ebin.pub_vertebrate-life-10th-edition-9781605356075-9781605357218-1605356077-1605357219 [116-122].pdf

CHAPTER 6 T he appearance of jaws and internally supported paired appendages (described in Chapter 3) were the basis for a new radiation of vertebrates with diverse predatory and locomotor specializations. The extant cartilaginous fishes—sharks, rays, and chimaeras—are the descendants of one clade o...

CHAPTER 6 T he appearance of jaws and internally supported paired appendages (described in Chapter 3) were the basis for a new radiation of vertebrates with diverse predatory and locomotor specializations. The extant cartilaginous fishes—sharks, rays, and chimaeras—are the descendants of one clade of this radiation. Chondrichthyans are often thought of as primitive fishes, but the more we come to understand them, the more apparent it becomes that they are highly derived in their own fashion, even if they lack many of the derived features of osteichthyans. Most modern chondrichthyans are marine, although there are a handful of freshwater sharks and rays. 6.1 Chondrichthyes: The Cartilaginous Fishes Chondrichthyans make a definite first appearance in the fossil record in the Early Devonian, although isolated scales and possible teeth appear in Ordovician sediments, and undoubted chondrichthyan scales are known from the early Silurian. The oldest articulated fossil (i.e., a fossil with the bones connected) of a chondrichthyan is Doliodus problematicus from the Early Devonian of Canada. Although sharklike in appearance, Doliodus was not a neoselachian; that group (which contains the extant sharks) is unknown until the Mesozoic. Chondrichthyans can be divided into two groups (Figures 6.1 and 6.2), although the fossil lineages make this subdivision a little more complex. Elasmobranchii (Greek elasma, “plate”; branchia, “gills”) have multiple gill openings on each side of the head. This group includes the extant Neoselachii (Greek neos, “new”; New Latin selachos, “cartilaginous fish”): sharks (mostly torpedo-shaped forms with five to seven gill openings on each side of the head) and rays (including skates) (dorsoventrally flattened forms with five pairs of gill openings on the ventral surface Smokeybjb/CC BY-SA 3.0 Radiation and Diversification of Chondrichthyes of the head). Neoselachians are also characterized by an independently mobile upper jaw (hyostyly; see Chapter 7 for a discussion of chondrichthyan jaws). The sharklike form was probably the ancestral chondrichthyan condition. Holocephali (Greek holos, “whole, entire”; kephale, “head”) is named for the undivided appearance of the head that results from having a single external gill opening. Individual gill slits are covered by an operculum formed by soft tissue that is supported on the hyoid arch by an opercular cartilage. The common names of extant holocephalans—chimaeras, rabbitfishes, ratfishes, and ghost sharks—reflect their bizarre forms. They have a fishlike body and a long, flexible tail. Some species have a head that resembles a caricature of a rabbit, with big eyes and broad tooth plates that look a bit like a rabbit’s teeth. In contrast to the mobile upper jaw of extant elasmobranchs, the upper jaw of chimaeras and their fossil relatives is fused with the skull (holostyly, a condition convergent with that of humans). In addition, the dorsal elements of the hyoid arch are separate (pharygeohyal and epihyal, equivalent to the pharyngeobranchial and epibranchial elements of the gill arches) and are not fused together into a hyomandibula, as in other extant gnathostomes (see Chapter 3). Distinctive characters of chondrichthyans Chondrichthyans are defined by two unique characters: A cartilaginous skeleton of individual small calciumcontaining units with a distinctive microstructure called tesserate prismatic calcifications. The presence of pelvic claspers in males, which are used for internal fertilization. (You saw in Chapter 3 that some placoderms had pelvic claspers, but these were not homologous with the pelvic claspers of chondrichthyans.) A cartilaginous endoskeleton is the ancestral condition in vertebrates, seen today in the hagfishes and lampreys. Some 96  CHAPTER 6 Radiation and Diversification of Chondrichthyes Batoidea (skates and rays) “Acanthodians” Iniopterygii SELACHII NEOSELACHII 