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THE SKELETON | Cartilaginous Fish Skeletal Anatomy
MUSCLES, SKELETON, SKIN, AND MOVEMENT
The Skeleton
Contents Cartilaginous Fish Skeletal Anatomy Cartilaginous Fish Skeletal Tissues Bony Fish Skeleton
Cartilaginous Fish Skeletal Anatomy KM Claeson, University of Texas at Austin, Austin, TX, USA MN Dean, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany ª 2011 Elsevier Inc. All rights reserved.
Introduction General Anatomy Sharks
Glossary Anterior Toward the front or head. In fishes, the term rostral can be substituted for anterior. Autostyly Jaw condition where palatoquadrate is strongly attached to the ethmoid region and directly fused to the auditory region of the chondrocranium. The hyomandibula does not participate in jaw suspension. Ceratotrichia Thin, keratinous fin rays, originating from large collagen fibers, and forming the distal-most elements in the fins of cartilaginous fishes (contrast with actinotrichia). Distal The furthest from the central nervous system, or in the direction away from the central brain. Receptors are the most distal retinal neurons. Dorsal Toward the top or back of the fish (the dorsal surface). Endoskeleton The skeletal system formed by all skeletal elements that are nondermal in developmental origin. Euhyostyly Jaw condition when the palatoquadrate has no ligamentous connection to the chondrocranium and does not contact it anteriorly, but only posteriorly via the hyomandibula (as in batoids). Extant A species or clade, etc., that is still in existence. Holostyly Jaw condition when palatoquadrate is fused to chondrocranium (as in Holocephalii).
Batoids Chimaeroids Further Reading
Hyostyly Jaw condition when the palatoquadrate articulates with the chondrocranium, but is not strongly attached or fused (as in most sharks). Lateral In a direction away, or a position far from the body’s midline (e.g., your eyes are lateral on your face and lateral to your nose). Medial In a direction toward, or a position near the body’s midline (e.g., your nose is medial on your face and medial to your eyes). Neoselachii A clade of cartilaginous fishes that includes extant sharks and batoids, but not chimaeroids. Posterior Toward the rear, or behind. In fishes, the term caudal can be substituted for posterior. Proximal Nearest to the central nervous system, or in the direction toward the central brain. Ganglion cells are the most proximal retinal neurons. Skeletal element An individual portion in a cartilaginous skeleton, analogous to individual bones in the skeleton of a bony vertebrate. Spiracle An external opening near the eye in elasmobranch fishes that communicates to the throat, via a passage between the hyomandibula and cranium.
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Suspensorium The chain of cartilages, including the hyomandibula that suspends the jaws from the chondrocranium.
Synarcual A series of fused vertebrae. Ventral Toward the bottom or belly of the fish (the ventral surface).
Introduction From the outside, for the most part, the members from each of the three major extant groups of the Chondrichthyes look unmistakably distinct; a reef shark could never be
confused with a barndoor skate or a white-spotted chi maera. Of course, these differences are reflected broadly in the skeleton; however, certain aspects of skeletal design are conserved among these fishes (Figures 1 and 2). The article The Skeleton: Cartilaginous Fish Skeletal Dorsal fin
(a)
Eye
Rostrum
External gills
Pectoral fin
Pelvic fin
(b) Dorsal fin
Nasal capsule
Chondrocranium
Rostrum
Upper jaw (palatoquadrate) Pectoral fin
Lower jaw (Meckel’s cartilage)
Scapulocoracoid
Caudal fin Ischiopubadic bar (pelvic girdle)
10 cm
Gill arches (posterior visceral arches)
(c)
(d)
10 cm Figure 1 The body plan of sharks: (a) external anatomy of silky shark, Carcharhinus falciformis, in lateral view; (b) skeletal anatomy of silky shark, Carcharhinus falciformis, in lateral view; (c) closeup of branchial basket in lateral view; and (d) close-up of branchial basket in ventral view. Skeleton was prepared by dissection and maceration before it was dried and mounted. Branchial basket collapsed during drying and is slightly deformed.
The Skeleton | Cartilaginous Fish Skeletal Anatomy
Rostrum (a)
(b)
Eye
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Nasal capsule Chondrocranium Upper jaw (palatoquadrate) Rostrum Antorbital cartilage Lower jaw (Meckel’s cartilage) Hyomandibula
Pectoral fin
Synarcual 5th Ceratobranchial Propterygium Mesopterygium Pelvic fin
Pectoral arch (suprascapular)
1st Dorsal fin 2nd Dorsal fin
1 cm
Ischiopubadic bar (pelvic girdle)
10 cm
(c)
Scapulocoracoid (pectoral girdle) Metapterygium
1st Dorsal fin 2nd Dorsal fin Thorn
Mouth
(d)
Gill slits
Compound 1st radial
Upper jaw (palatoquadrate) Eye Nasal capsule Lower jaw (Meckel’s cartilage) Rostrum Hyomandibula Gill arches
Pectoral fin 5th ceratobranchial Propterygium Mesopterygium Scapulocoracoid (pectoral girdle) Metapterygium Corocoid bar Compound 1st radial Ischiopubadic bar (pelvic girdle)
Pelvic fin
10 cm
1 cm
Figure 2 The body plan of batoids: (a) external anatomy of the barndoor skate, Dipturus laevis, in dorsal view; (b) skeletal anatomy of a skate, Raja sp., in dorsal view. Skeleton was prepared by clearing and staining. Chemicals are used to digest the muscle fibers and make them clear. Alcian blue stains for uncalcified cartilage and Alizerin red stains for calcified (mineralized and hard) cartilage. The skeleton in this specimen is fairly well developed; (c) external anatomy of the cownose stingray, Rhinoptera bonasus; (d) skeletal anatomy of the eagle ray, Myliobatis sp. Skeleton was prepared by clearing and staining. This is a young specimen; the skeleton is not very well calcified yet, although all major parts have developed. (b) Courtesy of President and Fellows of Harvard College.
Tissues discusses conservation and variation at the tissue level; here, we show how these different types of cartilages are assembled to form the skeletons of chondrichthyan fishes. A simplified chondrichthyan skeleton can be divided into three distinct parts – the axial, visceral, and the appendicular skeletons – that are discussed below. To understand the similarities and differences among taxonomic groups, it will help to think about the skeleton in pieces, just do as most anatomists, functional morphol ogists, and paleontologists. Researchers can compare these pieces through broad taxonomic surveys to gain
insight into chondrichthyan evolution and how certain morphologies might be tied to certain ecologies.
