. 3A and 5 ) and Pa. brachypterus ( Figs. 2F , 14 and 15 ), the lateral head originates ventrally at the processus lateralis hyomandibularis, at the ventral third of the vertical aspect of the preopercle, as well as on the processus caudalis quadrati [state 2]. With a narrow attachment, it only originates on the ventral third of the vertical aspect of the preopercle in O. latipes ( Figs. 2E , 12A – 12C and 13 ) and X. oophorus ( Fig. 3 ) [state 3].

Medial head. In Pe. fluviatilis , the medial head of A2/3 originates from the hyomandibular, the metapterygoid, and the symplectic, as well as from processus lateralis hyomandibularis ( Fig. 5 ) [state 0]. It originates from the hyomandibular and from the metapterygoid in R. corsula ( Figs. 6 and 7 ) [state 1] or only from the metapterygoid in Ap. lineatus ( Figs. 10 and 11 ) and Pa. brachypterus ( Figs. 2F , 14 and 15 ) [state 2]. It arises from the lateral faces of the quadrate, the symplectic, and the cartilaginous interspaces of the hyopalatine arch, and from the tendon of the m. adductor arcus palatini quadrati in O. latipes ( Figs. 12A – 12C and 13 ) and X. oophorus ( Fig. 3 ) [state 3]. The medial head of A2/3 originates ventrally at the sphenotic, laterally at the hyomandibular, and dorsally at the metapterygoid in D. pussila ( Figs. 16 and 17 ), B. belone ( Figs. 2H and 18 ), and S. saurus ( Figs. 19 and 20 ) [state 4].

Similar to the present study, Hertwig (2005) and Hertwig (2008) found the origin of the medial head of A2/3 to be highly variable. In addition to an adult specimen of S. saurus , a juvenile was studied ( Figs. 9E – 9H ). In this specimen, a different orientation of the A2/3-heads was found ( Werneburg, 2007 ). One could hypothesise that the medial head of A2/3 in the juvenile shifts its origin to a dorsal position and the intermedial head of A2/3 could shift its origin to a more ventral position (two transformation steps). Alternatively, the origin of the medial A2/3-head of the juvenile could shift ventrolaterally to the intermedial head of A2/3 and would be homologous to the intermedial head of A2/3 in the adult. Hence, the intermedial head of A2/3 in the juvenile (then the medial head of the adult) would keep its origin at the sphenotic (one transformation step). Those scenarios are very speculative because they are derived from only one observation. No final answer can be presented, because the variability of that character within S. saurus cannot be estimated. The species D. pussila , B. belone , and S. saurus show a very drastic ontogenetic elongation of the lower jaw (Hemiramphidae) or of both jaws (Belonidae, Scomberesocidae) ( Boughton, Collette & McCune, 1991 ; Lovejoy, 2000 ; Lovejoy, Iranpour & Collette, 2004 ). It would be valuable to study if, correlated to the elongation of jaws, changes in the anatomy of the jaw musculature occur (origin, volume, course, insertion). Comparative ontogenetic and electromyographic studies ( Focant, Jacob & Huriaux, 1981 ; Osse, 1969 ) could help to interpret the specific case mentioned herein. Ontogenetic changes in the anatomy of the jaw musculature were already observed by Hertwig (2005) in representatives of Goodeidae (Cyprinodontiformes: Crenichthys ). Nanichthys (Scomberesocidae) is often not accepted as a ‘genus’ in a taxonomic sense and is often referred to as a dwarf morphotype of Scomberesox ( Collette, 2004 ; Collette et al., 1984 ). However, if the juvenile specimen of S. saurus studied herein would actually represent a member of a valid genus Nanichthys , the arrangement of the A2/3-musculature may serve as a criterion to distinguish both species taxonomically.

Intermedial head. The intermedial head of A2/3 is situated between the lateral and the medial head. It originates only on the horizontal aspect of the preopercular in R. corsula ( Figs. 6 and 7 ) [state 0]. It takes its origin from the horizontal aspect of the preopercle and at the processus caudalis quadrati in Ap. lineatus ( Figs. 10 and 11 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ) [state 1] and originates only on the processus caudalis quadrati in O. latipes ( Figs. 12A – 12C and 13 ) and X. oophorus ( Fig. 3 ) [state 2]. An intermedial head is not present in Pe. fluviatilis , At. boyeri , Pa. brachypterus , and D. pussila .

Muscle portions. Unlike in all other species [state 0], A2/3 is laterally separated into two portions (by definition; see above and Werneburg, 2011 ) in At. boyeri ( Figs. 8 , 9 and 12D ) [state 1]. The muscle portions of A2/3 have separated origins lateral at the posterior part of the suspensoric as well as separated insertions medial to the lower jaw. The medial portion of A2/3 is differentiated into two heads at its origin. The lateral portion of its A2/3 is not separated into heads. Among the species studied herein, and indeed, considering data from Hertwig (2008) regarding several other atherinid species, this condition has to be declared autapomorphic for At. boyeri (Atheriniformes).

Orientation of muscle heads. The spatial orientations of the medial and the lateral head of A2/3 are different among species. In Pe. fluviatilis ( Figs. 2A and 5 ), Ap. lineatus ( Figs. 10 and 11 ), D. pussila ( Figs. 2G , 16 and 17 ), X. oophorus ( Fig. 3 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ), the medial head of A2/3 is situated dorsally to the lateral head or is at least clearly visible in lateral view [state 0]. The medial head of A2/3 is situated ventrally to the lateral head in At. boyeri ( Figs. 8 , 9 and 12D ) [state 1]. The lateral head is situated laterally to the medial head and can cover it completely in R. corsula ( Figs. 6 and 7 ), O. latipes ( Figs. 12A – 12C and 13 ), and Pa. brachypterus ( Figs. 2F , 14 and 15 ) [state 2].

Relative size of muscle heads. The medial and the lateral heads of A2/3 have about the same size in Pe. fluviatilis ( Fig. 5 ) and D. pussila ( Figs. 16 and 17 ) [state 0]. The medial head is relatively narrow when compared to the lateral head in Pa. brachypterus ( Figs. 14 and 15 ) [state 1]. The lateral head is quite widespread when compared to the medial head in R. corsula ( Figs. 6 and 7 ) and Ap. lineatus ( Figs. 10 and 11 ) [state 2]. The medial head is larger than the lateral head in O. latipes ( Figs. 2E , 12A – 12C and 13 ), X. oophorus ( Fig. 3 ), B. belone ( Figs. 2H and 18 ), and S. saurus ( Figs. 19 and 20 ) [state 3].

Insertion. Except for B. belone ( Figs. 2H and 18 ) and S. saurus ( Figs. 19 and 20 ), A2/3 only inserts on the medial side of the lower jaw [state 0]. In the former species, it also inserts on the coronomeckelian bone [state 1], which is only found in these two species. It represents a bone, which is posterodorsally fused with the border of processus primordialis anguloarticularis. Both bones are separated from each other by a clear suture ( Werneburg, 2007 ).

Intramandibular portion. An intramandibular portion of A2/3 is lacking in all Beloniformes [state 0]. It is present in R. corsula ( Figs. 6 and 7 ) and has a narrow insertion on the medial face of processus coronoideus dentalis [state 1]. In Ap. lineatus ( Figs. 10 and 11 ), it has broad insertions to the processus coronoideus dentalis, to cartilago Meckeli, and to the anguloarticular [state 2]. It inserts medially to the dentary in At. boyeri ( Figs. 8 , 9 and 12D ) [state 3] and has a narrow insertion medially to the anguloarticular in Pe. fluviatilis ( Fig. 5 ) [state 4].

The configuration of the intramandibular portion of A2/3 is different among non-beloniforms species studied here. As the criterion of homology, the intramandibular portion is defined to originate from an A2/3-associated aponeurosis or tendon herein. Hertwig (2008) , who observed few species of Beloniformes ( O. latipes and some hemiramphids), argued for an autapomorphic reduction of an intramandibular portion of A2/3 within Beloniformes, which I can confirm herein.

Intramandibular muscles possibly act in positioning the jaw ( Karrer, 1967 : “Stellbewegung”). Hertwig (2005) and Hertwig (2008) mentioned the reduction of intramandibular muscles and found a correlation between the loss of those muscles and a reduced mobility of particular bone elements. For Empetrichthys latos (Cyprinodontiformes), he noticed an ontogenetic reduction of intramandibular muscles. The movement of upper jaw bones in Beloniformes may be coupled to the movement of the lower jaw (see above) and hence they may underlie large mechanical stresses in fish hunting species. To withstand those forces, the bones of the lower jaw may have a higher degree of fusion resulting in the tendency to reduce intramandibular musculature.

Like Hertwig (2008) , I defined an intramandibular portion of A2/3 as present in Pe. fluviatilis . However, the configuration of the intramandibular musculature of Pe. fluviatilis could be interpreted differently. In the present study, two intramandibular muscles were differentiated. First, an intramandibular portion of A2/3 is described as originating from the tendon of A2/3 by only a few muscle fibres. It narrowly inserts on the medial face of the anguloarticulare. Second, an intramandibular m. adductor mandibulae ( Aω ) is described, which is tendinously originating from the preopercular and the quadrate. That muscle has a flat insertion medially to the dentary, to cartilago Meckeli, and to the anguloarticular.

In contrast, Osse (1969) only described one intramandibular muscle for Pe. fluviatilis . That muscle, “ Aω ” in Osse (1969) , has one origin at the tendon of A2/3. This “ Aω ” also has a narrow attachment to the anguloarticular, one tendinous attachment to the prearticular/quadrate and one flat insertion to the medial face of the lower jaw. Osse (1969) combined the Aω and the intramandibular portion of A2/3 of the present study as his “ Aω .” Therefore, he did not differentiate the course of muscle fibres and other associated structures. The fibres of the intramandibular portion of A2/3 of the present study run anteroventrad. The fibres of the Aω were found to originate as a double fibred muscle from the tendon originating from the prearticular/quadrate. However, some fibres also originate from the tendon of A2/3, which is only partly fused with the tendon of Aω . While both tendons fuse, the course of the Aω -tendon is still separable ( Fig. 5D ). The fusion of the tendons and the origin of some Aω -fibres at the A2/3-tendon may have persuaded Osse (1969) to define only one intramandibular muscle.

One additional interpretation of intramandibular muscle configuration is possible. If a tendinous insertion of A2/3 to the tendon of Aω is hypothesised, the origin of some Aω -fibres may have been shifted to the tendon of A2/3. In that case, no intramandibular portion of A2/3 would exist in Pe. fluviatilis . If this configuration is a plesiomorphic condition of Acanthopterygii, the character should also be interpreted as a reversal within Beloniformes. In contrast, if one hypothesises the intramandibular portion of A2/3 to be independently reduced in Pe. fluviatilis , the character should be considered as homoplastic in Pe. fluviatilis (Percomorpha) and Beloniformes. To clarify that controversy, additional species of Percomorpha and Acanthopterygii need to be observed in great detail, but this was outside the scope of the present study.

Intramandibular section of the m. adductor mandibulae complex ( Aω )

The intramandibular section of the m. adductor mandibulae complex ( Aω ) connects the suspensoric with the medial face of the lower jaw.

Origin. It originates with a tendon anteriorly at the medial face of the symplectic in Pa. brachypterus ( Figs. 14 and 15 ) and D. pussila ( Figs. 16 and 17 ) [state 0]. It originates directly at the ventral and the anterior edge of the quadrate in O. latipes ( Figs. 12A – 12C and 13 ) [state 1]. In R. corsula ( Figs. 6 and 7 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ), Aω originates broadly on the medial face of the quadrate and a part of the muscle can have a tendinous origin [state 2]. It attaches with a tendon anteroventrally to the medial face of the quadrate in At. boyeri ( Figs. 8 , 9 and 12D ) and Ap. lineatus ( Figs. 10 and 11 ) [state 3]; and in Pe. fluviatilis ( Fig. 5 ), it originates with a tendon anteriorly at the medial face of the horizontal aspect of the preopercular and to a small amount medially at the middle area of processus caudalis quadrati [state 4]. The Aω is absent in X. oophorus [state 5].