359 419 Ordovician 444 Stem chondrichthyans Placoderms Devonian 299 Silurian Paleozoic Carboniferous Permian 252 “Paraselachians” (Paraselachiamorpha) Triassic 201 Stem elasmobranchs Jurassic Mesozoic 145 Sarcopterygii (lobe-finned fishes and tetrapods) Cretaceous Hybodonta 66 Squalomorphii Galeomorphii “Holocephalans” Holocephalomorpha (including chimaeras) Neogene 23 Paleogene Cenozoic Present 2.6 Actinopterygii (ray-finned fishes) Sharks EUSELACHII HOLOCEPHALI (EUCHONDROCEPHALI) ELASMOBRANCHII EUCHONDRICHTHYES ? OSTEICHTHYES CHONDRICHTHYES EUGNATHOSTOMATA 485 Ma GNATHOSTOMATA Figure 6.1 Phylogenetic relationships of cartilaginous fishes. Tree showing the general diversification of jawed vertebrates, Pough Vertebrate Life 10E focusing on the best-corroborated probable relationships among Sinauer Associates the major groups of chondrichthyans. The paraselachians, Morales Studio shown here as a distinct lineage, were in fact probably paraphyVL10E_06.01.ai letic with respect2-12-18 to the holocephalans. The narrow lines show interrelationships only; they do not indicate times of divergence or the unrecorded presence of taxa in the fossil record. Blue bars indicate the group’s presence, and the light blue bar represents the possible presence of the group. The dashed line indicates current controversies about relationships. The hatched bar indicates possible occurrence based on limited evidence. 6.1 Chondrichthyes: The Cartilaginous Fishes Figure 6.2 Simplified phylogeny Chondrichthyes (cartilaginous fishes) Holocephali of cartilaginous fishes. Quotation marks indicate a paraphyletic group. A dagger (†) indicates an extinct taxon. Elasmobranchii Sharks Skates and rays Neoselachii Hybodonts † “Stem elasmobranchs”† “Paraselachians”† Chimaeras Euselachii Ostheichtyes (bony fishes) 97 Dorsoventrally flattened; enlarged pectoral fins Holostylic (fused) upper jaw Subterminal mouth; hyostylic (mobile) upper jaw Gill openings covered by soft tissue Tribasal fin Gill openings separate and uncovered Tesserate prismatic calcified cartilage in endoskeleton; pelvic claspers; placoid scales chondrichthyans mineralize portions of the skeleton, and may have perichondral bone surrounding the mineralized cartilage, but only osteichthyans (including tetrapods) have an endoskeleton composed entirely of bone, both perichondral and endochondral. Cartilage is not necessarily weaker than bone; calcified cartilage can be made extremely strong when there are multiple layers and internal supports, as in the jaws of rays that crunch mollusks. All vertebrates more derived than the extant agnathans have a bony exoskeleton of some sort, formed from dermal bone. You saw this external covering in the ostracoderms and placoderms in Chapter 3. Indeed, the bones just unPough Vertebrate Life 10e derneath the skin on the top of our skull are a remnant of Sinauer Associates this exoskeleton (see Chapter 2). Although chondrichthyans Morales Studio VL10E_06.02..ai 03-5-18 have evidently lost the extensive plates of dermal bones seen in other jawed fishes, they retain an exoskeleton of scales composed of dentine, enameloid, and even traces of bone, and also have these tissues in their teeth. These unique scales are called placoid scales, also known as dermal denticles, and they develop in the same way as teeth— that is, from a single dental papilla. Many chondrichthyans, especially chimaeras, also have complex labial cartilages associated with their jaws. The nature of the cartilaginous skeleton means that, unlike bone, it tends to fall apart after death; thus the extinct chondrichthyans are known largely from fossil teeth. Fortunately, chondrichthyans have a lot of teeth. Their teeth are not embedded in the jaw like those of extant bony fishes. Rather, they usually form in a tooth whorl, by which the teeth are continually replaced as they wear down and eventually fall off (Figure 6.3). Each tooth (A) Functional tooth Developing replacement teeth (B) Functional teeth Teeth soon to be shed Replacement tooth Figure 6.3 Tooth replacement by chondrichthyans. (A) Cross section of the jaw of an extant shark, showing a single functional tooth backed by a band of replacement teeth in various stages of development. Together, the functional and developing teeth form a tooth whorl. (B) The replacement teeth are visible behind the functional teeth in this skeletal shark jaw. (B, courtesy of Lisa Whitenack.) 