General Anatomy Axial Skeleton The axial skeleton includes the skull, vertebral column, and ribs. The skull of all chondrichthyan fishes is called the chondrocranium and is essentially a cartilaginous box containing the brain and other important sense organs. Although the adult chondrocranium is a single
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piece of cartilage with definable regions, it is assembled early in embryonic development through the coales cence of separate cartilages. The embryonic basal and ethmoid plates form the anterior wall and floor of the chondrocranium; the occipital arches form the posterior wall of the chondrocranium; and the orbital cartilages contribute to the lateral walls of the chondrocranium. Although the complete chondrocranium varies in size and shape among species, there are generally identifi able regions that are conserved across the different groups of chondrichthyans and can be used to make broad comparisons among groups. From roughly rostral to caudal, these are the rostrum, nasal capsule, antorbi tal process, orbital region, otic capsules, and occipital condyles (Figure 3). Posterior to the chondrocranium, the remainder of the axial skeleton is the vertebral column, composed of indi viduated vertebrae. There are three primary segments of a vertebra in chondrichthyans: dorsally, the paired basi dorsals, contributing to the neural arches that protect the spinal cord; ventrally, the paired basiventrals, contribut ing to hemal arches that house blood vessels; and, in the middle, the centrum. The vertebral centrum is a spoolshaped structure that acts as the primary load-bearing structure and to which the neural and hemal arches that protect the important surrounding soft tissues are attached. Although the arches are made of tessellated cartilage, as in the rest of the skeleton, the centra are
areolar cartilage; this is apparently the only place in the body where this tissue is found (see also The Skeleton: Cartilaginous Fish Skeletal Tissues). The centra are arranged so that the top and bottom of the spool face rostrally and caudally. Numerous centra are then strung together to form the spinal column, resembling many spools of thread strung together on a string. In the center of each centrum are the remains of the notochord, a stiff but flexible rod that serves as the embryonic foundation for the vertebral column. Among the different elasmo branch taxa, the shape of the persistent notochord in cross section is highly variable in fully developed centra, a result of differential folding as the areolar cartilage grows around it. That shape is consistent within certain groups of elasmobranchs and can be used diagnostically to distinguish between the vertebrae of different groups (e.g., those of sharks and batoids, Figure 4).
Visceral Arches Beneath the chondrocranium is the visceral skeleton, which includes the upper and lower jaws (palatoquadrate and Meckel’s cartilage), hyoid, and gill arch cartilages. These collected structures are called the visceral arches and can be thought of as jointed, symmetrical loops/ semicircles of cartilaginous elements, arranged in rostro caudal (anteroposterior) series, and supporting the breathing and feeding structures of the head. The joints
Otic
capsule
(a) Ethmoid region
Rostrum
Nasal capsule
Orbital region
(b)
(c) Rostrum
Rostrum Nasal capsule
Nasal capsule
Ethmoid region
Orbital region
Orbital region
Eye stalk Otic capsule Occipital condyles
Occipital condyles
Figure 3 The chondrocranium of a skate, Leucoraja ocellata: (a) lateral view; (b) dorsal view; (c) ventral view.
The Skeleton | Cartilaginous Fish Skeletal Anatomy (a)
B
A
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C
ee
(b)
A B Tessellated
cartilage
D E
Notochord
Uncalcified
cartilage
C
Figure 4 Cross section of vertebrae showing folding pattern of notochord in the centrum: (a) shark vertebrae, Stegostoma tigrinum, 660 mm long, �6 (A, vertebra from region of pectoral girdle; B, vertebra from post-cloacal region; C, vertebra from region half-way along the caudal fin); (b) batoid vertebrae, Rhinobatos granulatus, �3 (A, caudal vertebra, taken a short distance in front of the first dorsal fin; B, vertebra from the base of the caudal fin; C, from half-way between the base of the caudal fin and the extreme caudal end of the vertebral column; D, from half-way between C and the extreme hind end of the vertebral column; E, vertebra, a short distance behind D). Tessellated cartilage crust surrounds uncalcified cartilage. Notochord present as spokes (shark) or clover pattern (batoid). Modified from Ridewood (1921) On the calcification of the vertebral centra in sharks and rays. Philosophical Transactions of the Royal Society of London, Series B 210: 311–407.
in the arches allow them to expand and collapse, making breathing and feeding possible. The mandibular arch (the first visceral arch) forms the jaw in chondrichthyans. It is divided into two parts, the dorsal palatoquadrate (upper jaw) and the ventral Meckel’s cartilage (lower jaw). The palatoquadrate and Meckel’s cartilage changed shape many times during the evolution of the Chondrichthyes. This is correlated to a change in the way the jaw is attached to the chondrocranium. The earliest chondrichthyans from the Paleozoic had a massive palatoquadrate that was firmly attached to the chondrocranium and was not mobile. In the modern
Holocephalii, the jaws are also firmly in place, an arrangement is known as holostyly, which gave the group its name. The holostylic arrangement in Holocephalii is only convergent with the Paleozoic condition, and therefore these similar features are not derived from the same common ancestor. This Paleozoic type of jaw connection is known as autostylic. As chondrichthyans evolved, the palatoquadrate became less firmly connected with the chondrocranium and more mobile. There is evidence that these changes are correlated with the evolution of the variety of feeding styles seen in modern species.
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The hyoid arch (the second visceral arch) is posterior to and closely associated with the mandibular arch. It is also divided into dorsal and ventral components. The hyomandibula is the sole dorsal element and the ventral components are the ceratohyal and basihyal. The remain der of the visceral arches are known collectively as the gill arches or branchial basket (Figures 1(c) and 1(d)). The latter descriptor relates to the shape into which the series of U-shaped arches conform. As they are adjoined by ventral branchial cartilages, they form a structure that looks like the ribcage of a wooden ship, with the longer dorsal elements converging and connecting ventrally. The gill arches are the support system for the soft struc tures involved in gill ventilation and respiration. With this knowledge of the relative arrangements of the skeletal structures that support the mouth, throat, and gills, we can now understand the general pathway of water in a breathing shark; this pathway is likely, in general, true for chondrichthyans; however, it has yet to be demonstrated in chimaeroids. The chondrichthyans (as well as other fishes) extract oxygen when they bring water in and pass it over their gills. Water enters the orobranchial chamber through the jaws (visceral arch 1) or the spiracle (bounded posteriorly by visceral arch 2), typically as the floor of the chamber is depressed through ventral movement of the ventral hyoid and branchial arches. This water is pushed or drawn over the gills, and oxygen and carbon dioxide are exchanged across a net work of blood vessels found within the soft gill tissues. The water, then oxygen-depleted, passes out of the gill chamber by way of gill slit openings (the spaces between the branchial arches). In the sharks, the gill slits are lateral on the body, whereas in batoids the gill slits are ventral. The gill openings in chimaera are covered by a fleshy operculum with a single posteroventral exit (see also The Muscles: Bony Fish Cranial Muscles). Appendicular Skeleton The appendicular skeleton includes the cartilages of the paired fins and the limb girdles. In general, skeletal ele ments are smaller and more flexible the more distal they are in the appendicular skeleton. This is correlated with a tendency for proximal elements to be involved in sup porting the more distal elements of the appendicular skeleton, and those distal elements to be more involved in locomotion. The pectoral (forelimb) and pelvic (hindlimb) girdles are the support structures for the paired fins. The major ity of taxa have a U-shaped pectoral girdle, with each arm of the girdle pointing dorsally and comprised of coracoids, scapulae, and suprascapulae. The coracoids and scapulae often fuse into a scapulocoracoid, a term sometimes used in place of pectoral girdle. Suprascapulae are often small and might be absent from some groups. In certain
chondrichthyans, the pectoral girdle is tightly associated with the axial skeleton (i.e., the arms of the girdle articu late with the vertebral column). In contrast, the pelvic girdle is composed of a single ischiopubadic bar, is always completely free of the axial skeleton, and is closely asso ciated with the cloaca. The pectoral and pelvic fins are attached to the ventro lateral edges of their respective girdles. The components of these fins, from proximal to distal, are flat basal pterygial cartilages (two to four in the pectoral fin and two in the pelvic fin), rod-like radial cartilages, and long, parallel fin rays called ceratotrichia. Radial cartilages vary greatly in overall length and number depending on the taxon; for example, they form the majority of the pectoral fins in batoids, which tend to have reduced numbers of ceratotrichia. Fin rays form the jointed and flexible flap ping portion of the fin, which are referred to as actinotrichia (a derivation of dermatotrichia) in bony ray-finned fishes. In chondrichthyans, the fin rays are known as ceratotrichia because they are made of elastoidin (not bone), which has properties that are a combination of collagen and elastin. Ceratotrichia are homologous to actinotrichia in bony fishes.
