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Osteichthyan Feeding and Respiration

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Contributions to Zoology, 72 (I) 17-37 (2003) SPB Academic Publishing bv, The Hague The clavobranchialis musculature in sarcopterygian fishes, and contribution to osteichthyan feeding and respiration Zerina Johanson Palaeontology, Australian Museum, 6 College Street, Sydney, NSW 2010, Australia, e-mail: [email protected] Keywords:: Clavobranchiales, Sarcopterygii, Actinopterygii, Chondrichthyes, coracobranchiales, Dipnoi, Neoceratodus, Strepsodus Abstract Introduction Various fossil distinct the lungfish taxa preserve depressions on Muscles originating on pectoral girdle and in- the smooth postbranchial lamina ofthe dermal pectoral girdle. serting anteriorly on the mandible and branchial These depressions are largely unknown in other sarcopterygian arches depress or lower the mandible, hyoid arch, fishes, are but present in the rhizodont sarcopterygian Strepsodus. and more posterior gill arches. Of these muscles, Comparisons extant fishes these with actinopterygian suggest much of the research into ver- depressions mark the point of origin for the clavobranchialis gnathostome (jawed and has musculature, extending anterodorsally into the gill chamber to tebrates) feeding respiration focused on the insert on the ventral surface ofthe Studios ceratobranchial(s). sternohyoideus and coracomandibularis. The sterno- examining feeding and respiratory mechanisms ofbony fishes hyoideus (= rectus cervicus) attaches to the ventral (Osteichthyes) have emphasised the role of mandibular depres- of the hyoid arch and lowers the mandible within the oral portions sion in generating negative pressures cavity to draw in via the the latter run- water/air/food via suction. However, phylogenetically mandibulohyoid ligament, basal dorsal and actinopterygians, fossil lungfish and other fossil sarcoptc- ning between the ceratohyal the rear of rygians (such as Strepsodus) lack the apomorphies that increase the mandible (Lauder, 1979, 1980, 1982, 1983a, b, suction among bony fishes. In these taxa the clavobranchialis 1985; Lauder& Shaffer, 1985; Bemis, 1987; Bemis muscles to this re- may serve augment negative pressure by & Lauder, 1986; Shaffer & Lauder, 1985; & the Reilly tracting ceratobranchialsand increasing the size of the oral/ Lauder, 1990). This was described as a oropharyngeal cavity. A comparable action is performed by the general- ised the chondrichthyan coracobranchiales muscles, particularly during mechanism for Gnathostomata, occurring feeding, and the is function of these ventral gill arch muscles in acanthodians, actinopterygians, extant lungfishes, likely to be a synapomorphy of jawed vertebrates (Gnatho- coclacanths (the latter two groups representing the stomata). This musculature is absent from jawless vertebrates such Sarcopterygii) and aquatic salamanders as the Osteostraci. piscine (Lau- der, 1980, 1982, 1985; Bemis & Lauder, 1986; Campbell & Barwick, 1987, 1988a, 1999; Maisey, Contents 1989; Reilly & Lauder, 1990). Attachment surfaces for the sternohyoideus muscle and mandibulohyoid Introduction are also in various fossil sarco- 17 ligament preserved Materials ‘ and methods 18 pterygian taxa including Eusthenopteron (Jarvik, The dermal pectoral girdle of fossil sarcopterygians and 1980), Gogonasus (Long et ah, 1997: figs 39, 48B, associated muscle attachments 19 D), Medoevia (Lebedev, 1995: fig. 18B), The Glyptolepis role of the clavobranchialis in feeding and respira- 1972: and several fossil tion (Jarvik, fig. 28), lungfishes 2'j 1977; et ah, 1993; & Bar- Discussion 30 (Miles, Wang Campbell Conclusions Barwick & 33 wick, 1988a, 2002; Campbell, 1996; Acknowledgements ' KSW 33 Campbell, pers. comm. 2002). However, re- References 34 cent research on the chondrichthyan musculature 18 Z. Johanson - Clavobranchialis musculature in fossil lungfishes questioned the function ofthe mandibulohyoid liga- (Lauder, 1979, 1982, 1983a, b; Bemis & Lauder, in this the main muscle fossil ment group. Rather, lowering 1986). Nevertheless, among sarcopterygians, the mandible was the coracomandibularis, inserting a variety of fossil lungfish possess well developed at the symphysis of the chondrichthyan lower jaw muscle attachment surfaces on the postbranchial (Wilga et ah, 2000). laminae of the pectoral girdle. Comparable attach- As the mandibleis loweredand the mouth opened, ment surfaces occur on the clavicles of the rhizodont negative pressure (suction) created within the oral sarcopterygian fish Strepsodus. These surfaces may draws in aerated and food indicate the of clavobranchiales cavity water (or air) presence a com- materials. Mandibular depression was said to cre- parable to various actinopterygians (Jessen, 1972), in ate the greatest change in the volume of the oral and the size of the depression lungfish such as cavity and provide the greatest contribution to this Griphognathus indicates that the muscles themselves could be of substantial size. negative pressure (Lauder, 1985). Additionally, actinopterygians (e.g., Alexander, 1969, 1970; Liem, As described below, the action of ventral gill arch have both 1970; Lauder, 1983b), lepidosirenid lungfish (Pro- depressors may improved feeding topterus and Lepidosiren (Bemis, 1987; Bemis & and respiratory efficiency by increasing the rate at Lauder, 1986)) and aquatic salamanders (Lauder which water/food/air is brought into the oral cav- & Shaffer, 1985) modify various aspects of their ity in chondrichthyans, sarcopterygians and actino- jaws, skull, gill arch, pectoral girdle and muscle pterygians, and particularly in phylogenetically basal increase of the latter Evidence for the morphology to negative pressure gener- taxa two groups. pres- ated within the oral cavity. These modifications serve ence of these muscles