98  CHAPTER 6 Radiation and Diversification of Chondrichthyes on the functional edge of the jaw is but one member of a tooth whorl, attached to a ligamentous band (the dental lamina) that courses down the inside of the jaw cartilage deep below the fleshy lining of the mouth. A series of developing teeth is aligned in each whorl in a row directly behind the functional tooth. Tooth replacement in extant sharks can be rapid. Young sharks replace each lower-jaw tooth as often as every 8.2 days and each upper-jaw tooth every 7.8 days, although the rate of replacement varies considerably with species, age, and the general health of the shark, as well as with environmental factors such as water temperature. Tooth whorls are also seen in acanthodians, which are now considered to be the sister group to the chondrichthyans. They are also found in some basal osteichthyans (as are rooted teeth). Thus, tooth whorls are probably a primitive feature of crown gnathostomes (i.e., all gnath­ ostomes excluding the now-extinct placoderms). The grinding tooth plates of chimaeras, which are not replaced, are a secondary modification of the original dental condition. Many of the extinct related forms, such as paraselachians, also had tooth whorls, as did some of the earlier holocephalans. Extant chondrichthyans also have distinctive features of their internal anatomy and physiology, notably a large, lipid-filled liver that renders them neutrally buoyant (i.e., relatively stationary in the water, neither sinking nor floating upwards). In addition, chondrichthyans retain nitrogenous compounds that raise their internal osmotic concentrations, and ketones are the primary metabolic substrates of their skeletal and cardiac muscles. 6.2 Evolutionary Diversification of Chondrichthyes The classification of extant chondrichthyans into Elasmobranchii and Holocephali reflects a division that dates back almost to the start of chondrichthyan history. Both the fossil record and molecular dating techniques indicate that this division had occurred by the start of the Devonian. Elasmobranchii contains the extant Neoselachii plus extinct relatives. Holocephali includes chimaeras and related extinct forms. When fossils are considered, Holocephali can be seen to be part of a larger group that also includes paraselachians (extinct sharklike forms, paraphyletic with respect to holocephalans). This larger grouping is also known as the Euchondrocephali. Paleozoic chondrichthyan radiations Chondrichthyans probably exhibited their greatest diversity during the Paleozoic, both in terms of number of species and ecomorphological types. Most species were less than 50 cm long, and body forms included almost every shape known among extant fishes, from dorsoventrally flattened through fusiform to ribbonlike. Paleozoic stem chondrichthyans Fragmentary remains of chondrichthyans are known from the Middle Ordovician, but definitive forms are not known until the Devonian. The Ordovician and Silurian remains consist of scales that share derived features with scales of crown chondrichthyans. The stem chondrichthyian iniopterygians are known from the Carboniferous. These were smallish (20–60 cm) and rather chimaera-like in form, with large, dorsally positioned pectoral fins. Inioipterygians were originally thought to be related to holocephalans, but various features (including the primitive nature of the braincase) now place them outside the crown chondrichthyians. Paleozoic elasmobranchs The first elasmobranchs appeared in the Early Devonian. Many were generally sharklike in form, although they lacked several derived characters of modern sharks. A conspicuous difference between the stem elasmobranchs and modern sharks is the position of the mouth; stem elasmobranchs had a terminal mouth located at the front of the head, rather than a subterminal mouth beneath a protruding snout (or rostrum) as in modern sharks. They also lacked the independently mobile upper jaw of extant sharks and rays. Cladoselache is a representative example of a stem elasmobranch (Figure 6.4A). It was about 2 m long when fully grown, with large fins, a large mouth, and five separate external gill openings on each side of the head. Like