Sharks The term shark is a common name that refers to a large taxonomic sampling of chondrichthyans (approximately 403 of 970 chondrichthyans, �41.5%) that are neither batoids nor chimaeroids. In general, sharks have a long body, and the paired fins are relatively short compared with the body (Figure 1). However, there is a lot of variation in the shark skeleton. For instance, the goblin shark, Mitsukurina, has a skull with an enormous rostrum that protrudes far anteriorly over a highly protrusible mouth while the angel shark, Squatina, has a short snout and relatively fixed mouth, but its fins extend anteriorly and resemble wings. In this section, we base our description of a generalized shark skeleton on the common dogfish shark, Squalus. Axial Skeleton In the ethmoid region of sharks, a short, broad median rostrum is situated anteromedially to the paired nasal capsules, giving many sharks a bullet-shaped body. The nasal capsules are round and situated anteroventrally. Posterior to the nasal capsules are very large orbits, broad cavities in the chondrocranium that house the eyes. The boundaries of the orbit are defined by the antorbital process, supraorbital crest, and postorbital pro cess of the chondrocranium. The orbit is open ventrally. The interorbital space (the space between the eyes on the dorsal surface of the chondrocranium) is slightly narrower than the broad ethmoid region and roughly the same size as the optic region.
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Visceral Arches
Axial Skeleton
In most modern sharks, the palatoquadrate articulates with the chondrocranium, but not firmly, a condition called hyostyly. The hyoid cartilages (hyomandibula and ceratohyal) attach to the palatoquadrate and Meckel’s cartilage, forming a movable suspensorium. The third hyoid cartilage, a large median basihyal, articu lates at its lateral edges with the distal ends of the left and right ceratohyals.
Batoids often possess elaborate rostral and/or antorbital cartilages projecting off the anterior ethmoid region of the chondrocranium (Figure 3). The rostral and antorbital cartilages are highly variable among batoids and play a large role in determining the overall shape of the body disk. In rajiforms (skates), rhinobatiforms (guitarfishes), and pristioforms (sawfish) there is an anteriorly projecting ros tral cartilage that is continuous with the ethmoid region and articulates with one or two rostral appendages distally. In myliobatiforms (stingrays) and torpediniforms (electric rays), the projecting rostral cartilage is absent or miniscule. The antorbital cartilages of torpediniforms, however, are paired and greatly expanded compared to the antorbital cartilages of rajiforms. Antorbital cartilages articulate with the nasal capsule proximally. Nasal capsules are round to oval to kidney-bean shaped and project ventrolaterally. In some batoids, the pectoral fin articulates with the distal margins of the antorbital cartilage. Posterior to the nasal capsule is the orbit. The interorbital space is narrower than the internasal space. The otic capsules are posterior to the orbit and are only slightly wider than the interorbital space. All batoids share a modified vertebral element known as the synarcual. This is not to be confused with the chimaeroid synarcual (discussed below). The batoid synarcual cartilage is a long tube-like element, hypothe sized to be the fusion of the first several vertebrae. Little is known about the synarcual cartilage; however, new research indicates that only neural arches contribute to the tube-like portion in which the spinal cord sits. Anteriorly, the synarcual contacts the chondrocranium. Posteriorly, it is forked and is closely associated with isolated centra made of areolar cartilage. In stingrays, a second, posterior synarcual is present.
Appendicular Skeleton The pectoral girdle in sharks includes fused coracoid and scapular cartilages (the scapulocoracoid) and suprascapular cartilages. The ventromedial portion of the scapulocora coid is the coracoid bar. The scapular process projects posterodorsally from the lateral end of the coracoid bar. The boundary between the coracoid and scapula occurs roughly where the proximal portion of the basal ptergygia of the pectoral fin articulates with the scapulocoracoid. The pectoral fin skeleton is composed of three short basal pterygia: the proptergygium (anteriormost), mesoptery gium (medial), and metapterygium (posteriormost). Long radial cartilages extend from the distal ends of all three basal pterygia. Cartilaginous ceratotrichia comprise the distalmost portion of the pectoral fin.
Batoids Batoids represent over half of the extant species diversity of Neoselachii. Except in a small handful of cases, they are easily distinguished from other chondrichthyans by their flat bodies (Figure 2). Compared to the generalized shark body plan, the paired pectoral fins are immense and stretched anteriorly and posteriorly, then effectively joined to the sides of the head; this creates a dorsoven trally flattened body disk anterior to the pelvic girdle. However, within the distinctive depressiform body plan of batoids, there is considerable variation, especially in the shape of the body disk and the stoutness of the tail, which are often representative of swimming mode and ecology. For instance, electric rays are usually nearly circular, a function of the lateral displacement of the pectoral fins by the electric organs. This organization makes their pectoral fins less useful for locomotion; instead they swim by a more shark-like wagging of the tail. Many benthic stingrays also have round body disks, although they lack electric organs; these species locomote along the bottom by undulating the margins of their wings. Some of the largest stingrays, on the other hand, have diamond-shaped bodies with massive, powerful fins for swimming and whip-like, nonpropulsive tails.