Hertwig (2005) defined as a common character of hemiramphids: The origin of the flat tendon of Aω is situated at a part of the symplectic, which points rostrad. He studied species of Hyporhamphus , Nomorhamphus , and Hemiramphodon . Due to the diverging observation in D. pussila herein ( Figs. 16 and 17 ), this character on the origin of Aω cannot be confirmed to be diagnostic for all hemiramphids. However, as that character was also found in Pa. brachypterus ( Figs. 14 and 15 ), a potential synapomorphic character of (Exocoetidae + Hemiramphidae) is identified and a possible monophyly of Hemiramphidae could be indicated ( Rosen, 1964 ; Rosen & Parenti, 1981 ; Collette et al., 1984 ). This would contradict the works of Lovejoy, Iranpour & Collette (2004) and Aschliman, Tibbetts & Collette (2005) , who found “Hemiramphidae” paraphyletic. In the work of Lovejoy, Iranpour & Collette (2004) , the Zenarchopteridae (among others Dermogenys , Hemiramphodon , Nomorhamphus ) oppose the paraphyletic “Belonidae” (incl. Scomberesocidae) and Hyporhamphus belongs to a group, which opposes (Zenarchopteridae + “Belonidae”). Several species of “Hemiramphidae” that are closely related to Exocoetidae in the work of Lovejoy, Iranpour & Collette (2004) , as well as several other species of the remaining groups of Beloniformes need to be observed to gain a better understanding on how that character is distributed. The absence of Aω was documented for some atherinomorph species by Hertwig (2008) and the reduction must have occurred several times independently.

Shape. In R. corsula ( Figs. 6 and 7 ), Aω is separated into two heads at the level of the quadrate. The lateral head inserts broadly to the medial face of the dentary and cartilago Meckeli. The medial head of Aω inserts ventrally to the medial face of the dentary and anteriorly to the medial face of the anguloarticular [state 0]. The Aω represents a double-feathered muscle in Pe. fluviatilis ( Fig. 5 ), At. boyeri ( Figs. 8 , 9 and 12D ), D. pussila ( Figs. 16 and 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ), in which one of the muscle parts may project to a far caudad direction [state 1]. The Aω is a parallel fibred muscle in O. latipes ( Figs. 12A – 12C and 13 ) and Pa. brachypterus ( Figs. 14 and 15 ) [state 2] and a simple feathered muscle in Ap. lineatus ( Figs. 10 and 11 ) [state 3].

Insertion. On the medial face of the lower jaw, the Aω (when not differentiated into heads) inserts broadly to the dentary, cartilago Meckeli and/or to the anguloarticular in Pe. fluviatilis ( Fig. 5 ), At. boyeri ( Figs. 8 , 9 and 12D ), Pa. brachypterus ( Figs. 14 and 15 ), and D. pussila ( Figs. 16 and 17 ) [state 0]. It inserts broadly to the dentary, to the anguloarticular, and to the cartilago Meckeli, whereby a ventral part in feathered muscles inserts far anteriorly to the medial face of the dentary in B. belone ( Fig. 18 ) and S. saurus ( Figs. 19 and 20 ) [state 1]. It inserts to the ventral part of the dentary in Ap. lineatus ( Figs. 10 and 11 ) [state 2] and posteriorly to the dentary and medially at the cartilago Meckeli in O. latipes ( Figs. 12A – 12C and 13 ) [state 3].

Hertwig (2005) and Hertwig (2008) has shown that the configuration of Aω is highly variable among Cyprinodontiformes. In comparison, this can also be concluded for the species observed herein.

M. intermandibularis

Cross section. M. intermandibularis connects the contralateral dentaries at their medial faces. The cross-section of m. intermandibularis is +/− round in At. boyeri ( Figs. 8 , 9 and 12D ) [state 0]. It is big-bellied oval in Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and 7 ), O. latipes ( Figs. 12A – 12C and 13 ), and X. oophorus ( Fig. 3 ); i.e., it is at its maximum twice as broad as high [state 1]. It is elongated oval in Ap. lineatus ( Figs. 10 and 11 ), Pa. brachypterus ( Figs. 14 and 15 ), D. pussila ( Figs. 16 and 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ); i.e., it is (mostly much) more than twice as broad as high [state 2].

In each species studied, several specimens were observed and a tendency of a rounder cross-section of the muscle was found in At. boyeri ( Figs. 8 , 9 and 12D ). In addition, the assignment to big-bellied or elongated oval has to be understood as a tendency in the variability of the specimens observed.

Shape. The m. intermandibularis is parallel fibred and has no tendinous origin at the dentary in Pe. fluviatilis ( Fig. 5 ), At. boyeri ( Figs. 8 , 9 and 12D ), Pa. brachypterus ( Figs. 14 and 15 ), D. pussila ( Figs. 16 and 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ) [state 0]. However, it is spindle-shaped and has a tendinous origin at the dentary in R. corsula ( Figs. 6 and 7 ), Ap. lineatus ( Figs. 10 and 11 ), O. latipes ( Figs. 12A – 12C and 13 ), and X. oophorus ( Fig. 3 ) [state 1].

M. protractor hyoidei

Origin. The m. protractor hyoidei connects the branchial apparatus with the lower jaw. It originates laterally at the ceratohyal in Pe. fluviatilis ( Fig. 5 ), Pa. brachypterus ( Figs. 14 and 15 ), and D. pussila ( Figs. 16 and 17 ) [state 0], with two heads ventrally and laterally at the ceratohyal and at the anterior tips of the branchiostegal rays in O. latipes ( Figs. 12A – 12C and 13 ) [state 1], ventrally to the ceratohyal in R. corsula ( Figs. 6 and 7 ), At. boyeri ( Figs. 8 , 9 and 12D ), Ap. lineatus ( Figs. 10 and 11 ), and X. oophorus ( Fig. 3 ) [state 2] and medially to the ceratohyal in B. belone ( Fig. 18 ) and S. saurus ( Figs. 19 and 20 ) [state 3].

Course. A fusion with the contralateral m. protractor hyoidei occurs at the level of the jaws or suspensoric and united, they travel rostrad in R. corsula ( Figs. 6 and 7 ), Ap. lineatus , O. latipes ( Figs. 12A – 12C and 13 ), X. oophorus ( Fig. 3 ) (in relation to the jaw joint, the protractor fuses more anteriorly in X. oophorus when compared to O. latipes ), Pa. brachypterus ( Figs. 14 and 15 ), and D. pussila ( Figs. 16 and 17 ) and anteroventrally at the fused mm. protractor hyoidei a tendon can be formed on each side [state 0]. Such a fusion does not occur in Pe. fluviatilis ( Fig. 5 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ) [state 1]. In At. boyeri ( Figs. 8 , 9 and 12D ), at the level of the anguloarticular, the muscles fuse only in their ventral regions; they separate on the level of the dentary in order to insert independently of the contralateral muscle to the dentary [state 2].

Anterior part. When reaching m. intermandibularis, m. protractor hyoidei has a flat shape in Ap. lineatus ( Figs. 10 and 11 ), O. latipes ( Figs. 12A – 12C and 13 ), and X. oophorus ( Fig. 3 ) [state 0], or it is about as broad as high in Pe. fluviatilis ( Fig. 5 ), At. boyeri ( Figs. 8 , 9 and 12D ), Pa. brachypterus ( Figs. 14 and 15 ), D. pussila ( Figs. 16 and 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ) [state 1]. At this level, m. protractor hyoidei already differentiated into two heads. The dorsal head is flat and the ventral head is as high as broad in R. corsula ( Figs. 6 and 7 ) [state 2].

When reaching the dentary, the flat shape of the muscle in Ap. lineatus ( Figs. 10 and 11 ) and O. latipes could be hypothesized as being an autapomorphic character of Cyprinodontoidei sensu Rosen (1964) ( Fig. 1A ).

Insertion. M. protractor hyoidei inserts dorsally to the insertion of m. intermandibularis at the dentary and covers at least the posterodorsal area of the latter muscle in Ap. lineatus ( Figs. 10 and 11 ), Pa. brachypterus ( Figs. 14 and 15 ), and S. saurus ( Figs. 19 and 20 ) [state 0]. In Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and 7 ), O. latipes ( Figs. 12A – 12C and 13 ), D. pussila ( Figs. 16 and 17 ), and B. belone ( Fig. 18 ), it inserts ventrally to the m. intermandibularis at the dentary [state 1]. It inserts dorsally as well as ventrally of m. intermandibularis to the dentary in X. oophorus ( Fig. 3 ) [state 2].

Insertion tendon. The ventral part of m. protractor hyoidei extends into a long tendon, which reaches the anterior tip of the lower jaw in D. pussila ( Figs. 16 and 17 ) and B. belone ( Fig. 18 ) [state 0]. It does not extend into a long tendon to reach the anterior tip of the lower jaw in Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and 7 ), At. boyeri ( Figs. 8 , 9 and 12D ), O. latipes ( Figs. 12A – 12C and 13 ), and X. oophorus ( Fig. 3 ) [state 1].

The anteroventral elongation of musculature in the region of the dentary seems to be associated with the elongated lower jaw within Beloniformes. In D. pussila ( Figs. 16 and 17 ) and B. belone ( Fig. 18 ), also a ventral insertion of m. adductor mandibulae ( Aω ) to the anterior tip of the lower jaw can be recognised. Besides the latter muscle, m. intermandibularis is also extended far rostrad in S. saurus ( Figs. 19 and 20 ), however, in this species m. protractor hyoidei does not reach the anterior tip of the lower jaw. Referring to Haszprunar (1998) , one could argue that the elongation of a muscle within the lower jaw is simply an adaptation correlated to food ingestion and hence would not have a value for phylogenetic questions. However, as noted by de Pinna (1991) and Haas (2003) , such adaptations can be informative at particular hierarchical levels.

M. adductor arcus palatini

Origin and insertion. The anterior portion of m. adductor arcus palatini, the only portion of this muscle studied herein, originates along the whole parasphenoid and inserts dorsally along the entire suspensoric in R. corsula ( Figs. 6 and 7 ), Ap. lineatus ( Figs. 10 and 11 ), O. latipes ( Figs. 2E , 12A – 12C and 13 ), X. oophorus ( Fig. 3 ), and D. pussila ( Figs. 2G , 16 and 17 ) (in addition to other small attachments) [state 0]. In contrast, it originates on the posterior part of the parasphenoid and inserts on the posterior region of the suspensoric in Pe. fluviatilis ( Figs. 2A and 5 ), At. boyeri ( Figs. 2C , 8 , 9 and 12D ), Pa. brachypterus ( Figs. 2F , 14 and 15 ), B. belone ( Figs. 2H and 18 ), and S. saurus ( Figs. 19 and 20 ) [state 1].

M. levator arcus palatini

M. levator arcus palatine originates on the skull roof behind the eye, runs ventrally, and inserts dorsally to the posterior part of the suspensoric.

Origin. It originates broadly on the sphenotic in Pa. brachypterus ( Figs. 2F , 14 and 15 ) and D. pussila ( Figs. 2G , 16 and 17 ) [state 0]. In R. corsula ( Figs. 2B , 6 and 7 ), B. belone ( Figs. 2H and 18 ), and S. saurus ( Figs. 19 and 20 ), it originates on a ridge of the sphenotic, the processus sphenoticus, and some fibres originate directly on the sphenotic [state 1]. The muscle arises via a short tendon from the ventral edge of the transverse process of the sphenotic and runs ventrad along the posterior margin of the orbit, dorsally from the hyomandibular, and with few fibres from the sphenotic in O. latipes ( Figs. 2E , Figs. 12A – 12C and 13 ) and X. oophorus ( Fig. 3 ) [state 2]. It originates ventrally at the dermosphenotic in At. boyeri ( Figs. 2C , 8 , 9 and 12D ) [state 3] and from the autosphenotic and with some fibres at the sphenotic in Pe. fluviatilis ( Figs. 2A and 5 ) and Ap. lineatus ( Figs. 2D , 10 and 11 ) [state 4].

