The Morphology and Evolution of the Ventral Gill Arch Skeleton in Batoid Fishes (Chondrichthyes: Batoidea)

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The Morphology and Evolution of the Ventral Gill Arch Skeleton in Batoid Fishes (Chondrichthyes: Batoidea) <oologzcal Journal ofhe Lznnean SocieQ (199l), 102: 75-100. With 10 figures The morphology and evolution of the ventral gill arch skeleton in batoid fishes (Chondrichthyes: Batoidea) TSUTOMU MIYAKE AND JOHN D. MCEACHRAN Department of Biology, Dalhousie University, Halifax, Nova Scotia, B3H 431, Canada and Department of Wildlqe and Fisheries Sciences, Texas AdYM University, College Station, TX 77843, U.S.A. Received July 1988, reuised manuscript accepted October I990 The ventral gill arch skeleton was examined in some representatives of batoid fishes. The homology of the components was elucidated by comparing similarities and differences among the components of the ventral gill arches in chondrichthyans, and attempts were made to justify the homology by giving causal mechanisms of chondrogenrsis associated with the vcntral gill arch skeleton. The ceratohyal is present in some batoid fishes, and its functional replacement, the pseudohyal, seems incomplete in most groups of batoid fishes, except in stingrays. The medial fusion of the pseudohyal with successive ceratobranchials occurs to varying degrees among stingray groups. The ankylosis between the last two ceratobranchials occurs uniquely in stingrays, and it serves as part of the insertion of the last pair of coracobranchialis muscles. ‘The basihyal is possibly independently lost in electric rays, the stingray genus Urotrygan (except U. dauzesz) and pelagic myliohatoid stingrays. ‘I‘he first hypobranchial is oriented anteriorly or anteromedially, and it varies in shape and size among batoid fishes. It is represented by rami projecting posterolaterally from the basihyal in sawfishes, guitarfishes and skates. It consists of a small piece ofcartilage which extends anteromedially from the medial end of the first ccratobranchial in electric rays. It is a large cartilaginous plate in most of stingrays. It is absent in pelagic myliobatoid stingrays. The remaining hypobranchial cartilages also vary in shape and size among batoid fishes. Torpedo and possibly the Jurassic Be1emnobali.r and Spathobatis possess the generalized or typical chondrichthyan ventral gill arch structure in which the hypobranchials form a X-shaped pattern. In the electric ray Hypnos and narkinidid and narcinidid electric rays, the hypobranchial components are oriented longitudinally along the mid-portion of the ventral gill arches. They form a single cartilaginous plate in the narkinidid electric rays, Narcine and Diplobatis. In guitarfishes and skates, the second hypobranchial is unspecialized, and in skates, it does not have a direct contact with the second ceratobranchial. In both groups, the third and fourth hypobranchials are composed of a small cartilage which forms a passage for the afferent branches of the ventral aorta and serve as part of the insertion of the coracobranchialis muscle. In sawfishes and stingrays, the hypobranchials appear to be included in the medial platc. In sawfishes, the second and third components separately chondrify in adults, but the fourth component appears to be fused with the middle medial plate. In stingrays, a large medial plate appears to include thr second through to the last hypohranchial and most of the basibranchial copulae. The medial plate probahly develops independently in sawfishes and stingrays. Because thc last basibranchial copula appears to be a composite of one to two hypobranchials and at least two basibranchial copulae, the medial plate may be formed by several developmental processes of chondrogenesis. More detailed comparative anatomical and developmental studies are needed to unveil morphogenesis and patternings of the ventral gill arch skeleton in batoid fishes. KEY WORDS:-- Batoids - ehondrichthyans ~ ontogeny - homology 75 0024-4082/91/050075 + 26 $03.00/0 0 1991 The Linnean Society of London 76 T. MIYAKE AND J. D. MCEACHRAN CONTENTS Introduction .................... 76 Material and methods .................76 Development of ventral gill arch skeleton .............77 Ventral gill arch skeleton in holocephalans and sharks ..........78 Ventral gill arch skeleton in batoid fishes .............81 Discussion .................... 93 Acknowledgements ..................97 References .................... 98 Abbreviations used in figures ................99 Appendix ..................... 