Visceral Arches Batoids share a jaw morphology known as euhyostyly. In this condition, the proximal hyomandibula and distal cer atoyal are still present, as in sharks. However, euhyostyly permits more freedom of movement of the hyomandibula relative to the ceratohyal, and – due to the comparative lack of ligamentous associations – of the jaws relative to the cranium. This type of suspensorium allows a great range of motion in the mouth of rays, with many species able to protrude their jaws up to 50% of their head length and some capable of twice this. The ceratohyal is secon darily free from the suspensorium and contributes to the gill arches. The basihyal, which is large and easily identi fied in sharks, is fused with the first hypobranchial cartilages in batoids to create a horizontal bar on the floor of the throat, anteromedial to the remaining visceral cartilages. The gill arches are wedged between the pec toral fins and axial skeleton, and are sometimes tightly
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connected to the synarcual. External gill slits are ventral to the body in batoids. Appendicular Skeleton In most batoids, the pectoral girdle and fins form the dominant structures for locomotion; this is in contrast to those species with thick shark-like tails that swim by lateral movements of the tail (e.g., sawfishes, guitarfishes, and electric rays). The different cartilages of the girdle fuse together to create a sturdy U-shaped scapulocoracoid car tilage. Dorsally, the scapulocoracoid articulates with the vertebral column via the suprascapula. This means that the pectoral girdle is the shape of a ring, unlike in other chondrichthyans where the U is not completely closed dorsally. The length of the pectoral fins of Raja and other batoids is often half their total body length or more. The cartilages that create the base of the wing-like structure (pro-, meso-, and metapterygia) are expansive, especially the pro- and metapterygia. In some species, the propterygia is so long that it articulates with the antorbital cartilage anteriorly. Pectoral fins of skates and rays consist of a series of parallel radial cartilages that emanate from the basal pterygia of the pectoral girdle. The structural reinforce ment of individual radials, as well as the arrangement and bracing of joints between them, is variable among different groups of batoids and is reflective of locomotory life style (e.g., oscillatory vs. undulatory swimming).
Chimaeroids Chimaeroids have large heads, long snouts, and tube-like bodies that taper to small and sometimes whip-like tails. They are sister group to the elasmobranchs, but exter nally, they bear little resemblance to their shark and batoid relatives. Axial Skeleton If batoid heads are flat (depressiform), those of chimae roids are narrow (compressiform). Paired lateral rostral rods that lie medial to the nasal capsules extend anteriorly from the ethmoid region. This entire area, anterior to the orbits and surrounding the rostral rods, is packed with soft tissues and as such, the rostrum is soft and flexible. A single median rostral rod is slightly dorsal to the lateral rostral rods, which supports the tip of the nose and is sometimes exceedingly long (e.g., in the Rhinochimaeridae). The nasal capsules are bulbous and project laterally from the anteroventral portion of the ethmoid region. The chimaeroid face is shorter than that of most of the other chondrichthyans: the orbit is posterior to the ethmoid region, anterior to the brain, and dorsal to
the paired olfactory tracts. The orbit is bounded ventrally by a suborbital ridge, anteriorly by the antorbital crest, and posteriorly by the postorbital. The left and right orbits are separated by a thin wall of connective tissue, which forms the interorbital septum. Posterior to the orbit in all chimaeroids is the otic region. The semicircular canals of the ear (see also Hearing and Lateral Line: The Ear and Hearing in Sharks, Skates, and Rays) bulge on the dorsal surface of the chondrocranium. Posteriorly, the otic region extends to the prominent occipital crest. Posterior to the chondrocranium is the chimaeroid synarcual. The synarcual is loosely articulated with the occipital region. The synarcual is a cartilaginous plate formed by the fusion of the first 10 vertebral segments. On the dorsal edge of the synarcual is an articulation sur face for the basal cartilage of the first dorsal fin and the fin spine. The chimaeroid synarcual is not tightly associated with the suprascapular cartilage and the pectoral girdle, which is in contrast to the condition in batoids. Visceral Arches The suspension and morphology of the jaws of chimae roids is unique among extant Chondrichthyes. Unlike the looser jaw suspensions of the elasmobranch fishes, in chimaeroids the palatoquadrate is fused with the chon drocranium and the hyoid is nonsuspensory (i.e., it does not form a movable suspensorium for the upper and lower jaws). In addition, whereas all other chondrichthyans replace their teeth, the broad, hypermineralized tooth plates of chimaeroids are permanent. The Meckel’s cartilage (lower jaw) is fused at the symphysis, forming a single, U-shaped element. Appendicular Skeleton The pectoral girdle is positioned just posterior to the neurocranium. The paired halves of the pectoral girdle are fused at the symphysis. The ventralmost portion of the pectoral girdle is the coracoid region. The dorsal portion is the elongate scapular process. This distal por tion of the scapular process points anterodorsally to lie lateral to the base of the chimaeroid synarcual. The pectoral fins are dibasal (with two basal cartilages) and articulate with the glenoid fossa on the posterior edge of the coracoid by way of the basal cartilages (propterygium and metapterygium). These pterygia support the radials of the pectoral fin. The pelvic fins lie along the ventral surface of the body. The single basipterygium of the pelvic fin is a flat ovoid cartilage. The anterior margin of the pectoral fin is defined by the basipterygial process, which is formed by the fusion of the proximalmost radials and the basipterygium. Additional radials articulate with the basipterygium and are situated parallel to the basip terygial process.
The Skeleton | Cartilaginous Fish Skeletal Anatomy See also: Aquaculture: Physiology of Fish in Culture Environments. Brain and Nervous System: Functional Morphology of the Brains of Cartilaginous Fishes. Buoyancy, Locomotion, and Movement in Fishes: Feeding Mechanics; Paired Fin Swimming; Undulatory Swimming. Design and Physiology of the Heart Cardiac Anatomy in Fishes. Detection and Generation of Electric Signals: Electric Organs. Hearing and Lateral Line: Auditory System Morphology; The Ear and Hearing in Sharks, Skates, and Rays. Integrated Function and Control of the Gut: Barrier Function of the Gut. Smell, Taste, and Chemical Sensing: Morphology of the Gustatory (Taste) System in Fishes; Morphology of the Olfactory (Smell) System in Fishes. The Muscles: Cartilaginous Fishes Cranial Muscles. The Skeleton: Cartilaginous Fish Skeletal Tissues.
Further Reading Claeson KM (2008) Variation of the synarcual in the California Ray, Raja inornata (Elasmobranchii: Rajidae). Acta Geologica Polonica 58: 121–126.