The m. levator arcus palatini plesiomorphically originates at the autosphenotic and with some fibres at the sphenotic. This condition is also visible in Ap. lineatus ( Figs. 10 and 11 ) and could be assumed as being plesiomorphic for all Cyprinodontiformes (compare to Hertwig, 2005 ; Karrer, 1967 ).

Course. During its course from origin to insertion, the thickness of m. adductor arcus palatini hardly changes in R. corsula ( Figs. 2B , 6 and 7 ), O. latipes ( Figs. 2E , 12A – 12C and 13 ), and X. oophorus ( Fig. 3 ) [state 0], whereas in all other species it becomes more than twice as thick [state 1].

Relation to other muscles. M. levator arcus palatini runs dorsally of the medial and lateral head of A2/3 and does not run between both heads heads in Pe. fluviatilis ( Figs. 2A and 5 ), R. corsula ( Figs. 2B , 6 and 7 ), Ap. lineatus ( Figs. 10 and 11 ), O. latipes ( Figs. 2E , 12A – 12C and 13 ), X. oophorus ( Fig. 3 ), and Pa. brachypterus ( Figs. 2F , 14 and 15 ) [state 0]. It is clearly situated between the lateral and the medial head of A2/3 in D. pussila ( Figs. 16 and 17 ) [state 1] or it is only partly surrounded by the lateral and by the medial head of A2/3 in B. belone ( Figs. 2H and 18 ) and S. saurus ( Figs. 19 and 20 ) [state 2].

Insertion. On the lateral face of the suspensoric of Pe. fluviatilis ( Fig. 5 ), Ap. lineatus ( Figs. 10 and 11 ), Pa. brachypterus ( Figs. 14 and 15 ), D. pussila ( Figs. 16 and 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ), m. levator arcus palatini inserts onto the hyomandibular and to the metapterygoid and with some fibres, it also can attach anteriorly to the processus lateralis hyomandibularis [state 0]. In O. latipes ( Figs. 12A – 12C and 13 ) and X. oophorus ( Fig. 3 ), it inserts on the broad face of the praeopercular and posterodorsally to the symplectic [state 1]. In R. corsula ( Figs. 6 and 7 ) and At. boyeri ( Figs. 8 , 9 and 12D ), it inserts on the hyomandibular, anteriorly to the processus lateralis hyomandibularis, to the metapterygoid, and to the broad face of the preopercular [state 2].

Kulkarni (1948) identified the metapterygoid as being reduced within Adrianichthyidae. This suggestion was only based on his observations in Horaichthys setnai and O. melastigma . Werneburg & Hertwig (2009) identified a horizontal suture in the ‘symplectic’ ( sensu Kulkarni, 1948 ) of O. latipes , which could represent the border of the metapterygoid. In histological sections and hence in 3D reconstructions ( Werneburg & Hertwig, 2009 ), such a differentiation of bones was not visible. As such, the situation remains unclear.

M. dilatator operculi

Origin. M. dilatator operculi connects the opercle with the skull roof. It originates ventrally at the lateral face of the sphenotic in Pa. brachypterus ( Figs. 2F , 14 and 15 ), X. oophorus ( Fig. 3 ), and S. saurus ( Figs. 19 and 20 ) [state 0]. It originates laterally at the sphenotic, at the autosphenotic, and with some fibres possibly at the anteroventral area of the pterotic in Pe. fluviatilis ( Figs. 2A and 5 ), At. boyeri ( Figs. 2C , 8 , 9 and 12D ), and Ap. lineatus ( Figs. 2D , 10 and 11 ) [state 1]. In R. corsula ( Figs. 2A , 6 and 7 ), O. latipes ( Figs. 2E , 12A – 12C and 13 ), D. pussila ( Figs. 2G , 16 and 17 ), and B. belone ( Figs. 2H and 18 ), it originates laterally at the sphenotic and anteriorly at the lateral face of the pterotic [state 2].

Shape. Anteriorly, m. dilatator operculi extends almost to the eye and lies dorsally to m. levator arcus palatini in R. corsula ( Figs. 2A , 6 and 7 ), At. boyeri ( Figs. 2C , 8 , 9 and 12D ), Ap. lineatus ( Figs. 2D , 10 and 11 ), and O. latipes ( Figs. 2E , 12A – 12C and 13 ) [state 0]. It does not reach the eye region in Pe. fluviatilis ( Figs. 2A and 5 ), X. oophorus ( Fig. 3 ), Pa. brachypterus ( Figs. 2F , 14 and 15 ), D. pussila ( Figs. 2G , 16 and 17 ), B. belone ( Figs. 2H and 18 ), and S. saurus ( Figs. 19 and 20 ) [state 1].

M. levator operculi

Origin. The m. levator operculi connects the opercle with the skull roof. It is an undivided muscle with an origin ventrally at the lateral face of the pterotic in all taxa studied [state 0], except for Pe. fluviatilis . In this species is a bipartite muscle with a large anterior origin ventrally at the lateral face of the pterotic and a small posterior origin ventrally at the ventral situated extrascapula ( Figs. 2A and 5 ) [state 1].

Insertion. M. levator operculi inserts dorsally to the medial face of the opercle and has a continuous horizontal level of insertion in Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and 7 ), Ap. lineatus ( Figs. 10 and 11 ), O. latipes ( Figs. 12A – 12C and 13 ), X. oophorus ( Fig. 3 ) , Pa. brachypterus ( Figs. 14 and 15 ), and D. pussila ( Figs. 16 and 17 ) [state 0]. It also inserts dorsally at the medial face of the opercle in B. belone ( Fig. 18 ) and S. saurus ( Figs. 19 and 20 ), but it attaches more ventrally to the anterior region of the medial face of the opercle [state 1]. The muscle inserts dorsally to the medial face and dorsally to the lateral face of the opercle in At. boyeri ( Figs. 8 , 9 and 12D ) [state 2].

Truncus maxillaris infraorbitalis trigemini. The truncus maxillaris infraorbitalis trigemini branches into the ramus mandibularis trigemini and ramus maxillaris trigemini short before or after leaving the neurocranium in Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and 7 ), At. boyeri ( Figs. 8 , 9 and 12D ), and Ap. lineatus ( Figs. 10 and 11 )—and dorsally to the suspensoric, the ramus mandibularis trigemini covers the ramus maxillaris trigemini laterally [state 0]. Contrary, in O. latipes ( Figs. 12A – 12C and 13 ), X. oophorus ( Fig. 3 ) , Pa. brachypterus ( Figs. 14 and 15 ), and D. pussila ( Figs. 16 and 17 ), it first branches at the level of the eye [state 1]. In B. belone ( Fig. 18 ) and S. saurus ( Figs. 19 and 20 ), it branches already within the neurocranium. Afterwards, the ramus maxillaris trigemini splits into two branches. Dorsally to the posterior part of the suspensoric, the branches align laterally and medially along the course of ramus mandibularis trigemini. On the level of the jaw joint, the branches of ramus maxillaris trigemini change their course into an anterodorsad direction and enter the upper jaw. Ramus mandibularis trigemini travels anteroventrad to the lower jaw [state 2].

Ramus mandibularis facialis. The ramus mandibularis facialis branches after leaving the hyomandibular laterally to the suspensoric in order to run with two branches to the medial side of the suspensoric in At. boyeri ( Figs. 8 , 9 and 12D ), Ap. lineatus ( Figs. 10 and 11 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ) [state 0]. In Pe. fluviatilis ( Fig. 5 ), R. corsula ( Figs. 6 and 7 ), O. latipes ( Figs. 12A – 12C and 13 ), Pa. brachypterus ( Figs. 14 and 15 ), and D. pussila ( Figs. 16 and 17 ) it branches differently [state 1]. The course of that nerve could not be followed in X. oophorus ( Fig. 3 ).

Lig. premaxillo-maxilla. This ligaments spans broadly between premaxilla and maxilla in B. belone ( Fig. 18 ) and S. saurus ( Figs. 19 and 20 ) [state 0] and between the proximal ends of the premaxilla and the maxilla in all other species [state 1].

Hertwig (2008) argued for the absence of the ligament in Beloniformes and mentioned an extensive area of connective tissue instead. Based on arguments of Werneburg (2013b) , I homologise this tissue with the broad ligament found in other taxa.

Primordial ligament. This ligament is present as a lig. maxillo-anguloarticulare between the maxilla and the anguloarticular in Pe. fluviatilis ( Figs. 2A and 5 ) and At. boyeri ( Figs. 2C , 8 , 9 and 12D ) [state 0]. The ligament is absent in all other species [state 1].

Upper jaw/palatine ligament. A ligament, which connects the palatine and the upper jaw, is present as lig. palato-maxilla between palatine and maxilla in At. boyeri ( Figs. 8 , 9 and 12D ), Ap. lineatus ( Figs. 10 and 11 ), O. latipes ( Figs. 12A – 12C and 13 ), X. oophorus ( Fig. 3 ), and Pa. brachypterus ( Figs. 14 and 15 ) [state 0]. It is present as lig. palato-premaxilla between palatine and premaxilla in Pe. fluviatilis ( Fig. 5 ) [state 1] or is absent in R. corsula ( Figs. 6 and 7 ), D. pussila ( Figs. 16 and 17 ), B. belone ( Fig. 18 ), and S. saurus ( Figs. 19 and 20 ) [state 2].

An autapomorphy in the ground pattern of Atherinomorpha may be the presence of a lig. palato-maxilla. The absence of the ligament in R. corsula ( Figs. 6 and 7 ) and a different attachment of the ligament in Pe. fluviatilis makes it impossible to reconstruct the ground pattern.

Lig. parasphenoido-suspensorium. This ligament is present in Pe. fluviatilis ( Fig. 5 ), At. boyeri ( Figs. 8 , 9 and 12D ), and S. saurus ( Figs. 19 and 20 ) [state 0]. It is absent in all other species [state 1].

For Pe. fluviatilis , Osse (1969) described two ligaments (his No. XVII and XVIII) that originate from the parasphenoid and insert to the dorsal edge of the suspensoric. This differentiation of the ligament could not be identified in the manual dissections performed for the present study.

Conclusions

In the present study, the variety of jaw, suspensoric, and opercle muscles was described for several acanthopterygian fishes with a focus on Beloniformes. The diversity of jaw muscles within Beloniformes corresponds to the external differences in their jaw morphology. As such, long beaked forms and species with protractible mouths show remarkable differences in their jaw musculature that may be correlated to stiffening or high mobility of the jaws.

Most important anatomical differences detected in this study exist in the external jaw musculature of Beloniformes. The jaw adductors belong to the most intensely studied muscles in vertebrates due to their prominent size and variation in the head and their importance for feeding mechanisms ( Haas, 2001 ; Diogo, 2008 ; Diogo & Abdala, 2010 ; Daza et al., 2011 ; Konstantinidis & Harris, 2011 ; Werneburg, 2013a ; Werneburg, 2013b ; Datovo & Vari, 2013 ; Datovo & Vari, 2014 ). Among Acanthopterygii, the external section of m. adductor mandibulae (A1) experienced comprehensive diversifications ( Wu & Shen, 2004 ), and among Beloniformes, it can either be present or absent.