99 INTRODUCTION Batoid fishes comprise 400 to 500 living species in five subgroups (pristoids, rhinobatoids, rajoids, torpedinoids and myliobatoids) within recent elasmobranchs (Compagno, 1973, 1977; McEachran, 1982). The earliest known batoids are rhinobatoid-like fishes from the Lower Jurassic (Saint-Seine, 1949; Cappetta, 1987; Carroll, 1988). Anatomical studies of the group have been extensive (Gegenbaur, 1865, 1872; Parker, 1879; Garman, 1913; Allis, 1923), and they have provided an important basis for studying phylogenetic interrelationships of batoid fishes (White, 1937). However, recent phylogenetic studies have not produced a consensus of interrelationships of the taxa (Maisey, 1984a, 1986) and there is disagreement as to whether batoid fishes are monophyletic (Compagno, 1973, 1977) or diphyletic (Jarvik, 1977). Lack of consensus among these studies (Compagno, 1973, 1977; Heemstra & Smith, 1980; Maisey, 1984b) appears to be due in part to their lack of comprehensive anatomical comparisons of the major taxa. The gill arch skeleton has been well studied in fishes and has been used to infer phylogenetic interrelationships of osteichthyan fishes (Nelson, 1969; Lauder & Liem, 1983). In chondrichthyans, the ventral gill arch skeleton has been described by Gegenbaur ( 1872), Garman ( 19 13), Holmgren ( 1940, 1941), Hamdy (1956, 1957, 1973) and Hamdy & Khalil (1973). These studies revealed that chondrichthyans are unique in possessing a C-shaped pattern of hypobranchial cartilages and that the pattern of batoid fishes is considerably modified from the generalized condition in chondrichthyans (Nelson, 1969; Miyake, 1988). Thus, specialization of the ventral gill arch skeleton in batoid fishes makes it difficult to homologize the components throughout chondrichthyans (Miyake, 1988). Preliminary results of studies of the ventral gill arch skeleton in batoid fishes are presented here. Attempts were made to trace homologous components of the ventral gill arch skeleton throughout the major taxa of batoid fishes, and causal explanations of developmental processes are given to support our discussions on homology of the ventral gill arch skeleton in batoid fishes. MATERIAL AND METHODS Structures of the ventral gill arch skeleton in chondrichthyans were examined from gross dissections, from cleared and stained specimens and from X-radiographs of specimens. Embryos and juvenile specimens were cleared and double-stained with Alcian Blue (Kodak 14091) and Alizarin (Alizarin sodium EVOLU'I'ION OF BATOIDS 77 sulphonate, Fisher Scientific Company) for cartilage and calcified cartilage, respectively (Dingerkus & Uhler, 1977). All specimens illustrated in the figures are listed in the Appendix. Homologies of the components of the ventral gill arch skeleton in batoid fishes were elucidated by comparing the components of the ventral gill arch skeleton among chondrichthyans. Causal explanations of developmental processes are offered to support our perceptions of homology of the ventral gill arch skeleton in chondrichthyans based on our conceptual framework of homology (Miyake el al., in press). DEVELOPMENT OF VENTRAL GILL ARCH SKELETON The pattern of the ventral gill arch skeleton in recent elasmobranchs can be elucidated from the blastematic condensation and subsequent chondrification of the skeleton in the spiny dogfish Squalus acanthias embryos (Holmgren, 1940; El-Toubi, 1952; Jollie, 1971) (Fig. 1) and in some embryos of batoid fishes (Holmgren, 1940). The first horizontal blastema forms medially between the blastemas of the presumptive ceratohyal or pseudohyal. Because this portion of the skeleton articulates with the ceratohyal in adult holocephalans and sharks (Fig. 2) and with either the ceratohyal or pseudohyal in adult batoid fishes, it is considered to be the basihyal component. However, it either comprises the basihyal and the first hypobranchial (Miyake, 1988) or merely represents the first basibranchial copula (Nelson, 1969). According to Jollie (1971) the lateral longitudinal portion of the blastema is a component of the presumptive first hypobranchial. This blastema is continuous with the diagonally oriented first ceratobranchial blastema. In most sharks, the first pair of hypobranchials is either the distolateral ramus of the basihyal, as seen in Squalus acanthias, or is not chondrified. In some sharks the first hypobranchial is represented by a small piece of cartilage between the basihyal and the first ceratobranchial. In batoid fishes, the first pair of hypobranchials is either the distolateral ramus of the basihyal or a separate cartilage. In the 50 mm embryo of Raja (Raja)clavata, the basihyal and the first pair of hypobranchials are present as separate components A B C D Figure 1. Early development of the ventral gill arch skeleton in Squalus aranlhias Linnacus. A, 35-37 mm TL; B, 48 mm TL; C, 67 mm TL; D, 102 mm TL. A from Jollie (1971: fig. 8); B from Holmgren (1940: fig. 68); C and D from El-Toubi (1952: figs 3, 5). The star indicates where the blastema of the first hypobranchial develops. Arrow heads indicate a topographic relationship of hypobranchials with their corresponding ceratobranchials. 7a T. MIYAKE AND J. D. MCEACHRAN (Holmgren, 1940: fig. 138). At later
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