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Daniel JF (1934) The Elasmobranch Fishes. Berkeley, CA: University of California Press. Dean MN and Motta PJ (2004) Anatomy and functional morphology of the feeding apparatus of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea). Journal of Morphology 262: 462–483. Didier DA (1995) Phylogenetic systematics of extant chimaeroid fishes. American Museum Novitates 3119: 1–86. Garman S (1913) The Plagiostomia (Sharks, Skates, and Rays), Memoirs of the Museum of Comparative Zoology at Harvard College. Cambridge, MA: Harvard University. Goodrich ES (1958) Studies on the Structure and Development of Vertebrates. New York: Dover. Holmgren N (1941) Studies on the head in fishes embryological, morphological, and phylogenetical researches. Part II: Comparative anatomy of the adult selachian skull with remarks on the dorsal fins in sharks. Acta Zoologica (Stockholm) 22: 1–100. Kemp NE (1977) Banding pattern and fibrillogenesis of ceratotrichia in shark fins. Journal of Morphology 154: 187–203. Liem KF, Bemis WE, Walter WF, Jr., and Grande L (2001) Functional Anatomy of the Vertebrates: An Evolutionary Perspective, 3rd edn. Orlando, FL: Harcourt College Publishers. Ridewood WG (1921) On the calcification of the vertebral centra in sharks and rays. Philosophical Transactions of the Royal Society of London, Series B 210: 311–407. Schaefer JT and Summers AP (2005) Batoid wing skeletal structure: Novel morphologies, mechanical implications, and phylogenetic patterns. Journal of Morphology 264: 298–313.
The Skeleton
Contents Cartilaginous Fish Skeletal Anatomy Cartilaginous Fish Skeletal Tissues Bony Fish Skeleton
Cartilaginous Fish Skeletal Anatomy KM Claeson, University of Texas at Austin, Austin, TX, USA MN Dean, Max Planck Institute of Colloids and Interfaces, Potsdam, Germany ª 2011 Elsevier Inc. All rights reserved.
Introduction General Anatomy Sharks
Glossary Anterior Toward the front or head. In fishes, the term rostral can be substituted for anterior. Autostyly Jaw condition where palatoquadrate is strongly attached to the ethmoid region and directly fused to the auditory region of the chondrocranium. The hyomandibula does not participate in jaw suspension. Ceratotrichia Thin, keratinous fin rays, originating from large collagen fibers, and forming the distal-most elements in the fins of cartilaginous fishes (contrast with actinotrichia). Distal The furthest from the central nervous system, or in the direction away from the central brain. Receptors are the most distal retinal neurons. Dorsal Toward the top or back of the fish (the dorsal surface). Endoskeleton The skeletal system formed by all skeletal elements that are nondermal in developmental origin. Euhyostyly Jaw condition when the palatoquadrate has no ligamentous connection to the chondrocranium and does not contact it anteriorly, but only posteriorly via the hyomandibula (as in batoids). Extant A species or clade, etc., that is still in existence. Holostyly Jaw condition when palatoquadrate is fused to chondrocranium (as in Holocephalii).
Batoids Chimaeroids Further Reading
Hyostyly Jaw condition when the palatoquadrate articulates with the chondrocranium, but is not strongly attached or fused (as in most sharks). Lateral In a direction away, or a position far from the body’s midline (e.g., your eyes are lateral on your face and lateral to your nose). Medial In a direction toward, or a position near the body’s midline (e.g., your nose is medial on your face and medial to your eyes). Neoselachii A clade of cartilaginous fishes that includes extant sharks and batoids, but not chimaeroids. Posterior Toward the rear, or behind. In fishes, the term caudal can be substituted for posterior. Proximal Nearest to the central nervous system, or in the direction toward the central brain. Ganglion cells are the most proximal retinal neurons. Skeletal element An individual portion in a cartilaginous skeleton, analogous to individual bones in the skeleton of a bony vertebrate. Spiracle An external opening near the eye in elasmobranch fishes that communicates to the throat, via a passage between the hyomandibula and cranium.
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Suspensorium The chain of cartilages, including the hyomandibula that suspends the jaws from the chondrocranium.
Synarcual A series of fused vertebrae. Ventral Toward the bottom or belly of the fish (the ventral surface).
Introduction From the outside, for the most part, the members from each of the three major extant groups of the Chondrichthyes look unmistakably distinct; a reef shark could never be
confused with a barndoor skate or a white-spotted chi maera. Of course, these differences are reflected broadly in the skeleton; however, certain aspects of skeletal design are conserved among these fishes (Figures 1 and 2). The article The Skeleton: Cartilaginous Fish Skeletal Dorsal fin
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Eye
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10 cm Figure 1 The body plan of sharks: (a) external anatomy of silky shark, Carcharhinus falciformis, in lateral view; (b) skeletal anatomy of silky shark, Carcharhinus falciformis, in lateral view; (c) closeup of branchial basket in lateral view; and (d) close-up of branchial basket in ventral view. Skeleton was prepared by dissection and maceration before it was dried and mounted. Branchial basket collapsed during drying and is slightly deformed.
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Rostrum (a)
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Nasal capsule Chondrocranium Upper jaw (palatoquadrate) Rostrum Antorbital cartilage Lower jaw (Meckel’s cartilage) Hyomandibula
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Figure 2 The body plan of batoids: (a) external anatomy of the barndoor skate, Dipturus laevis, in dorsal view; (b) skeletal anatomy of a skate, Raja sp., in dorsal view. Skeleton was prepared by clearing and staining. Chemicals are used to digest the muscle fibers and make them clear. Alcian blue stains for uncalcified cartilage and Alizerin red stains for calcified (mineralized and hard) cartilage. The skeleton in this specimen is fairly well developed; (c) external anatomy of the cownose stingray, Rhinoptera bonasus; (d) skeletal anatomy of the eagle ray, Myliobatis sp. Skeleton was prepared by clearing and staining. This is a young specimen; the skeleton is not very well calcified yet, although all major parts have developed. (b) Courtesy of President and Fellows of Harvard College.
Tissues discusses conservation and variation at the tissue level; here, we show how these different types of cartilages are assembled to form the skeletons of chondrichthyan fishes. A simplified chondrichthyan skeleton can be divided into three distinct parts – the axial, visceral, and the appendicular skeletons – that are discussed below. To understand the similarities and differences among taxonomic groups, it will help to think about the skeleton in pieces, just do as most anatomists, functional morphol ogists, and paleontologists. Researchers can compare these pieces through broad taxonomic surveys to gain
insight into chondrichthyan evolution and how certain morphologies might be tied to certain ecologies.