The A1 lowers the upper jaw in most fishes. As an autapomorphy of Beloniformes, Mickoleit (2004) mentioned the reduced mobility of bones related to the upper jaw. Hertwig (2005) hypothesised that the reduced mobility of those bones might be correlated with the reduction of A1 within Beloniformes or the displacement of the A1-insertion apart from the upper jaw. In the present study, such a replacement of A1 was discovered in O. latipes ( Fig. 2E ; see also Werneburg & Hertwig, 2009 ). This species can still move its upper jaw during feeding (I Werneburg, pers. obs., 2006), which questions the possibility of a functional correlation of the character pair mentioned by Hertwig (2005) and Hertwig (2008) , namely ‘A1 no longer attached to upper jaw’ and ‘non-moveable upper jaw bones’.

Moreover, in the flying fish Pa. brachypterus , which has no A1 ( Fig. 2F ), a protrusible jaw was discovered herein. Therefore, the upper jaw bones are moveable against each other ( Figs. 14 and 15 ).

The hemiramphid Dermogenys pusilla , which hunts at the surface of the water ( Meisner, 2001 ), is able to easily move its short upper jaw, although the species has no A1 ( Fig. 2G ). Hence, coupled by ligament attachments, the lifting of the upper jaw appears to be indirectly performed by lowering the lower jaw. A deep coupling of those structures can be hypothesised for most other A1-lacking Beloniformes. In addition, the mobility of the protrusible upper jaw of Pa. brachypterus suggests a strong ligament-bone interaction ( Figs. 14 and 15 ).

Among hemiramphids, whose phylogenetic relationship is debated, A1 can be absent (this study: Dermogenys pussila ; Hertwig, 2008 : Hyporhamphus unifasciatus ) or can be present ( Hertwig, 2008 : Nomorhamphus sp., Hemiramphodon phaiosoma ; Rosen, 1964 : Arrhamphus brevis ). Also Exocoetidae seem to have members with an A1 ( Wu & Shen, 2004 : Cypselurus cyanopterus , Parexocoetus mento ; but see comments in the Results section) and members without an A1 (this study: Pa. brachypterus ). The phylogenetic significance of those conditions can first be adequately estimated when more species are observed and more clarity exists about phylogenetic interrelationship. But this requires further detailed and comprehensive observations.

At least for B. belone ( Fig. 2H ) and S. saurus ( Figs. 19 and 20 ), one may hypothesise that the loss of the A1 could be related to a strong fixation of the upper jaw to the cranium, realised by lig. premaxillo-frontale. Whether the upper jaw of both species is still moveable in vivo is not known so far, but is not expected.

As seen in hemiramphids, an elongated lower jaw not necessarily involves the reduction of A1. Xenopoecilus oophoris , an adrianichthyid with duckbill-like jaws, also has an A1 ( Fig. 3 ), which is attached to the upper jaw. This indicates that also an elongated upper jaw, which possibly was present in the ground pattern of Beloniformes already ( Parenti, 1987 ), not necessarily implies the loss of A1. Only the derived condition of two species, B. belone and S. saurus , which possess a stiffened upper jaw, may be clearly correlated to the loss of A1. As such, it can be expected that another belonid, Potamorrhamphis eigenmannii ( Miranda Ribeiro, 1915 ), which has a moveable upper jaw in vivo (I Werneburg, pers. obs., 2006), could have an A1, but this hypothesis needs further observation. The present study shows that the loss of A1 must not be interpreted only in correlation to elongated jaws. Other biomechanical requirements must be considered.

The studied selection of non-beloniform species must be handled with care when choosing them as potential outgroup species (as example see Hertwig, 2008 ). Compared to the insufficient documentation of the cranial musculature of most acathopterygian groups, the species dissected herein appear to show several derived characters. E.g., Rh. corsula has three main components of A2/3. Most mugiliform taxa, however, are reported to have a different arrangement of that muscle ( Gosline, 1993 : Agonostomus ; Van Dobben, 1935 : Mugil ; Wu & Shen, 2004 : Chelon , Crenimugil ; Starks, 1916 : Mugil ; Eaton, 1935 : Mugil ). As the authors of these studies did not observe histological sections, these findings could represent artefacts caused by the lower resolution of manual dissection.

As representative of the potential sister group to all remaining Beloniformes, the adrianichthyids Oryzias latipes and Xenopoecilus oophorus were studied herein. Hertwig (2005) , Hertwig (2008) and Werneburg & Hertwig (2009) already diagnosed several derived characters for O. latipes that could be affirmed herein and together with X. oophorus , it shares several derived characters. Due to the distinctive morphology of Adrianichthyidae, problems could arise when reconstructing the jaw muscle configuration in the ground pattern of Beloniformes. In addition to several derived characters, the taxon seems to display several plesiomorphic characters shared with Cyprinodontiformes. This finding persuaded Rosen (1964) and Li (2001) to postulate a sister group relationship of Adrianichthyidae + Cyprinodontiformes, named as Cyprinodontoidei ( Fig. 1A ). The present study highlights which characters are most variable among near related species and may assist taxon and character selection in future phylogenetic studies.

The differing external jaw morphology of diverse beloniform fishes is nicely reflected in the anatomy of their jaw musculature. Apparent changes concern the absence or presence of the A1 and arrangements of the intramandibular musculature. Both muscles are coupled to the upper or lower jaw, which are connected by ligaments themselves. The strong attachment of the upper jaw to the neurocranium, as visible in needlefishes and sauries, involves complex rearrangements of the soft tissue of the jaw apparatus.

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Introduction, acknowledgements.

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A functional analysis of jaw suspension in elasmobranchs

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CHERYL D. WILGA, A functional analysis of jaw suspension in elasmobranchs, Biological Journal of the Linnean Society , Volume 75, Issue 4, April 2002, Pages 483–502, https://doi.org/10.1046/j.1095-8312.2002.00037.x

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The morphology of the jaw suspension and upper jaw are quantified and related to upper jaw protrusion in five elasmobranchs possessing four jaw suspension types: broadnose sevengill, Notorynchus cepedianus , orbitostylic — amphistylic; spiny dogfish, Squalus acanthias , orbitostylic; bonnethead, Sphyrna tiburo , and lemon, Negaprion brevirostris , hyostylic; and Atlantic guitarfish, Rhinobatos lentiginosus , euhyostylic. The results indicate that jaw suspension type is not a good predictor of jaw mobility as previously thought. Instead, the best morphological predictor of jaw mobility appears to be either a long ethmopalatine ligament or no ligament, both of which allow the upper jaw to project further from the cranium. The morphology of the palatoquadrate-cranial articulation is key in determining the mobility of the jaws indicating that it should be included in descriptions of jaw suspension states. One advantage of upper jaw protrusion appears to be a reduction in the time to jaw closure by closing the mouth dorsally by upper jaw protrusion as well as ventrally by lower jaw elevation. A table of revised jaw suspension types is presented to illustrate the phylogenetic differences among gnathostome groups. Jaw suspension types mapped onto a gnathostome phylogeny support the evolution of holostyly and hyostyly from an autodiastylic ancestral condition.

Protrusion of the upper jaw during jaw closure on the prey is an integral part of feeding behaviour in elasmobranchs. In the past, the mobility of the upper jaw relative to the cranium has been thought to depend on the type of jaw suspension ( Huxley, 1876 ; Luther, 1909 ; Haller, 1926 ; Zlabek, 1931 ; Schaeffer, 1967 ; Moss, 1972 , 1977 ; Hyman, 1979 ). According to the literature, including comparative vertebrate anatomy textbooks, the type of jaw suspension in elasmobranchs (sharks, skates, and rays) is generally accepted as a major factor in determining the extent of jaw mobility ( Gregory, 1904 ; Schaeffer, 1967 ; Maisey, 1980 , 1984 ). The specific factors relating jaw suspension to upper jaw protrusion are not well understood and have not been investigated quantitatively. Therefore, the goal of this study is to quantify the relationship between jaw suspension, jaw and hyoid morphology, and upper jaw mobility in five species of elasmobranchs with four different jaw suspension types.

The three traditional types of jaw suspension have been defined primarily by the amount of support that the hyomandibular element of the hyoid arch gives to the mandibular arch ( Table 1 ) (Huxley, 1976; Gregory, 1904 ). A nonsuspensorial hyomandibula coupled with a palatoquadrate (upper jaw) that is fused to the cranium is referred to as autostylic ( Fig. 1B , Holocephali; O, Dipnoi; P, Tetrapoda). A palatoquadrate that is independent of and suspended from the cranium primarily by ligaments anteriorly and by a hyomandibula that is presumed to contribute little to jaw support is said to be amphistylic ( Fig. 1C , Xenacanthida; E, Palaeospinax ; G, Hexanchiformes). In contrast, the hyomandibula is thought to contribute more to jaw support than the anterior ligaments in hyostylic suspension ( Fig. 1D , Hybodontida; I, Heterodontiformes; J, Carcharhiniformes).

Summary of jaw suspension types by morphology in selected vertebrates (Based on Huxley, 1876; Gregory, 1904 ; De Beer & Moy-Thomas, 1935 ; Jollie, 1962a , b , 1971 ; Schaeffer, 1967 , 1981 ; Miles, 1968 ; Moy-Thomas & Miles, 1971 ; Compagno, 1973 , 1977 ; Zangerl & Williams, 1975 ; Jarvik, 1977 ; Maisey, 1980 , 1983 ; Carroll, 1988 ; Gaudin, 1991 ; Shirai, 1992 , 1996 ; Schultze, 1993 ; Carvalho, 1996 ; Janvier, 1996 ; Lund & Grogan, 1997 ; Maisey & Carvalho, 1997 ; Grogan et al. , 1999 ). Jaw Suspension terminology from De Beer & Moy-Thomas (1935) , Maisey (1980) and Grogan & Lund (2000)

Left lateral views of representative gnathostomes showing articulations involved in jaw suspension. Fig. 1A . Autodiastylic ancestor. Fig. 1B . Callorhinchus , Holocephali. Fig. 1C . Pleuracanthus , Xenacanthida. Fig. 1D . Hybodus , Hybodontida. Fig. 1E . Palaeospinax . Fig. 1F . Chlamydoselachus , Chlamydoselachida. Fig. 1G . Heptranchias , Hexanchiformes. Fig. 1H . Squalus , Squaliformes. Fig 1I. Heterodontus, Heterodontiformes. Fig. 1J . Sphyrna , Carcharhiniformes. Fig. 1K . Rhinobatos , Batoidea. Fig. 1L . Acanthodes , Acanthodii. Fig. 1M . Ephinephelus , Actinopterygii. Fig. 1N . Latimeria , Crossopterygii. Fig. 1O . Neoceratodus , Dipnoi. Fig. 1P . Ambystoma , Tetrapoda. Articulation surfaces marked with arrows. B, basal; C, ceratohyal; E, ethmoidal; EP, epihyal; H, hyomandibula; L, lower jaw; O, orbital; P, postorbital; T, paratemporal; U, upper jaw (redrawn from the following: Woodward, 1886 ; Schaeffer & Rosen, 1961 ; Jollie, 1962a ; Schaeffer, 1967 ; Miles, 1968 ; Maisey, 1977 , 1980 ; Zangerl, 1981 ; Lauder & Shaffer, 1985 ; Bemis, 1986 ; Lund & Grogan, 1997 ; Wilga, 1997 ; Wilga & Motta, 1998a , b ).

These three jaw suspension types broadly define hyomandibular support for the mandibular arch but did not include the various articulations of the palatoquadrate to the cranium, which are also important in jaw support. In all extant sharks the hyomandibula links the jaws to the cranium and thus is always functionally suspensory, and therefore hyostylic, to some degree ( Maisey, 1980 , 1984 ). Therefore, in this sense, hyostyly was not clearly distinguishable from amphistyly. Consequently, after examining the cranial-jaw articulations of Gegenbaur (1872) , Parker (1878) and Gregory (1904) , Goodrich & Lankester (1909) added the secondary requirement of a postorbital articulation between the postorbital process of the cranium and the palatoquadrate to the definition of amphistylic suspension in order to clearly distinguish it from hyostylic suspension.

