Physiology of Elasmobranch Fishes: Structure and Interaction with Environment

Robert E. Shadwick, Anthony Peter Farrell, Colin Brauner, Colin J. Brauner

• Publisher: Academic Press
• Year: 2015
• Print ISBN:
  9780128012895
• eBook ISBN:
  9780128014431
• Topic: Technology & Engineering
• Subtopic: Physiology
• Index: Technology & Engineering

Fish Physiology: Physiology of Elasmobranch Fishes, Volume 34A is a useful reference for fish physiologists, biologists, ecologists, and conservation biologists. Following an increase in research on elasmobranchs due to the plight of sharks in today's oceans, this volume compares elasmobranchs to other groups of fish, highlights areas of interest for future research, and offers perspective on future problems. Covering measurements and lab-and-field based studies of large pelagic sharks, this volume is a natural addition to the renowned Fish Physiology series. - Provides needed comprehensive content on the physiology of elasmobranchs - Offers a systems approach between structure and interaction with the environment and internal physiology - Contains contributions by leading experts in their respective fields, under the guidance of internationally recognized and highly respected editors - Highlights areas of interest for future research, including perspective on future problems

1

Elasmobranchs and Their Extinct Relatives: Diversity, Relationships, and Adaptations Through Time

Philippe Janvier and Alan Pradel

1. Introduction

2. Systematic and Phylogenetic Framework of Chondrichthyan Diversity

2.1. Names, Taxa, and Characters

2.2. Chondrichthyan Diversity and Interrelationships

3. Environments and Adaptations

4. Conclusion

Current views about chondrichthyan phylogeny and systematics are briefly reviewed, with particular reference to the living and fossil taxa that are, or have been, once referred to as “elasmobranchs.” Recent reviews of early fossil chondrichthyans suggest that the last common ancestor of the living elasmobranchs and holocephalans probably lived by the end of the Devonian period, about 370–380 Myr ago, but a number of Paleozoic, shark-like chondrichthyans are currently regarded as stem chondrichthyans that diverged before the last common ancestor of all living taxa. Stem holocephalans display an amazing morphological diversity that reflects adaptations to very diverse benthic habitats. By contrast, both stem elasmobranchs and stem chondrichthyans are generally shark-like and were probably adapted to a pelagic mode of life. The earliest evidence for tessellated prismatic calcified cartilage, the “signature” of euchondrichthyans (i.e., all chondrichthyans which possess tessellated calcified prismatic cartilage), is about 400 Myr old, but scales and teeth tentatively assigned to chondrichthyans have been recorded from earlier periods. The “acanthodians,” a paraphyletic ensemble of Paleozoic fishes known since about 445 Myr are currently regarded as possible stem chondrichthyans that diverged before the rise of euchondrichthyans.

Keywords

Elasmobranchii; Holocephali; Chondrichthyes; paleontology; phylogeny; relationships; diversity; adaptations

Current views about chondrichthyan phylogeny and systematics are briefly reviewed, with particular reference to the living and fossil taxa that are, or have been, once referred to as “elasmobranchs.” Recent reviews of early fossil chondrichthyans suggest that the last common ancestor of the living elasmobranchs and holocephalans probably lived by the end of the Devonian period, about 370–380 Myr ago, but a number of Paleozoic, shark-like chondrichthyans are currently regarded as stem chondrichthyans that diverged before the last common ancestor of all living taxa. Stem holocephalans display an amazing morphological diversity that reflects adaptations to very diverse benthic habitats. By contrast, both stem elasmobranchs and stem chondrichthyans are generally shark-like and were probably adapted to a pelagic mode of life. The earliest evidence for tessellated prismatic calcified cartilage, the “signature” of euchondrichthyans (i.e., all chondrichthyans which possess tessellated calcified prismatic cartilage), is about 400 Myr old, but scales and teeth tentatively assigned to chondrichthyans have been recorded from earlier periods. The “acanthodians,” a paraphyletic ensemble of Paleozoic fishes known since about 445 Myr are currently regarded as possible stem chondrichthyans that diverged before the rise of euchondrichthyans.