and active branchial arch to increase the flow of water/air into the mouth, depression can also be found in certain fossil gnatho- improving the efficiency of both respiration and stomes such as the Placodermi, suggesting the ac- feeding. By comparison, fossil sarcopterygians (in- tion of this gill arch musculature in feeding and cluding non-lepidosirenid lungfish) appear to lack respiration occurs throughout jawed fishes. By com- these modifications, as do fossil and phylogenetically parison, the action of the sternohyoideus muscle in basal actinopterygians (Lauder, 1980, 1982), and lowering the mandible and opening the mouth the within the mouth via the arch and negative pressure generated hyoid mandibulohyoid liga- cavity of these taxa was considered to be relatively ment, described as a feature of the Gnathostomata low (Lauder, 1980). (e.g., Lauder, 1980, 1982), does not occur in chon- However, little consideration has been given in drichthyans (Wilga et ah, 2000), nor in placoderms these discussions to the musculature responsible (Johanson, in press). In these taxa the coracomandi- for the more and the the depressing posterior gill arches, bularis, inserting at jaw symphysis, opens its role in expanding and increasing the volume of mouth. the oropharyngeal cavity during the initial stages of feeding and respiration. These muscles, in- cluding the clavobranchiales in osteichthyans and Materials and methods the coracobranchiales in chondrichthyans, originate on (or in association with) the pectoral girdle and Specimens illustrated were either photographed after insert on the ventral the surfaces of branchial arches being coated with an ammonium chloride sublimate evidence indi- scanned in (ceratobranchials). Experimental (Figs 3, 4, 5) or from various publica- cates that the coracobranchialesact chondrichthyan tions (Figs 1, 2, 7). Line drawings (Fig. 6) were to the branchial basket depress during feeding made directly from photographs. In Figure 8, a 25 (Moss, 1977; Mallatt, Motta 1997: 1996; et ah, cm long individual of the lungfish Neoceratodus lig. 4), a link the indicating between activity of was cut by hand into sections and photographed these muscles and the movement of and Institutional water food on a light table. abbreviations: AMF: into the mouth. Similar of activity the clavobran- Australian Museum, Sydney; QMF: Queensland chialis has musculature not been examined in sarco- Museum, Brisbane. pterygians (extant lungfish) nor in actinopterygians Contributions to Zoology, 72 (I) - 2003 19 The dermal pectoral girdle of fossil and includes the Porolepiformes, inwhich the lamina sarcoptery-gians and associated muscle can be relatively wide with no indication of mus- attachments attachments cle present (Jarvik, 1972). Youngolepis (Chang, 1991) is also assigned to the Dipnomorpha The dermal pectoral girdle of fossil sarcopterygians (Ahlberg, 1991) and its postbranchial lamina ap- is well known be covered in dermal (e.g., Andrews & Westoll, 1970a, b; pears to ornament (also the Jarvik, 1972, 1980; Miles, 1977; Long, 1989; Fox onychodont Strunius) rather than smooth. The Tetra- et ah, 1995; Lebedev, 1995; Ahlberg & Johanson, podomorpha include taxa more closely related to Johanson than 1997; & Ahlberg, 1997). Among these, a the Tetrapoda the Dipnoi (lungfish) and gen- of reduced variety fossil lungfish including Sagenodus, Eoc- erally possess postbranchial lamina, often tenodus, Pillararhynchus, Holodipterus, Gripho- only represented by a narrow, unornamented strip gnathus, Chirodipterus and Ctenodus (Watson & along the dorsomedial margin of the cleithrum and Gill, 1923; Miles, 1977; Long, 1987; Pridmore et clavicle (Jarvik, 1972, 1980; Fox et ah, 1995; Le- ah, 1994; Barwick & Campbell, 1996; Campbell bedev, 1995). However, distinct depressions are & associated with
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    Muscle Development in the Shark Scyliorhinus Canicula: Implications for the Evolution of the Gnathostome Head and Paired Appendage Musculature Janine M

    Ziermann et al. Frontiers in Zoology (2017) 14:31 DOI 10.1186/s12983-017-0216-y RESEARCH Open Access Muscle development in the shark Scyliorhinus canicula: implications for the evolution of the gnathostome head and paired appendage musculature Janine M. Ziermann1*, Renata Freitas2,3 and Rui Diogo4 Abstract Background: The origin of jawed vertebrates was marked by profound reconfigurations of the skeleton and muscles of the head and by the acquisition of two sets of paired appendages. Extant cartilaginous fish retained numerous plesiomorphic characters of jawed vertebrates, which include several aspects of their musculature. Therefore, myogenic studies on sharks are essential in yielding clues on the developmental processes involved in the origin of the muscular anatomy. Results: Here we provide a detailed description of the development of specific muscular units integrating the cephalic and appendicular musculature of the shark model, Scyliorhinus canicula. In addition, we analyze the muscle development across gnathostomes by comparing the developmental onset of muscle groups in distinct taxa. Our data reveal that appendicular myogenesis occurs earlier in the pectoral than in the pelvic appendages. Additionally, the pectoral musculature includes muscles that have their primordial developmental origin in the head. This culminates in a tight muscular connection between the pectoral girdle and the cranium, which founds no parallel in the pelvic fins. Moreover, we identified a lateral to ventral pattern of formation of the cephalic muscles, that has been equally documented in osteichthyans but, in contrast with these gnathostomes, the hyoid muscles develop earlier than mandibular muscle in S. canicula. Conclusion: Our analyses reveal considerable differences in the formation of the pectoral and pelvic musculatures in S.