General Anatomy Axial Skeleton The axial skeleton includes the skull, vertebral column, and ribs. The skull of all chondrichthyan fishes is called the chondrocranium and is essentially a cartilaginous box containing the brain and other important sense organs. Although the adult chondrocranium is a single
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piece of cartilage with definable regions, it is assembled early in embryonic development through the coales cence of separate cartilages. The embryonic basal and ethmoid plates form the anterior wall and floor of the chondrocranium; the occipital arches form the posterior wall of the chondrocranium; and the orbital cartilages contribute to the lateral walls of the chondrocranium. Although the complete chondrocranium varies in size and shape among species, there are generally identifi able regions that are conserved across the different groups of chondrichthyans and can be used to make broad comparisons among groups. From roughly rostral to caudal, these are the rostrum, nasal capsule, antorbi tal process, orbital region, otic capsules, and occipital condyles (Figure 3). Posterior to the chondrocranium, the remainder of the axial skeleton is the vertebral column, composed of indi viduated vertebrae. There are three primary segments of a vertebra in chondrichthyans: dorsally, the paired basi dorsals, contributing to the neural arches that protect the spinal cord; ventrally, the paired basiventrals, contribut ing to hemal arches that house blood vessels; and, in the middle, the centrum. The vertebral centrum is a spoolshaped structure that acts as the primary load-bearing structure and to which the neural and hemal arches that protect the important surrounding soft tissues are attached. Although the arches are made of tessellated cartilage, as in the rest of the skeleton, the centra are
areolar cartilage; this is apparently the only place in the body where this tissue is found (see also The Skeleton: Cartilaginous Fish Skeletal Tissues). The centra are arranged so that the top and bottom of the spool face rostrally and caudally. Numerous centra are then strung together to form the spinal column, resembling many spools of thread strung together on a string. In the center of each centrum are the remains of the notochord, a stiff but flexible rod that serves as the embryonic foundation for the vertebral column. Among the different elasmo branch taxa, the shape of the persistent notochord in cross section is highly variable in fully developed centra, a result of differential folding as the areolar cartilage grows around it. That shape is consistent within certain groups of elasmobranchs and can be used diagnostically to distinguish between the vertebrae of different groups (e.g., those of sharks and batoids, Figure 4).
Visceral Arches Beneath the chondrocranium is the visceral skeleton, which includes the upper and lower jaws (palatoquadrate and Meckel’s cartilage), hyoid, and gill arch cartilages. These collected structures are called the visceral arches and can be thought of as jointed, symmetrical loops/ semicircles of cartilaginous elements, arranged in rostro caudal (anteroposterior) series, and supporting the breathing and feeding structures of the head. The joints
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Figure 3 The chondrocranium of a skate, Leucoraja ocellata: (a) lateral view; (b) dorsal view; (c) ventral view.
The Skeleton | Cartilaginous Fish Skeletal Anatomy (a)
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Figure 4 Cross section of vertebrae showing folding pattern of notochord in the centrum: (a) shark vertebrae, Stegostoma tigrinum, 660 mm long, �6 (A, vertebra from region of pectoral girdle; B, vertebra from post-cloacal region; C, vertebra from region half-way along the caudal fin); (b) batoid vertebrae, Rhinobatos granulatus, �3 (A, caudal vertebra, taken a short distance in front of the first dorsal fin; B, vertebra from the base of the caudal fin; C, from half-way between the base of the caudal fin and the extreme caudal end of the vertebral column; D, from half-way between C and the extreme hind end of the vertebral column; E, vertebra, a short distance behind D). Tessellated cartilage crust surrounds uncalcified cartilage. Notochord present as spokes (shark) or clover pattern (batoid). Modified from Ridewood (1921) On the calcification of the vertebral centra in sharks and rays. Philosophical Transactions of the Royal Society of London, Series B 210: 311–407.
in the arches allow them to expand and collapse, making breathing and feeding possible. The mandibular arch (the first visceral arch) forms the jaw in chondrichthyans. It is divided into two parts, the dorsal palatoquadrate (upper jaw) and the ventral Meckel’s cartilage (lower jaw). The palatoquadrate and Meckel’s cartilage changed shape many times during the evolution of the Chondrichthyes. This is correlated to a change in the way the jaw is attached to the chondrocranium. The earliest chondrichthyans from the Paleozoic had a massive palatoquadrate that was firmly attached to the chondrocranium and was not mobile. In the modern
Holocephalii, the jaws are also firmly in place, an arrangement is known as holostyly, which gave the group its name. The holostylic arrangement in Holocephalii is only convergent with the Paleozoic condition, and therefore these similar features are not derived from the same common ancestor. This Paleozoic type of jaw connection is known as autostylic. As chondrichthyans evolved, the palatoquadrate became less firmly connected with the chondrocranium and more mobile. There is evidence that these changes are correlated with the evolution of the variety of feeding styles seen in modern species.
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The hyoid arch (the second visceral arch) is posterior to and closely associated with the mandibular arch. It is also divided into dorsal and ventral components. The hyomandibula is the sole dorsal element and the ventral components are the ceratohyal and basihyal. The remain der of the visceral arches are known collectively as the gill arches or branchial basket (Figures 1(c) and 1(d)). The latter descriptor relates to the shape into which the series of U-shaped arches conform. As they are adjoined by ventral branchial cartilages, they form a structure that looks like the ribcage of a wooden ship, with the longer dorsal elements converging and connecting ventrally. The gill arches are the support system for the soft struc tures involved in gill ventilation and respiration. With this knowledge of the relative arrangements of the skeletal structures that support the mouth, throat, and gills, we can now understand the general pathway of water in a breathing shark; this pathway is likely, in general, true for chondrichthyans; however, it has yet to be demonstrated in chimaeroids. The chondrichthyans (as well as other fishes) extract oxygen when they bring water in and pass it over their gills. Water enters the orobranchial chamber through the jaws (visceral arch 1) or the spiracle (bounded posteriorly by visceral arch 2), typically as the floor of the chamber is depressed through ventral movement of the ventral hyoid and branchial arches. This water is pushed or drawn over the gills, and oxygen and carbon dioxide are exchanged across a net work of blood vessels found within the soft gill tissues. The water, then oxygen-depleted, passes out of the gill chamber by way of gill slit openings (the spaces between the branchial arches). In the sharks, the gill slits are lateral on the body, whereas in batoids the gill slits are ventral. The gill openings in chimaera are covered by a fleshy operculum with a single posteroventral exit (see also The Muscles: Bony Fish Cranial Muscles). Appendicular Skeleton The appendicular skeleton includes the cartilages of the paired fins and the limb girdles. In general, skeletal ele ments are smaller and more flexible the more distal they are in the appendicular skeleton. This is correlated with a tendency for proximal elements to be involved in sup porting the more distal elements of the appendicular skeleton, and those distal elements to be more involved in locomotion. The pectoral (forelimb) and pelvic (hindlimb) girdles are the support structures for the paired fins. The major ity of taxa have a U-shaped pectoral girdle, with each arm of the girdle pointing dorsally and comprised of coracoids, scapulae, and suprascapulae. The coracoids and scapulae often fuse into a scapulocoracoid, a term sometimes used in place of pectoral girdle. Suprascapulae are often small and might be absent from some groups. In certain
chondrichthyans, the pectoral girdle is tightly associated with the axial skeleton (i.e., the arms of the girdle articu late with the vertebral column). In contrast, the pelvic girdle is composed of a single ischiopubadic bar, is always completely free of the axial skeleton, and is closely asso ciated with the cloaca. The pectoral and pelvic fins are attached to the ventro lateral edges of their respective girdles. The components of these fins, from proximal to distal, are flat basal pterygial cartilages (two to four in the pectoral fin and two in the pelvic fin), rod-like radial cartilages, and long, parallel fin rays called ceratotrichia. Radial cartilages vary greatly in overall length and number depending on the taxon; for example, they form the majority of the pectoral fins in batoids, which tend to have reduced numbers of ceratotrichia. Fin rays form the jointed and flexible flap ping portion of the fin, which are referred to as actinotrichia (a derivation of dermatotrichia) in bony ray-finned fishes. In chondrichthyans, the fin rays are known as ceratotrichia because they are made of elastoidin (not bone), which has properties that are a combination of collagen and elastin. Ceratotrichia are homologous to actinotrichia in bony fishes.