1 Introduction

Living elasmobranchs (in current sense) include sharks (squalomorphs and galeomorphs) and batomorphs (sawfishes, rays, skates, and torpedoes), and are the sister group of holocephalans (chimaeroids). Elasmobranchs and holocephalans are gathered into a higher group, the chondrichthyans (cartilaginous fishes). The idea that elasmobranchs and even all chondrichthyans are “primitive” jawed vertebrates (gnathostomes) stems from the conception of vertebrate systematics and evolution that progressively arose in the second half of the nineteenth century. The lack of an extensive bony skeleton in chondrichthyans was regarded as “primitive” because it is also the condition observed in living cyclostomes (hagfishes and lampreys), whose lack of jaws also suggested an earlier divergence in vertebrate history. Other arguments in favor of the “primitiveness” of elasmobranchs were based on their anatomy, notably the classical resemblance and presumed serial homology of their mandibular and hyoid arches with the series of the gill arches, already noticed by early anatomists (e.g., Owen, 1866), and later supported by the discovery of early, fossil shark-like elasmobranchs (Dean, 1909). The reputedly “primitive” anatomy of elasmobranchs has also justified extensive studies of their physiology, with the aim of reconstructing the hypothetical phenotypic condition for the last common ancestor of all gnathostomes. Ultimately, all these data were expected to help our understanding of the adaptive context of the evolutionary processes that has subsequently led to the rise of bony fishes (osteichthyans), including their limbed members, the tetrapods (terrestrial vertebrates). However, as the knowledge of living elasmobranch biology was accumulating, paleontologists provided an increasingly large assembly of anatomical data on various extinct Paleozoic jawed and jawless fishes, which revolutionized the interpretation of character distributions (Janvier 1996, 2015; Brazeau and Friedman, 2015). Notably, they showed that bone was largely present in both the dermal skeleton and endoskeleton of armored jawless fishes, or “ostracoderms,” thereby suggesting that bone preceded the rise of jaws long before the divergence of cartilaginous fishes. Whence, then, the chondrichthyans? Among early vertebrate paleontologists, Stensiö (1969) proposed a surprising theory about the polyphyletic origin of chondrichthyans, in which elasmobranchs, rays, and holocephalans derived independently from three groups of placoderms (an ensemble of Paleozoic, armored jawed fishes) by progressive loss of their ability to produce endoskeletal bone and breakdown of their dermal armor (suggested by the fact that the scales of the earliest chondrichthyans were not placoid, but possessed a growing bony base bearing many separate odontodes). Stensiö's view was obviously based on some striking anatomical resemblances between the shark's braincase to that of certain placoderms (the arthrodires), and by some superficial, convergent overall morphologies shared by rays and holocephalans with other groups of placoderms (the rhenanids and ptyctodonts, respectively). This theory is now dismissed, but provided interesting insights into the possibility that the lack of bone in chondrichthyans could be a derived condition. Placoderms are currently regarded as a paraphyletic array of stem jawed vertebrates that have successively diverged before the last common ancestor of chondrichthyans and osteichthyans (Brazeau and Friedman, 2015). Chondrichthyans, in turn, are currently thought to be most closely related to some of the somewhat shark-like Paleozoic fishes, referred to as “acanthodians,” whose phylogenetic position has been long erratic (Brazeau, 2009; Brazeau and Friedman, 2015), although they were already viewed as stem chondrichthyans by Goodrich (1909).

Most of what we know about fossil chondrichthyans is based on isolated teeth or fin spines, and such remains, albeit poorly informative, nevertheless document relatively well the history of the groups that still have extant relatives and possess closely similar elements of the dermal skeleton. However, the elucidation of the relationships of the major extinct chondrichthyan taxa essentially rests on a small number of specimens (generally braincases, but sometimes articulated skeletons) preserved in three dimensions thanks to the thin layer of prismatic calcified cartilage that lines their surface. Such exceptional preservations are particularly welcome for reconstructing the internal anatomy of the braincase in stem chondrichthyans; that is, chondrichthyans that are neither elasmobranchs, nor holocephalans, but already posses prismatic calcified cartilage, the “signature” of the group, and are gathered with the latter into a group called euchondrichthyans (in order to distinguish them from other, possible stem chondrichthyans that do not possess this unique type of hard tissue, such as “acanthodians”) (Pradel et al., 2014). Such material, which can now be studied by nondestructive techniques of X-ray computed microtomography, provides invaluable information about the anatomy and relationships of these early forms and may help our understanding of what the last common ancestor of chondrichthyans and osteichthyans could have looked like, notably by revealing uniquely derived characters shared by the two groups, but which have been subsequently lost or strongly modified in either of them.