The traditional jaw suspension terminology also fails to distinguish among different suspensorial apparatus of widely separated phylogenetic groups that are classified with the same jaw suspension type. Therefore, in an attempt to identify developmental and phylogenetic trends in jaw suspension, Gregory (1904) extended the definitions of jaw suspension to secondarily include the relationship of the hyoid arch as a whole to the cranium. Note that the suspension types described by Gregory (1904) are useful, regardless of his outdated ideas of how they may have evolved. Thus the state of the hyoid arch elements (hyomandibula and ceratohyal), whether intact as in the ancestral state (hyomandibula and ceratohyal elements comprising the suspensorium) or modified from the ancestral state (broken-up with the hyomandibula functioning as the suspensorium and the ceratohyal disconnected from the hyomandibula), are included in his reclassification of jaw suspension types. Holostyly is distinguished from autostyly and characterized as fusion of the palatoquadrate to the cranium with a nonsuspensorial intact hyoid arch ( Fig. 1A , Holocephali). In contrast, fusion of the palatoquadrate to the cranium with a nonsuspensorial modified hyoid arch (hyoid arch elements interconnected by other skeletal elements) is retained as autostyly ( Fig. 1O , Dipnoi; P, Tetrapoda).

Three additional hyostylic jaw suspension types, euhyostylic, methyostylic, and orbitostylic, were identified and are thought to have evolved from hyostyly ( Gregory, 1904 ; Maisey, 1980 ; Lund & Grogan, 1997 ; Grogan et al. , 1999 ). Batoids are classified as euhyostylic because the mandibular arch is suspended solely by the hyomandibula with no palatoquadrate-cranial ligaments or articulations present and by the modified (broken-up) state of the hyoid arch ( Fig. 1K , Batoidea). Bony fishes are classified as methyostylic because interhyal skeletal elements interconnect the hyomandibula and ceratohyal ( Fig. 1L , Acanthodii; M, Actinopterygii; N, Actinistia). Developmental differences between the orbital and ethmoid processes and their articulation with the cranium prompted Maisey (1980) to propose that orbitostyly be reserved for those sharks in which the orbital process articulates with the orbital wall ( Fig. 1F , Chlamydoselachiformes; G, Hexanchiformes; H, Squaliformes), in contrast to the articulation of the ethmoid process with the ethmoid region as in hyostylic jaw suspension ( Fig. 1I , Heterodontiformes; J. Carcharhiniformes). Thus, inclusion of the morphological state of the palatoquadrate and hyoid arch has clarified the descriptions of jaw suspension types, both phylogenetically and functionally.

HYPOTHESIZED PATTERNS OF JAW FUNCTION

The mobility of the upper jaw in elasmobranchs has been qualitatively related to jaw suspension type. It has been presumed that hyostylic sharks have greater upper jaw protrusion than amphistylic sharks due to the lack of a postorbital articulation (Huxley, 1976; Luther, 1909 ; Haller, 1926 ; Zlabek, 1931 ; Schaeffer, 1967 ; Moss, 1972 ). It has also been suggested that the orbitostylic and amphistylic jaw suspension of hexanchiform sharks do not permit jaw protrusion because of the postorbital articulation ( Moss, 1972 , 1977 ; Zangerl & Williams, 1975 ). Others, however, report that hexanchiform sharks, including Chlamydoselachus , are capable of limited protrusion (i.e. just enough to bare the teeth) ( Compagno, 1977 ). Similarly, some studies presume that the longer orbital process of squaliform sharks, also orbitostylic, limits jaw protrusion just to baring of the teeth ( Schaeffer, 1967 ; Compagno, 1977 ), although others have proposed that the jaws are freely protractile ( Haller, 1926 ; Moss, 1977 ). Yet, all agree that hyostylic sharks, particularly galeoid sharks, have freely protrusible jaws ( Schaeffer, 1967 ; Moss, 1972 , 1977 ; Maisey, 1980 ; Compagno, 1988 ). The extensive ethmoid articulation of heterodontiform and orectolobiform sharks is presumed to greatly restrict jaw protrusion even though they are classified as hyostylic ( Holmgren, 1940 , 1942 ; Smith, 1942 ; Schaeffer, 1967 ; Maisey, 1980 ). Lastly, the lack of articulations between the palatoquadrate and the cranium in batoids is thought to allow increased mobility of the jaws and extreme jaw protrusion compared to the hyostylic condition ( Luther, 1909 ; Schaeffer, 1967 ).

The morphology of the jaw suspension, such as the size and angle of the hyomandibula and type of palatoquadrate-cranial connections, has also been related to upper jaw protrusion and gape distance during feeding in sharks ( Moss, 1977 ). During feeding in carcharhiniform and lamniform sharks, the posteriorly directed hyomandibulae are pulled laterally disengaging the ethmoid articulation and allowing the upper jaw to rotate anteroventrally into the protruded position, also increasing the lateral and vertical dimensions of the gape ( Moss, 1972 , 1977 ; Frazzetta & Prange, 1987 ; Motta et al. , 1997 ; Wilga, 1997 ). Although hexanchiform sharks also have long posteriorly directed hyomandibulae, protrusion of the upper jaw may be confined to a dorsoventral plane as the orbital articulation does not clear the ethmopalatine groove, even at maximum protrusion ( Maisey, 1983 ; C. D. Wilga, pers. observ.). In contrast, the postorbital articulation in hexanchiform sharks slides readily and does not appear to impede vertical upper jaw mobility ( Compagno, 1988 ; C. D. Wilga, pers. observ.). It has also been suggested that the extent of upper jaw protrusion in squaliform sharks may be limited, compared to carcharhinid sharks, by the short laterally directed hyomandibula and the large orbital articulation which may restrict upper jaw movement ( Compagno, 1977 ). It has recently been shown, however, that spiny dogfish Squalus acanthias have freely protractile upper jaws during feeding ( Wilga & Motta, 1998a ). Batoids have long anteriorly directed hyomandibulae and most have extremely protrusile jaws ( Luther, 1909 ; Schaeffer, 1967 ; Wilga & Motta, 1998b ).

Based on the findings above, previous hypotheses about the relationship between upper jaw mobility and head morphology can be tested. (1) Relatively long posteriorly or anteriorly directed hyomandibulae should allow the jaws to protrude a greater distance from the cranium than do shorter more laterally directed hyomandibulae. (2) Loose ethmoid or orbital articulations (i.e. longer interconnecting ethmopalatine ligaments) with shorter processes should allow greater upper jaw movement than do tighter ones (i.e. shorter ethmopalatine ligaments) with longer processes.

In addition, previous hypotheses about jaw suspension types can be used to predict mobility of the jaws in the five species examined here. (1) Broadnose sevengill sharks, Notorynchus cepedianus (orbitostylic and amphistylic) should have the smallest upper jaw protrusion based on the postorbital articulation, despite the long posteriorly directed hyomandibula and short orbital process ( Fig. 1G , Galea: Hexanchiformes). (2) Spiny dogfish, Squalus acanthias (orbitostylic) should have the second smallest upper jaw protrusion based on the short laterally directed hyomandibula and long orbital process ( Fig. 1H , Squalea: Squaliformes). (3) Bonnethead sharks, Sphyrna tiburo , and lemon sharks, Negaprion brevirostris (both hyostylic) should have the second largest upper jaw protrusion based on the long posteriorly directed hyomandibula and short orbital process ( Fig. 1J , both Galea: Carcharhiniformes). (4) Atlantic guitarfish, Rhinobatos lentiginosus (euhyostylic) should have the largest upper jaw protrusion based on the long anteriorly directed hyomandibula and lack of palatoquadrate-cranial articulations ( Fig. 1K , Batoidea: Rhinobatiformes). Finally, in order to test the importance of including the morphology of the palatoquadrate and palatoquadrate-cranial connections as well as the hyomandibula in descriptions of jaw suspension states ( Grogan, 1993 ), hyomandibular variables are compared to hyomandibular and palatoquadrate variables in a principal components analysis.

Morphological characters were measured on five individuals each of Rhinobatos lentiginosus [3.6– 4.6cm head length (HL), 50.5–62.5cm total length (TL)], Sphyrna tiburo (6.5–7.4cm HL, 75–80cm TL), Squalus acanthias (4.7–5.6cm HL, 49.5–59.6cm TL), and Negaprion brevirostris (6.03–7.49cm HL, 61– 84cm TL) and four individuals of Notorynchus cepedianus (3.90–9.1cm HL, total length unknown). Fresh dead specimens were used for the morphological measurements in all species except for N. cepedianus in which three preserved specimens were used in which mobility of the skeletal elements was excellent (NMNH 27191, 27071, 61234) and was consistent with skeletal element mobility in the fresh specimen.

Five morphological characters were measured: upper jaw length; hyomandibula length; hyomandibula angle; orbital process length; and ethmopalatine ligament length ( Fig. 2 ). Measurements were taken as follows ( Fig. 2 ): hyomandibula length in cm from proximal to distal end; hyomandibula angle in degrees between a mid-sagittal line on the cranium from the rostrum to the hyomandibula-cranial joint and a line drawn along the anterior edge of the hyomandibula; upper jaw length in cm from proximal to distal end; extended ethmopalatine ligament length in cm from a line drawn along the dorsal edge of the palatoquadrate to the ventral edge of the ethmoid groove; orbital process length in cm from the base (as determined by a line drawn along the dorsal edge of the palatoquadrate) to the tip; and head length in cm from anterior nasal capsule to posterior otic capsule. Anatomical measurements were made to the nearest mm or degree with a mm-ruler, calipers, or protractor. These morphological variables are not used in distinguishing species or in constructing hypotheses of phylogeny, although the presence of the ethmoid, orbital, and postorbital articulations may be used as characters ( Compagno, 1977 ; Carvalho, 1996 ; McEachran et al. , 1996 ; Shirai, 1996 ; Lund & Grogan, 1997 ).

Dorsal (top) and left lateral (bottom) views of a generalized shark skull illustrating morphological measurements. Dotted lines indicate length measured: CT, ceratohyal; EP, ethmopalatine ligament; HYM, hyomandibula; MD, mandible; NC, capsule; OP, orbital process; OT, otic capsule; PQ, palatoquadrate or upper jaw.

Two kinematic variables were used in this paper, peak gape and peak upper jaw protrusion. Peak gape and peak upper jaw protrusion distance were calculated by digitizing the anterior tip of the upper jaw and the anterior tip of the lower jaw. Mobility or protrusion of the upper jaw was measured as the vertical distance that the upper jaw traveled from the resting position to the peak protruded position ( Fig. 3 ). Five individuals each of Rhinobatos lentiginosus (25 trials, mean five per individual), Sphyrna tiburo (22 trials, mean four per individual), Squalus acanthias (26 trials, mean five per individual), Negaprion brevirostris (20 trials, mean four per individual) and Notorynchus cepedianus (9 trials, mean two per individual) were videotaped during feeding to examine jaw mobility and gape distance. Pieces of fish ( S. acanthias , N. brevirostris , N. cepedianus ) or shrimp ( S. tiburo and R. lentiginosus ) just smaller than the diameter of the mouth, whichever was closest to natural prey for that particular species, were dropped into the tank or offered on a feeding stick until the shark was satiated. Kinematic variables were measured relative to the reference point of the field prior to the start of lower jaw depression because this initiated the feeding sequence. The maximum value calculated for each individual was used in the analysis. Videotape of broadnose sevengill sharks Notorynchus cepedianus feeding was provided by G. V. Dykhuisen of the Monterey Bay Aquarium. These variables were calculated as a percentage of head length for N. cepedianus , as no reference measurement was recorded in the video. These variables for S. acanthias , N. brevirostris , S. tiburo and R. lentiginosus are taken from previous work on feeding behaviour using the same individuals as in the morphological measurements above ( Motta et al. , 1997 ; Wilga & Motta, 1998a , b ; Wilga & Motta, 2000).