Sharks The term shark is a common name that refers to a large taxonomic sampling of chondrichthyans (approximately 403 of 970 chondrichthyans, �41.5%) that are neither batoids nor chimaeroids. In general, sharks have a long body, and the paired fins are relatively short compared with the body (Figure 1). However, there is a lot of variation in the shark skeleton. For instance, the goblin shark, Mitsukurina, has a skull with an enormous rostrum that protrudes far anteriorly over a highly protrusible mouth while the angel shark, Squatina, has a short snout and relatively fixed mouth, but its fins extend anteriorly and resemble wings. In this section, we base our description of a generalized shark skeleton on the common dogfish shark, Squalus. Axial Skeleton In the ethmoid region of sharks, a short, broad median rostrum is situated anteromedially to the paired nasal capsules, giving many sharks a bullet-shaped body. The nasal capsules are round and situated anteroventrally. Posterior to the nasal capsules are very large orbits, broad cavities in the chondrocranium that house the eyes. The boundaries of the orbit are defined by the antorbital process, supraorbital crest, and postorbital pro cess of the chondrocranium. The orbit is open ventrally. The interorbital space (the space between the eyes on the dorsal surface of the chondrocranium) is slightly narrower than the broad ethmoid region and roughly the same size as the optic region.
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In most modern sharks, the palatoquadrate articulates with the chondrocranium, but not firmly, a condition called hyostyly. The hyoid cartilages (hyomandibula and ceratohyal) attach to the palatoquadrate and Meckel’s cartilage, forming a movable suspensorium. The third hyoid cartilage, a large median basihyal, articu lates at its lateral edges with the distal ends of the left and right ceratohyals.
Batoids often possess elaborate rostral and/or antorbital cartilages projecting off the anterior ethmoid region of the chondrocranium (Figure 3). The rostral and antorbital cartilages are highly variable among batoids and play a large role in determining the overall shape of the body disk. In rajiforms (skates), rhinobatiforms (guitarfishes), and pristioforms (sawfish) there is an anteriorly projecting ros tral cartilage that is continuous with the ethmoid region and articulates with one or two rostral appendages distally. In myliobatiforms (stingrays) and torpediniforms (electric rays), the projecting rostral cartilage is absent or miniscule. The antorbital cartilages of torpediniforms, however, are paired and greatly expanded compared to the antorbital cartilages of rajiforms. Antorbital cartilages articulate with the nasal capsule proximally. Nasal capsules are round to oval to kidney-bean shaped and project ventrolaterally. In some batoids, the pectoral fin articulates with the distal margins of the antorbital cartilage. Posterior to the nasal capsule is the orbit. The interorbital space is narrower than the internasal space. The otic capsules are posterior to the orbit and are only slightly wider than the interorbital space. All batoids share a modified vertebral element known as the synarcual. This is not to be confused with the chimaeroid synarcual (discussed below). The batoid synarcual cartilage is a long tube-like element, hypothe sized to be the fusion of the first several vertebrae. Little is known about the synarcual cartilage; however, new research indicates that only neural arches contribute to the tube-like portion in which the spinal cord sits. Anteriorly, the synarcual contacts the chondrocranium. Posteriorly, it is forked and is closely associated with isolated centra made of areolar cartilage. In stingrays, a second, posterior synarcual is present.
Appendicular Skeleton The pectoral girdle in sharks includes fused coracoid and scapular cartilages (the scapulocoracoid) and suprascapular cartilages. The ventromedial portion of the scapulocora coid is the coracoid bar. The scapular process projects posterodorsally from the lateral end of the coracoid bar. The boundary between the coracoid and scapula occurs roughly where the proximal portion of the basal ptergygia of the pectoral fin articulates with the scapulocoracoid. The pectoral fin skeleton is composed of three short basal pterygia: the proptergygium (anteriormost), mesoptery gium (medial), and metapterygium (posteriormost). Long radial cartilages extend from the distal ends of all three basal pterygia. Cartilaginous ceratotrichia comprise the distalmost portion of the pectoral fin.
Batoids Batoids represent over half of the extant species diversity of Neoselachii. Except in a small handful of cases, they are easily distinguished from other chondrichthyans by their flat bodies (Figure 2). Compared to the generalized shark body plan, the paired pectoral fins are immense and stretched anteriorly and posteriorly, then effectively joined to the sides of the head; this creates a dorsoven trally flattened body disk anterior to the pelvic girdle. However, within the distinctive depressiform body plan of batoids, there is considerable variation, especially in the shape of the body disk and the stoutness of the tail, which are often representative of swimming mode and ecology. For instance, electric rays are usually nearly circular, a function of the lateral displacement of the pectoral fins by the electric organs. This organization makes their pectoral fins less useful for locomotion; instead they swim by a more shark-like wagging of the tail. Many benthic stingrays also have round body disks, although they lack electric organs; these species locomote along the bottom by undulating the margins of their wings. Some of the largest stingrays, on the other hand, have diamond-shaped bodies with massive, powerful fins for swimming and whip-like, nonpropulsive tails.
Visceral Arches Batoids share a jaw morphology known as euhyostyly. In this condition, the proximal hyomandibula and distal cer atoyal are still present, as in sharks. However, euhyostyly permits more freedom of movement of the hyomandibula relative to the ceratohyal, and – due to the comparative lack of ligamentous associations – of the jaws relative to the cranium. This type of suspensorium allows a great range of motion in the mouth of rays, with many species able to protrude their jaws up to 50% of their head length and some capable of twice this. The ceratohyal is secon darily free from the suspensorium and contributes to the gill arches. The basihyal, which is large and easily identi fied in sharks, is fused with the first hypobranchial cartilages in batoids to create a horizontal bar on the floor of the throat, anteromedial to the remaining visceral cartilages. The gill arches are wedged between the pec toral fins and axial skeleton, and are sometimes tightly
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connected to the synarcual. External gill slits are ventral to the body in batoids. Appendicular Skeleton In most batoids, the pectoral girdle and fins form the dominant structures for locomotion; this is in contrast to those species with thick shark-like tails that swim by lateral movements of the tail (e.g., sawfishes, guitarfishes, and electric rays). The different cartilages of the girdle fuse together to create a sturdy U-shaped scapulocoracoid car tilage. Dorsally, the scapulocoracoid articulates with the vertebral column via the suprascapula. This means that the pectoral girdle is the shape of a ring, unlike in other chondrichthyans where the U is not completely closed dorsally. The length of the pectoral fins of Raja and other batoids is often half their total body length or more. The cartilages that create the base of the wing-like structure (pro-, meso-, and metapterygia) are expansive, especially the pro- and metapterygia. In some species, the propterygia is so long that it articulates with the antorbital cartilage anteriorly. Pectoral fins of skates and rays consist of a series of parallel radial cartilages that emanate from the basal pterygia of the pectoral girdle. The structural reinforce ment of individual radials, as well as the arrangement and bracing of joints between them, is variable among different groups of batoids and is reflective of locomotory life style (e.g., oscillatory vs. undulatory swimming).