Skeletal characters sometimes provide information that is indirectly useful to physiologists, such as features linked to particular functions of the labyrinth (e.g., low-frequency phonoreception; Maisey and Lane, 2010). However, fossil chondrichthyans may also provide information about certain soft tissues (e.g., muscles, blood vessels, kidneys, brain, coloration patterns; Dean, 1909; Zangerl, 1981; Maisey, 1989; Grogan and Lund, 2000; Pradel et al., 2009) that are exceptionally preserved under certain environmental conditions and as an effect of bacterially induced mineralization. Such soft-tissue data, long regarded as trivial by paleontologists, can now be studied in great detail, thereby allowing further inferences about the biology of these fossil organisms. The goal of this introduction is to provide physiologists with a systematic framework against which functional inferences may be tested in order to enlighten the evolutionary history of the interactions of chondrichthyans with the environments throughout time (remarkable reconstructions of the early chondrichthyans and their environment can be found in a semi-popular book by Cuny and Beneteau, 2013).

2 Systematic and Phylogenetic Framework of Chondrichthyan Diversity

2.1 Names, Taxa, and Characters

The name Elasmobranchii (elasmobranchs) was erected by Bonaparte (1838) for an ensemble of living fishes that in fact included the “Selacha” (sharks and rays) and the “Holocephala” (chimaeras). Bonaparte's “Elasmobranchii” was thus identical in contents to Huxley's (1880) “Chondrichthyes” (chondrichthyans), which is currently widely used because it allowed the inclusion of a number of shark-like fossil groups whose affinities to either modern “sharks” or modern chimaeras were obscure (see review in Maisey, 2012). Chondrichthyan, elasmobranch, and holocephalan monophyly is currently well corroborated by phenotypic and phylogenomic data (Maisey et al., 2004; Heinicke et al., 2009). When dealing with phylogenies and classifications that include fossil taxa, it is necessary to define clearly the contents of the taxa that are characterized by unique features (autapomorphies). Therefore, the notions of total-, stem-, and crown group are important to define the degree of generality of the characters and avoid referring a member of a stem group to a crown group because of overall resemblance, as it has often happened for some Paleozoic “sharks” (for the definition of the notion of total-, stem- and crown-groups, see Janvier, 2007). Current chondrichthyan phylogenies are relatively well corroborated, in particular for the crown groups of elasmobranchs and holocephalans (i.e., the last common ancestor of a group and all its living and fossil descendants). This concerns essentially Cenozoic and Mesozoic taxa, but a number of Paleozoic taxa regarded as stem elasmobranchs or stem holocephalans still remain of debated relationships. In addition, some Paleozoic taxa are now quite clearly identified as stem chondrichthyans (Pradel et al., 2011, 2014; Maisey et al., 2014), but the last common ancestor to crown chondrichthyans is regarded as late Devonian (about 370 Myr) in age, on the basis of the earliest evidence for stem holo...

Table of contents

• Cover image
• Title page
• Table of Contents
• Copyright
• Contents of Physiology of Elasmobranch Fishes: Internal Processes, Volume 34B
• Contributors
• Preface
• List of Abbreviations
• 1. Elasmobranchs and Their Extinct Relatives: Diversity, Relationships, and Adaptations Through Time
• 2. How Elasmobranchs Sense Their Environment
• 3. Elasmobranch Gill Structure
• 4. Functional Anatomy and Biomechanics of Feeding in Elasmobranchs
• 5. Elasmobranch Muscle Structure and Mechanical Properties
• 6. Swimming Mechanics and Energetics of Elasmobranch Fishes
• 7. Reproduction Strategies
• 8. Field Studies of Elasmobranch Physiology
• Index
• Other Volumes in the Fish Physiology Series