Representative video images illustrating kinematic measurements. Arrows indicate distance measured. (A) peak upper jaw protrusion. (B) Peak gape.

A one-way ANOVA was performed on the variables to test for differences among species using length measurements recalculated as percentage of head length in order to make interspecific comparisons on species that do not overlap in size. Raw values for hyomandibula angle were used. If a significant difference among species was detected by the ANOVA, a Student-Newman-Keuls multiple comparisons test was applied in order to detect specific differences among the species. The data passed the Levene Median test for homogeneity of variances and the Kolmogorov-Smirnoff test for normal distribution. Statistical tests were performed using SAS statistical software (Version 6.12). A Students t -test was used to test the contribution that peak protrusion of the upper jaw makes to reduce peak gape. In this test, peak gape was compared to peak gape minus upper jaw protrusion. The percent that peak upper jaw protrusion reduces the gape is calculated as follows: (peak upper jaw protrusion/peak gape distance) × 100. In order to examine the relationships among the morpho-logical and kinematic variables, a principal components analysis (PCA) was performed on the correlation matrix to group the variables into multivariate descriptive units.

JAW SUSPENSION

The jaw suspension of spiny dogfish, Squalus acanthias , is orbitostylic ( Fig. 4A ). The short laterally directed hyomandibula is the posterior source of jaw suspension with the ceratohyal-basihyal complex then articulating with the distal hyomandibula. Anteriorly, the palatoquadrate articulates with the orbital wall of the cranium by a relatively long orbital process. In the resting position, the base of the long orbital process of the upper jaw lies in a vertically orientated ethmopalatine groove, while the dorsal portion articulates with the orbital wall. The relatively long sheath-like ethmopalatine ligament extends from the edges of the ethmopalatine groove to the base of the orbital process and ensheathes the orbital process. In the retracted position, the ethmopalatine ligament folds back on itself. The orbital process in the ethmopalatine groove, the ectethmoid condyles and the hyomandibula restrict anteroposterior movement of the upper jaw. During manual manipulation, the orbital process does not leave the ethmopalatine groove even at peak upper jaw protrusion. Therefore, the orbital process in the ethmopalatine groove restricts both lateral and anteroposterior movement of the upper jaw. Ventral movement of the upper jaw is restricted primarily by the length of the unfolded ethmopalatine ligament and also by the surrounding skin and muscles between the upper jaw and chondrocranium.

Jaw suspension type in the (A) spiny dogfish Squalus acanthias (B) sevengill shark Notorynchus cepedianus (C) lemon Negaprion brevirostris and bonnethead Sphyrna tiburo sharks (D) Atlantic guitarfish Rhinobatos lentiginosus . Black, ethmopalatine ligament; light grey, palatoquadrate or upper jaw; medium grey, ceratohyal; dark grey, hyomandibula, cranium and mandible in white. CR, cranium; CT, ceratohyal; EA, ethmopalatine articulation; HY, hyomandibula; MD, mandible or lower jaw; OA, otic articulation; OB, orbital process; PQ, palatoquadrate or upper jaw; RA, orbital articulation.

The jaw suspension of broadnose sevengill sharks, Notorynchus cepedianus , is both amphistylic and orbitostylic ( Fig. 4B ). The hyomandibula is slim, directed posteriorly and joins the palatoquadrate to the cranium while the ceratohyal-basihyal complex articulates at its distal end. The orbital articulation is similar to dogfish, but sevengills have a relatively shorter orbital process and ethmopalatine ligament. It also has an additional articulation between the palatoquadrate and cranium in which the anteromedial region of the dorsal quadrate connects with the otic capsule by a small gliding-like articulation. The two sides of the otic articulation slide enough to allow the upper jaw to protrude from and clear the labial margins. During manual manipulation approximating video images of feeding individuals, the palatoquadrate articular surface may move well anteroventral to the postorbital articular surface of the joint, such that they are no longer in contact.

Carcharhiniform sharks have a hyostylic type of jaw suspension as illustrated by the lemon shark Negaprion brevirostris ( Fig. 4C ) and the bonnethead Sphyrna tiburo ( Fig. 1J ). The relatively long posteriorly directed hyomandibula suspends the jaws from the cranium posteriorly while the palatoquadrate articulation suspends the jaws from ethmoid region of the cranium anteriorly. The ceratohyal-basihyal complex articulates with the distal hyomandibula. In the resting position, the short ethmoid process (analogous to the orbital process of squaliform sharks) of the upper jaw lies in a vertically orientated ethmopalatine groove in the ethmoid plate, ventral to the orbit. The relatively thick rope-like ethmopalatine ligament folds onto itself and extends from the edges of the ethmopalatine groove to the orbital process. The ethmopalatine ligament is shorter in bonnetheads than in lemon sharks. The orbital process in the ethmopalatine groove, the ectethmoid condyles and the hyomandibula restrict anteroposterior movement of the upper jaw. The orbital process clears the ethmopalatine groove at peak upper jaw protrusion during manual manipulation (estimated position from video recordings) and probably does not restrict lateral movement of the upper jaw. Protrusion or ventral movement of the upper jaw is restricted up to the length of the ethmopalatine ligament.

The jaw suspension type in Atlantic guitarfish Rhinobatos lentiginosus is euhyostylic ( Fig. 4D ). The moderately long hyomandibula is directed anteriorly and is the sole element suspending the jaws from the cranium, there are no ligaments or articulations connecting the palatoquadrate to the cranium in batoids. The ceratohyal-basihyal complex is disconnected completely from the hyomandibula and instead is attached to the first branchial arch. The anterior face of the jaws are transversely and ventrally orientated in batoids in contrast to longitudinally and anteriorly directed in sharks.

GENERAL PREY CAPTURE BEHAVIOUR

Prey capture is the initial acquisition of the prey. The expansive or jaw opening phase begins with mouth opening by nearly simultaneous depression of the lower jaw and may be accompanied by elevation of the cranium ( Fig. 5 , left). If labial cartilages are present, they are extended as the lower jaw is depressed ( Fig. 5A , left). If suction feeding is present, as in Squalus acanthias and Rhinobatos lentiginosus , the orobranchial chamber is rapidly expanded and the prey may be drawn by suction inflow into the mouth shortly before peak labial cartilage extension and peak lower jaw depression ( Fig. 5A, B , left). If ram feeding is present, as in Negaprion brevirostris , Sphyrna tiburo , and Notorynchus cepedianus , the jaws are opened widely and engulf the prey as the predator swims over it ( Figs 5C–E , left). The compressive or jaw closing phase begins at peak gape and is followed by upper jaw protrusion and elevation of the lower jaw. When present, peak head lift occurs shortly before the jaws close completely. Peak upper jaw protrusion is attained just prior to complete elevation of the lower jaw ( Fig. 5 , right). Peak hyoid depression occurs after the upper and lower jaws are completely closed. The recovery or jaw retraction phase begins at jaw closure and consists of depression of the cranium (if elevated previously) and retraction of the upper jaw and hyoid. The recovery phase ends when the cranial elements are returned to the prefeeding resting position.

Video images of representative individuals showing peak gape (left) and peak upper jaw protrusion (right). A, Squalus acanthias; B, Rhinobatos lentiginosus ; C, Negaprion brevirostris ; D, Sphyrna tiburo ; E, Notorynchus cepedianus .

ANALYSIS OF VARIANCE

Video images of representative individuals illustrate the variation in peak gape and peak upper jaw protrusion among the five species ( Fig. 5 ). Analysis of variance reveals that all of the morphological variables show some differences among the five species ( Table 2 ; Fig. 6 ). No trends corresponding to jaw suspension type were detected. Those taxa with longer upper jaw lengths, longer hyomandibula lengths and larger hyomandibular angles had smaller upper jaw protrusion ( Notorynchus cepedianus , Sphyrna tiburo , and Negaprion brevirostris ) than those taxa possessing shorter upper jaw lengths, shorter hyomandibula lengths and smaller hyomandibular angles ( Squalus acanthias and Rhinobatos lentiginosus ). Longer ethmopalatine ligaments or the lack of an ethmopalatine ligament was found in those species showing greater upper jaw protrusion ( N. brevirostris , S. acanthias and R. lentiginosus ). Finally, the length of the orbital or ethmoid process had no relationship to upper jaw protrusion. The Students T -test showed that gape distance is significantly reduced by protrusion of the upper jaw in S. acanthias , R. lentiginosus , and N. brevirostris but not in S. tiburo and N. cepedianus ( Table 3 ).

Means and results of ANOVA on morphological variables in five each of Squalus acanthias (SA), Sphyrna tiburo (ST), Rhinobatos lentiginosus (RL), Notorynchus cepedianus (NC) and Negaprion brevirostris (NB)

Values are means of maximal values measured. Length and protrusion are indicated as percent of head length. HYM, hyomandibula; LCP, ethmopalatine ligament; OP, orbital process; UJ, upper jaw. SNK = results of Student- Newman-Keuls multiple comparisons test.

Significant difference at Bonferroni adjusted value of P = 0.007.

Box plots showing mean, range and standard error of morphological variables measured. Notorynchus cepedianus (NC), Squalus acanthias (SA), Sphyrna tiburo (ST), Negaprion brevirostris (NB) and Rhinobatos lentiginosus (RL).

Percent of maximum gape reduced by upper jaw protrusion

Significant P -value of 0.05.

PRINCIPAL COMPONENTS ANALYSIS

In the hyomandibula only analysis, principal components one and two account for 97% of the variance among the variables, PC3 only adds 3% to the total variance (not illustrated). Three of the five species cluster in different areas of morphospace in a plot of PC1 by PC2 with two species overlapping ( Fig. 7 , top). As is often the case (but see Gibb, 1997 ), PC1 is indicative of a size factor with the larger species loading higher than the smaller species ( Table 4 ). Hyomandibular angle is the only variable that loads highly on PC2. Thus, Notorynchus cepedianus loads high and positive on PC2, while the rest of the species load around zero. Gape distance loads high and positive on PC3, with hyomandibular length loading high and negative. The species cluster according to jaw suspension type, but not by jaw mobility.

Principal components analysis of hyomandibula only (top) and hyomandibula and palatoquadrate (bottom) variables in Squalus acanthias (black circles), Sphyrna tiburo (white triangles), Rhinobatos lentiginosus (grey squares), Notorynchus cepedianus (black diamonds), Negaprion brevirostris (grey hexagons).

Component loadings and correlation coefficients generated by PCA on hyomandibula, palatoquadrate and kinematic variables

Significant at P = 0.05.

In the combined hyomandibula and palatoquadrate analysis, principal components one and two account for 87% of the variance among the variables, PC3 contributes 9% of total variance (not illustrated) ( Fig. 7 , bottom). The five species cluster in distinctly different areas of morphospace in a plot of PC1 by PC2 ( Fig. 7 ). Again, PC1 is indicative of a size factor with the larger species loading higher than the smaller species ( Table 4 ). Upper jaw protrusion and ethmopalatine ligament length are the only variables that load highly on PC2. Thus, Squalus acanthias and Negaprion brevirostris load high and positive on PC2 while Notorynchus cepedianus and Sphyrna tiburo load negative, with Rhinobatos lentiginosus intermediate. Hyomandibula length loads high and positive on PC3, with hyomandibula angle loading negative. The species cluster according to jaw suspension type and jaw mobility by PC2.