Chimaeroids Chimaeroids have large heads, long snouts, and tube-like bodies that taper to small and sometimes whip-like tails. They are sister group to the elasmobranchs, but exter nally, they bear little resemblance to their shark and batoid relatives. Axial Skeleton If batoid heads are flat (depressiform), those of chimae roids are narrow (compressiform). Paired lateral rostral rods that lie medial to the nasal capsules extend anteriorly from the ethmoid region. This entire area, anterior to the orbits and surrounding the rostral rods, is packed with soft tissues and as such, the rostrum is soft and flexible. A single median rostral rod is slightly dorsal to the lateral rostral rods, which supports the tip of the nose and is sometimes exceedingly long (e.g., in the Rhinochimaeridae). The nasal capsules are bulbous and project laterally from the anteroventral portion of the ethmoid region. The chimaeroid face is shorter than that of most of the other chondrichthyans: the orbit is posterior to the ethmoid region, anterior to the brain, and dorsal to
the paired olfactory tracts. The orbit is bounded ventrally by a suborbital ridge, anteriorly by the antorbital crest, and posteriorly by the postorbital. The left and right orbits are separated by a thin wall of connective tissue, which forms the interorbital septum. Posterior to the orbit in all chimaeroids is the otic region. The semicircular canals of the ear (see also Hearing and Lateral Line: The Ear and Hearing in Sharks, Skates, and Rays) bulge on the dorsal surface of the chondrocranium. Posteriorly, the otic region extends to the prominent occipital crest. Posterior to the chondrocranium is the chimaeroid synarcual. The synarcual is loosely articulated with the occipital region. The synarcual is a cartilaginous plate formed by the fusion of the first 10 vertebral segments. On the dorsal edge of the synarcual is an articulation sur face for the basal cartilage of the first dorsal fin and the fin spine. The chimaeroid synarcual is not tightly associated with the suprascapular cartilage and the pectoral girdle, which is in contrast to the condition in batoids. Visceral Arches The suspension and morphology of the jaws of chimae roids is unique among extant Chondrichthyes. Unlike the looser jaw suspensions of the elasmobranch fishes, in chimaeroids the palatoquadrate is fused with the chon drocranium and the hyoid is nonsuspensory (i.e., it does not form a movable suspensorium for the upper and lower jaws). In addition, whereas all other chondrichthyans replace their teeth, the broad, hypermineralized tooth plates of chimaeroids are permanent. The Meckel’s cartilage (lower jaw) is fused at the symphysis, forming a single, U-shaped element. Appendicular Skeleton The pectoral girdle is positioned just posterior to the neurocranium. The paired halves of the pectoral girdle are fused at the symphysis. The ventralmost portion of the pectoral girdle is the coracoid region. The dorsal portion is the elongate scapular process. This distal por tion of the scapular process points anterodorsally to lie lateral to the base of the chimaeroid synarcual. The pectoral fins are dibasal (with two basal cartilages) and articulate with the glenoid fossa on the posterior edge of the coracoid by way of the basal cartilages (propterygium and metapterygium). These pterygia support the radials of the pectoral fin. The pelvic fins lie along the ventral surface of the body. The single basipterygium of the pelvic fin is a flat ovoid cartilage. The anterior margin of the pectoral fin is defined by the basipterygial process, which is formed by the fusion of the proximalmost radials and the basipterygium. Additional radials articulate with the basipterygium and are situated parallel to the basip terygial process.
The Skeleton | Cartilaginous Fish Skeletal Anatomy See also: Aquaculture: Physiology of Fish in Culture Environments. Brain and Nervous System: Functional Morphology of the Brains of Cartilaginous Fishes. Buoyancy, Locomotion, and Movement in Fishes: Feeding Mechanics; Paired Fin Swimming; Undulatory Swimming. Design and Physiology of the Heart Cardiac Anatomy in Fishes. Detection and Generation of Electric Signals: Electric Organs. Hearing and Lateral Line: Auditory System Morphology; The Ear and Hearing in Sharks, Skates, and Rays. Integrated Function and Control of the Gut: Barrier Function of the Gut. Smell, Taste, and Chemical Sensing: Morphology of the Gustatory (Taste) System in Fishes; Morphology of the Olfactory (Smell) System in Fishes. The Muscles: Cartilaginous Fishes Cranial Muscles. The Skeleton: Cartilaginous Fish Skeletal Tissues.
Further Reading Claeson KM (2008) Variation of the synarcual in the California Ray, Raja inornata (Elasmobranchii: Rajidae). Acta Geologica Polonica 58: 121–126.
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Daniel JF (1934) The Elasmobranch Fishes. Berkeley, CA: University of California Press. Dean MN and Motta PJ (2004) Anatomy and functional morphology of the feeding apparatus of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea). Journal of Morphology 262: 462–483. Didier DA (1995) Phylogenetic systematics of extant chimaeroid fishes. American Museum Novitates 3119: 1–86. Garman S (1913) The Plagiostomia (Sharks, Skates, and Rays), Memoirs of the Museum of Comparative Zoology at Harvard College. Cambridge, MA: Harvard University. Goodrich ES (1958) Studies on the Structure and Development of Vertebrates. New York: Dover. Holmgren N (1941) Studies on the head in fishes embryological, morphological, and phylogenetical researches. Part II: Comparative anatomy of the adult selachian skull with remarks on the dorsal fins in sharks. Acta Zoologica (Stockholm) 22: 1–100. Kemp NE (1977) Banding pattern and fibrillogenesis of ceratotrichia in shark fins. Journal of Morphology 154: 187–203. Liem KF, Bemis WE, Walter WF, Jr., and Grande L (2001) Functional Anatomy of the Vertebrates: An Evolutionary Perspective, 3rd edn. Orlando, FL: Harcourt College Publishers. Ridewood WG (1921) On the calcification of the vertebral centra in sharks and rays. Philosophical Transactions of the Royal Society of London, Series B 210: 311–407. Schaefer JT and Summers AP (2005) Batoid wing skeletal structure: Novel morphologies, mechanical implications, and phylogenetic patterns. Journal of Morphology 264: 298–313.