The only variable that correlated significantly with upper jaw protrusion was ethmopalatine ligament length. Accordingly, those species with longer ethmopalatine ligaments or that lacks the ligament loaded high and positive on PC1 ( Squalus acanthias , Negaprion brevirostris , Rhinobatos lentiginosus ), while those with shorter ethmopalatine ligaments ( Sphyrna tiburo , Notorynchus cepedianus ) loaded negatively on PC1. Hyomandibula length, upper jaw length, and hyomandibula angle correlate directly with gape height. Those species with greater magnitudes of these characters cluster positively on PC1 ( S. tiburo , N. cepedianus and N. brevirostris ). Three of the N. cepedianus individuals were much smaller than one individual and explains their more negative position on the plot.

JAW SUSPENSION TYPE AS A PREDICTOR OF JAW MOBILITY

The type of jaw suspension is not a good predictor of mobility of the jaws as measured by upper jaw protrusion during feeding in the five elasmobranchs tested. The mobility of the upper jaw differs widely from the predicted pattern according to jaw suspension type. Even within a jaw suspension type, the distance that the upper jaw is protruded varies greatly. Notorynchus cepedianus (9% HL) with its orbitostylic and amphistylic jaw suspension does have the smallest upper jaw protrusion as predicted; however, it was indistinguishable from Sphyrna tiburo (10% HL) which has a hyostylic jaw suspension that was predicted to have large upper jaw protrusion. In addition, Squalus acanthias (29% HL), which also has an orbitostylic jaw suspension and was predicted to have small upper jaw protrusion, protrudes its upper jaw just as far as Rhinobatos lentiginosus (26% HL), which was predicted to have the largest upper jaw protrusion based on its euhyostylic jaw suspension. Negaprion brevirostris (18% HL), which has a hyostylic jaw suspension, was predicted to have large upper jaw protrusion but instead is intermediate compared to the other species.

Results from other studies support the lack of relationship between jaw suspension and upper jaw protrusion. Among three hyostylic sharks, white sharks, Carcharodon carcharius (Lamniformes), have large upper jaw protrusion ( Tricas & McCosker, 1984 ), while leopard sharks, Triakis semifasciata (Carcharhiniformes), have moderate upper jaw protrusion ( Ferry-Graham, 1998b ) and swellsharks Cephaloscyllium ventriosum (Carcharhiniformes) have negligible upper jaw protrusion ( Ferry-Graham, 1998a ). Other hyostylic sharks, such as horn sharks, Heterodontus francisi (Heterodontiformes) have relatively little jaw protrusion (7% HL) ( Pretlow-Edmonds, 1999 ) similar to nurse sharks, Ginglymostoma cirratum (12% HL), and epaulette sharks, Hemiscyllium ocellatum (9% HL) (both Orectolobiformes) ( Wu, 1994 ). Another orectolobiform species, spotted wobbegongs, Orectolobus maculatus , can protrude the upper jaw up to 33% of head length ( Wu, 1994 ). Thus, this additional evidence supports the variability in upper jaw protrusion distance within a jaw suspension type.

The length of the ethmopalatine ligament is the only morphological variable measured that correlates significantly with the extent of upper jaw protrusion. Those elasmobranchs with a relatively loose ethmoid or orbital articulation (i.e. longer ethmopalatine ligaments) can protrude the upper jaw a larger distance during feeding than those with a more restricted articulation (i.e. shorter ethmopalatine ligaments). There is no correlation, however, between jaw suspension type and ethmopalatine ligament length among the five species. Squalus acanthias has longer ethmopalatine ligaments and greater upper jaw protrusion than Notorynchus cepedianus and both have orbitostylic jaw suspensions. Presumably, the postorbital articulation in N. cepedianus does not restrict upper jaw mobility any more than the short ethmopalatine ligaments since it readily disengages during manual manipulation of a fresh specimen ( Compagno, 1977 ; pers. Observ.). In addition, Negaprion brevirostris has longer ethmopalatine ligaments and greater upper jaw protrusion than Sphyrna tiburo even though they both have hyostylic jaw suspensions. Furthermore, the length of the ethmopalatine ligament and the distance that the upper jaw is protruded in S. tiburo is similar to that in N. cepedianus . Rhinobatos lentiginosus has a euhyostylic jaw suspension and was correctly predicted to have the largest upper jaw protrusion ( Luther, 1909 ; Schaeffer, 1967 ). R. lentiginosus , which has no ethmopalatine ligament to restrict upper jaw movement, and S. acanthias , which has the longest ethmopalatine ligament, both have similar upper jaw protrusion ability. Therefore, either the absence of ethmopalatine ligaments or the presence of relatively long ethmopalatine ligaments appears to allow the upper jaw to move further away from the cranium.

There may be a phylogenetic trend in the morphology of the ethmopalatine ligament in sharks. This ligament (see Fig. 4 ) is solid, ropelike and extends from the dorsal surface of the ethmoid (analogous to the orbital) process to the cranium in Negaprion brevirostris and Sphyrna tiburo , as is typical of carcharhiniform and lamniform sharks ( Compagno, 1988 ). It also contains elastic fibers in Negaprion brevirostris and may be extended longer than its resting length ( Motta & Wilga, 1995 ). In contrast, in three squaliform sharks, Squalus acanthias , Notorynchus cepedianus , and Heptranchias perlo , one heterodontiform shark, Heterodontus francisci , and one orectolobiform shark, Ginglymostoma cirratum , the ethmopalatine ligament is thin, sleevelike and encases the orbital process and its articulation ( Daniel, 1915 ; Motta & Wilga, 1999 ; personal observation). It is unknown whether these are the prevalent ethmopalatine ligament morphologies for these groups. The rope-like character state appears in lamniform and carcharhiniform sharks (see Fig. 1J ), while the sleeve-like character state appears in Chlamydoselachus , hexanchiforms, and other squalean sharks as well as heterodontiform and orectolobiform sharks (see Figs 1H, I ). It may be that the sleeve-like character state is plesiomorphic for sharks, although it is not clear what functional characteristics these alternate states confer. The differences in morphology, however, do correspond to the differences in development of the orbital and ethmoid processes.

There is no correlation between upper jaw protrusion distance and hyomandibular morphology. Neither relatively long posteriorly directed hyomandibulae nor long upper jaws appear to increase upper jaw protrusion distance, contrary to predictions. Those sharks with longer more posteriorly directed hyomandibulae and long upper jaws have the smallest upper jaw protrusion distance ( Notorynchus cepedianus , Negaprion brevirostris and Sphyrna tiburo ). In contrast, those with shorter more anteriorly directed hyomandibulae and shorter jaws have the largest upper jaw protrusion distance ( Squalus acanthias and Rhinobatos lentiginosus ). There is a significant positive correlation among gape distance, upper jaw length, hyomandibula length, and hyomandibula angle. This may simply be a function of upper jaw length. In connecting the jaws to the cranium ( Fig. 4 ) the hyomandibula must become longer as the upper jaw is lengthened. As the upper jaw becomes longer, the distal end of the hyomandibula is positioned more posteriorly thereby increasing the angle measured. In all five elasmobranchs the jaws extend anteriorly to the nasal capsules. Thus, as the upper jaw becomes shorter, the hyomandibula becomes shorter and the angle decreases.

ADVANTAGES OF UPPER JAW PROTRUSION

Protrusion of the upper jaw is a striking component of feeding behaviour in sharks and several advantages of this behaviour have been proposed (Wilga et al. , 2001). Protrusion shifts the upper jaw away from the cranium and exposes the teeth, thereby increasing grasping ability ( Moss, 1972 ; Frazzetta & Prange, 1987 ; Frazzetta, 1994 ). A protrusile upper jaw provides the shark with a versatile cutting and gouging apparatus when feeding yet maintains a hydrodynamic profile during locomotion ( Alexander & Mc, 1967 ; Moss, 1972 , 1977 ; Tricas & McCosker, 1984 ). Protrusion provides for a nearly simultaneous closure of upper and lower jaws ( Frazzetta, 1994 ). Jaw protrusion may enable more efficient biting and manipulation of the prey ( Springer, 1961 ; Alexander, 1967 ; Moss, 1972 ). Protrusion may also direct suction currents from the benthos into the mouth of benthic feeders, such as in batoids ( Moss, 1977 ). Only a few of these advantages, however, have been rigorously tested (see Wilga et al. , 1901 ).

One function of upper jaw protrusion may be to allow for a more rapid closure of the jaws when feeding as Frazzetta & Prange (1987) suggested. Protrusion of the upper jaw contributes significantly to reducing the mouth closing distance in Squalus acanthias , Rhinobatos lentiginosus , and Negaprion brevirostris ( Motta et al. , 1997 ; Wilga & Motta, 1998a , b ). In contrast, jaw closing distance was not significantly reduced by upper jaw protrusion in Sphyrna tiburo and Notorynchus cepedianus ( Wilga, 1997 ; Wilga & Motta, 2000). In the absence of upper jaw protrusion, the distance that the lower jaw would have to travel to close the mouth would increase assuming the velocity of jaw closure remains the same. Note that cranial depression and upper jaw protrusion are independent mechanisms in elasmobranchs. It should also be noted that the timing of upper jaw protrusion during feeding differs in most bony fishes (but see Gibb, 1997 ) and elasmobranchs. Upper jaw protrusion is linked to lower jaw depression in bony fishes and consequently begins as the lower jaw is depressed in the mouth opening phase (reviewed in Motta, 1984 ). Upper jaw protrusion begins during elevation of the lower jaw in the mouth closing phase in elasmobranchs and is not linked to lower jaw movements (Wilga et al. , 2000).

Protrusion of the upper jaw in elasmobranchs may be developmentally and functionally linked to adduction of the jaws. During development, the preorbitalis muscle separates from the anterior edge of the presumptive quadratomandibularis muscle, the main adductor muscle between the upper and lower jaw, and extends anteriorly to insert onto the cranium or anterior upper jaw ( Edgeworth, 1935 ). Together these two muscles form a functional unit called the adductor mandibulae complex ( Edgeworth, 1935 ; Lightoller, 1939 ). Not surprisingly, upper jaw protrusion occurs during jaw closure in all elasmobranch taxa that have been investigated (Wilga et al. , 2001).

NEW DEFINITION OF JAW SUSPENSION TYPES

A combination of jaw suspension types from Huxley (1876), Gregory (1904) , De Beer & Moy-Thomas (1935) , Maisey (1980) , and Grogan & Lund (2000) are proposed in order to illustrate the diversity of morphological states more accurately (see Table 1 , last column). The concepts of holostylic and autostylic jaw suspensions are generally in agreement. It appears that several ideas underlie our concept of what comprises a hyostylic jaw suspension in elasmobranchs: the hyomandibula suspends the jaws (Huxley, 1976; Maisey, 1980 ); jaw suspension types possessing a suspensory hyomandibula are a subset of hyostylic suspension ( Gregory, 1904 ; Maisey, 1980 ), and that hyostylic sharks possess an ethmoid articulation ( Maisey, 1980 ; E. D. Grogan, pers. comm.) ( Table 1 ). If these ideas are true, then hyostylic jaw suspension may be described as having a suspensory hyomandibula and an ethmoid articulation. The morphological state of the palatoquadrate-cranial connections may then be used to further subdivide jaw suspension types: a postorbital articulation indicates amphistylic suspension; an orbital articulation indicates an orbitostylic suspension; and loss of the palatoquadrate-cranial connections indicates a euhyostylic suspension. Using this combined classification of nonmutually exclusive jaw suspension types, only one shark group has more than one jaw suspension type, Hexanchiformes are both orbitostylic and amphistylic, while other elasmobranch groups fit into well defined morphological and functional jaw suspension types. Methyostylic jaw suspension in Actinopterygians is characterized by having a hyoid arch that is broken up by other intervening skeletal elements and a basal articulation. The addition of a postorbital articulation in Acanthodii and Actinistia is then referred to as metautodiastyly.

EVOLUTION OF JAW SUSPENSION

De Beer & Moy-Thomas, (1935) proposed a hypothetical ancestral condition for gnathostomes called autodiastyly because it presented a nonfused autostylic state from which all other jaw suspension types could be derived. In autodiastyly, the hyoid arch is nonsuspensorial, is similar in morphology to branchial arches and articulates with the palatoquadrate ( Fig. 1 a ). In this state the palatoquadrate is nonfused with ethmoidal and orbital articulations to the cranium, which are considered general gnathostome characters ( Janvier, 1996 ).

Determination of jaw suspension type in placoderms is problematic and may represent some preautodiastylic form or alternatively it may have lost the orbital articulation of some autodiastylic ancestor ( Grogan & Lund, 1900 ). The jaw suspension of placoderms is not well known because the hyomandibular cartilage is not preserved, however, the palatoquadrate is attached to the cranium in fossil arthrodires and thus is reported as autostylic but also possesses an ethmoid articulation ( Miles & Westol, 1968 ; Miles, 1969 ; Moy-Thomas & Miles, 1971 ; Goujet, 2001). The presence of a hyomandibula joining the cranium to the jaws and disconnected from the ceratohyal in rhenanid placoderms, similar to that in rays, is thought to be a derived condition from the basal placoderm state ( Moy-Thomas & Miles, 1971 ). The autostylic state of the jaw suspension in placoderms may actually be autodiastylic with the addition of interconnecting dermal elements similar to that of metautodiastyly ( Grogan & Lund, 1900 ). If so, then additional evidence is required to further resolve the current placoderm position as the sister group to all other gnathostomes as to whether they are the closer to Chondrichthyes or Osteichthyes.

Recent fossil evidence indicates that autodiastyly may be the ancestral jaw suspension type in gnathostomes. Studies of 18 complete to fragmentary specimens has confirmed that an operculate chondrichthyan Debeerius ellefseni thought to represent the condition prior to the divergence of holocephalans and elasmobranchs is autodiastylic (the prevalent mode of jaw suspension in carboniferous chondrichthyans), thus well supporting the theory that autodiastyly is the ancestral jaw suspension state for gnathostomes ( De Beer & Moy-Thomas, 1935 ; Grogan, 1993 ; Janvier, 1996 ; Lund & Grogan, 1997 ; Grogan et al. , 1999 ; Grogan & Lund, 1900 ). Another recent fossil, Pucapampella , described from the very generalized braincases of two specimens has postorbital, palatobasal, and possibly ethmoid articulations, may also represent a stem chondrichthyan (Maisey, 2001). If so, then stem chondrichthyans had more complex jaw suspensions, in having the ethmoid articulation of holocephalans and selachians, the postorbital articulation of basal selachians, and the palatobasal articulation of osteichthyans. Alternately, Pucapampella has lost the orbital articulation of the autodiastylic ancestor and gained the postorbital articulation of other basal elasmobranchs as well as the palatoabasal articulation found in metautodiastyly. Still another recent study on well preserved stethacanthids, shark-like fishes, suggests two contrasting trees, an unconventional topology in which holocephalans emerge from a paraphyletic clade of selachians and in which amphistyly is the ancestral type, and a more conventional topology similar to that in Figure 8 ( Coates & Sequira, 1901 ). Thus, the ancestral jaw suspension type in stem gnathostomes as well as chondrichthyans is still unclear. A more comprehensive analysis including all of those above is required to better understand the origin of gnathostomes and clarify the order of morphological rearrangements of the jaw suspension in early gnathostomes.

Relationships among the major lower vertebrate groups with type of jaw suspension mapped onto it. 0, AD, Autodiastyly; 1, HL, Holostyly; 2, AM, Amphistyly (has postorbital articulation); 3, HY, Hyostyly; 4, O, Orbitostyly; 5 OP, Orbitostyly with postorbital articulation; 6, E, Euhyostyly; 7, MA, Metautodiastyly (has postorbital articulation); 8, M, Methyostyly; 9, AU, Autostyly. Jaw suspension types from Table 1 . Jaw suspension types were mapped onto the cladogram according to Wiley et al. (1991) . (Cladogram after Maisey, 1986 ; Lauder & Liem, 1983 ; Carvalho, 1996 ; Shirai, 1996 ; Lund & Grogan, 1997 ).

Mapping of the jaw suspension types onto a gnathostome phylogeny can help to shed light on how the various jaw suspension states may have evolved ( Fig. 8 ). There is more evidence based on development of the palatoquadrate-cranial connections that autodiastyly is the ancestral jaw suspension type in chondrichthyes ( Fig. 1A ) ( De Beer & Moy-Thomas, 1935 ; Miles & Westol, 1968 ; Miles, 1969 ; Moy-Thomas & Miles, 1971 ; Lund & Grogan, 1997 ; Grogan et al. , 1999 ; Grogan & Lund, 1900 ). Selachian, chimaeroid, and osteichthyan jaw suspension states are all derivable from an autodiastylic plesiomorphic condition ( Grogan & Lund, 1900 ). Fusion of the palatoquadrate to the cranium evolved in holocephalans, while elaboration of a postorbital articulation and modification of the epihyal to form a suspensory hyomandibula evolved in selachians ( Lund & Grogan, 1997 ; Grogan et al. , 1999 ). Embryological evidence indicates that the postorbital articulation is a secondary development ( De Beer & Moy-Thomas, 1935 ; De Beer, 1937 ; Holmgren, 1940 ; Grogan et al. , 1999 ). If so, then this supports the derivation of amphistyly in cladoselachians and Palaeospinax from an autodiastylic state ( Figs 1C, E ) (Huxley, 1976; Gregory, 1904 ). Hyostyly was retained in the jaw suspensions of hybodontoid and galean sharks ( Figs 1D, I, J ) ( Maisey & Carvalho, 1997 ), while orbitostyly evolved and spread throughout squalean sharks ( Figs 1F–H ). Hexanchiform sharks retained the postorbital articulation as it acquired the orbitostylic articulation, and therefore possesses two jaw suspension types ( Fig. 1G ). If batoids are derived squaloids as Shirai (1996) and Carvalho (1996) hypothesize, then loss of the orbital articulation suggests a modified suspension that is ‘truly’ hyostylic, i.e. euhyostylic, with the hyomandibula functioning as the sole means of jaw support ( Fig. 1K ). Alternately, if batoids are the sister group to sharks as Compagno (1988) and Naylor (pers. comm.) theorize, then the euhyostylic state evolved from the autodiastylic state with the loss of the cranial-palatoquadrate articulations.

The distinctive morphology of the hyoid arch and suspensorium in bony fishes and cartilaginous fishes indicates that hyostyly arose along different paths from the ancestral form ( De Beer & Moy-Thomas, 1935 ). Similarly, it has been suggested that the amphistylic suspension in Acanthodes was independently acquired from that in Chondrichthyes ( Miles, 1968 ). Acanthodes , Climatius , and Latimeria ( Fig. 1L , Acanthodii; Fig. 1N , Actinistia) have a postorbital articulation and are considered amphistylic, but like Osteichthyes they also possess interhyal skeletal elements interconnecting the palatoquadrate and hyomandibula ( Janvier, 1996 ) as defined for methyostyly ( Gregory, 1904 ) and metautodiastyly ( Grogan & Lund, 1900 ). Furthermore, the palatobasal articulation is thought to be unique to osteichthyans and acanthodians ( Janvier, 1996 ; but see Gardiner, 1984 ). In Osteichthyes, the basal jaw suspension type appears to have been metautodiastyly, which may have evolved from autodiastyly with the acquisition of interhyal skeletal elements ( Grogan & Lund, 1900 ). A postorbital articulation may have developed secondarily as in Chondrichthyes and appears in some Acanthodii, Actinistia, and other fossil groups, such as osteolepiforms. Methyostyly then evolved in Actinopterygians while autostyly evolved in Dipnoi and Tetrapoda.

Within Chondrichthyes and Osteichthyes, some general trends in the evolution of jaw suspension are observed. After an early split from holocephalans, there is a trend towards an increase in mobility of the jaws in sharks ( Fig. 1B–K ). The earliest xenacanth ancestor possessed grasping dentition, long jaws and a large gape, as in Chlamydoselachus ( Carroll, 1988 ), which suggests a biting or ram feeding mechanism. Subsequent evolution involved shortening of the jaws and increased kinesis of the jaw suspension, which may have facilitated the evolution of a diversity of feeding mechanisms observed throughout shark and batoid groups such as suction ( Moss, 1977 ; Wilga et al. , 2000). A similar trend appears within the bony fishes ( Fig. 1L , Acanthodii; Fig. 1M , Actinopterygii) ( Schaeffer & Rosen, 1961 ). Palaeoniscoid fishes had a large gape and an obliquely orientated suspensorium (metautodiastyly or methyostyly) that also suggests a bite or ram feeding mechanism. Modifications in the palate and jaws increased the mobility of the upper jaw and are presumed to have led to an adaptive radiation of acanthopterygian feeding mechanisms, including suction feeders with highly protrusile jaws as in most teleosts. The reverse trend is observed in Sarcopterygii (metautodiastyly) with an increase in the number of articulations between the mandibular arch and the cranium until the upper jaw is fused to the cranium as in Dipnoi and Tetrapoda (autostyly) ( Fig. 1N , Actinistia; O, Dipnoi; P, Tetrapoda). Thus, major adaptive levels in the evolution of feeding mechanisms in Chondrichthyes have been accompanied by changes in suspension, orientation, and increasing mobility of the hyoid arch and palatoquadrate, which enhanced protrusion of the upper jaw, similar to that in Osteichthyes ( Schaeffer & Rosen, 1961 ).

What is clear is that there is considerable morphological variation among and within jaw suspension types and that generalizations regarding function often are not supported. Additional morphological and functional work is needed, on fossil as well as extant taxa, in order to clarify and understand the evolution of jaw suspension in gnathostomes and the functional states they confer.

I wish to express my appreciation to Philip Motta and Timothy Tricas for lively discussions that led to the concept of this project. Thanks to Gil Van Dykhuisen of Monterey Bay Aquarium and Philip Motta of the University of South Florida for providing video footage and data. Friday Harbor Laboratories, Mote Marine Laboratory, and the National Museum of Natural History provided facilities, equipment and specimens for dissection. This research was supported by an NRC-Ford Foundation Predoctoral Fellowship, University of Washington grant for research at Friday Harbor Laboratory, Mote Marine Laboratory and University of South Florida Graduate Fellowship in Elasmobranch Biology. Many thanks to Phil Motta, Eliot Drucker, Lara Ferry-Graham, Alice Gibb and George Lauder for their helpful comments on the manuscript.

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Typology of the Suspensorium Structure of Teleost Fishes in Regard to Their Feeding (Review)

• BIOLOGY, MORPHOLOGY, AND SYSTEMATICS OF HYDROBIONTS
• Published: 16 August 2022
• Volume 15 , pages 381–402, ( 2022 )

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• V. V. Makhotin 1 &
• E. S. Gromova 1  

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The suspensorium structure is reviewed and described for the definitive stage of development of Teleostei representatives in regard to the peculiarities of its functioning when using various types of feeding in this group of animals. The proposed qualitative classification of the suspensorium structure of fish is based on the strengthening or weakening of its structure. This review gives a description of the varieties of internal kinetics of the suspensorium of Teleostei species and describes the mechanism of internal adduction.

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Makhotin, V.V., Gromova, E.S. Typology of the Suspensorium Structure of Teleost Fishes in Regard to Their Feeding (Review). Inland Water Biol 15 , 381–402 (2022). https://doi.org/10.1134/S199508292204037X

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hyostylic jaw suspension  

A type of jaw suspension seen in most fishes, in which the upper jaw is not directly connected to the cranium. The attachment between cranium and upper jaw is made by a ligament at the front end and by the hyomandibular (... ...

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suspensorium

Definition of suspensorium

Word history.

New Latin, from Late Latin, instrument for suspending, from Latin suspensus (past participle of suspendere to suspend) + -orium

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