many other stem elasmobranchs, Cladoselache was probably a predator that swam in a sinuous manner, engulfing its prey whole or slashing them with daggerlike teeth. Xenacanthans were a lineage of mainly freshwater bottom-dwellers. These stem elasmobranchs had robust fins and heavily calcified skeletons that may have decreased their buoyancy. Some had elongated, eel-like bodies (Figure 6.4B). Xenacanthans appeared in the Devonian and survived until the end of the Triassic (possibly surviving into the Jurassic), at which time they died out without leaving direct descendants. Stethacanthid stem elasmobranchs from the Early Carboniferous showed remarkable sexual dimorphism. The five species of stethacanthids that have been described ranged in length from about 30 cm to nearly 3 m. The first dorsal fin and spine of males in this family were elaborated into a structure that was probably used in courtship. In two genera of stethacanthids, Orestiacanthus and Stethacanthus, this structure (the spine-brush complex) projected more or less upward and ended in a blunt surface that was covered with spines (Figure 6.4C). Males of two other genera of stethacanthids, Damocles and Falcatus, had a swordlike nuchal spine that projected forward parallel to the top of the head (Figure 6.4D). One of the fossils of Falcatus may be a pair that died in a precopulatory courtship position, with the female grasping the male’s dorsal spine in her jaws. These spines are odd-looking structures, but they are not unique; males of some extant chimaeras have a modification of the nuchal spine called a cephalic clasper that is used during courtship. 6.2 Evolutionary Diversification of Chondrichthyes (A) (A) Cladoselache Anterior dorsal fin Spine Posterior dorsal fin Spine Epichordal lobe 99 Functional teeth Notochord New teeth Scapulocoracoid (shoulder girdle) Pelvic girdle Pelvic fin Pectoral fin Hypochordal lobe Basals Encasing cartilage 100 mm Old teeth are retained. Radials (B) (B) Xenacanthus Upper jaw 100 mm Lower jaw Encasing cartilage holding whorl in place (C) Stethacanthus Spine-brush complex Labial cartilage holding whorl in place (C) 50 mm (D) Damocles Nuchal spine Figure 6.5 Tooth whorl of Helicoprion. (A) Lateral view Pelvic claspers 10 mm Figure 6.4 Paleozoic elasmobranchs. (A) Cladoselache. (B) Xenacanthus. (C) A male Stethacanthus, showing the first dorsal fin and spine elaborated into a brushlike structure atop the head. (D) Male Damocles serratus, a 15-cm-long, sharklike form from the Late Carboniferous, showing the sexually dimorphic nuchal spine and pelvic claspers (females had neither structure). (A,B after Moy-Thomas and Miles 1971; C after Benton 2005, adapted from Zanerl 2004; D after Lund 1986.) of the symphysial (middle of the lower jaw) tooth whorl of the paraselachian Helicoprion, showing the chamber into which the lifelong production of teeth spiraled. (B) The tooth whorl was attached to the lower jaw by encasing cartilage. (C) Reconstruction of Helicoprion. (A,B after Ramsay et al. 2015; C © Jamie Chirinos/Science Source.) As their name suggests (Greek para, “beside” or “near”), paraselachians looked like sharks; they had sharklike teeth, and their upper jaw was not fused to the cranium as in extant chimaeras. One of these forms was Helicoprion, a Triassic survivor, known for its bizarre, spiraling toothNote whorl Note I think our art Paleozoic holocephali Both holocephalans and parasela(Figure 6.5). There have been many weird and wonderful Originalthe art is really fuzzy in places. If you chians first appeared in the Middle Devonian, although reconstructions of what would have looked likelook at Pough Vertebrate LifeHelicoprion 10E A few areas I had to leave blank. our whorls ar Associates extantVertebrate holocephalan order Chimaeriformes did not appear in life, Sinauer but a detailed biomechanical analysis shows that this Pough Life 10E Trying to not introduce error. If better there seem to Morales Studio Sinauer Associates until the Late Carboniferous. The paraselachiansexamples (six orders) tooth whorl wasclean contained entirely within the mouth. Heare available I could VL10E_06.05.ai 3-6-18 Morales Studio and the other orders of holocephalans were mainly upPaleozoic, the details. licoprion probably fed on soft-bodied prey, using the tooth VL10E_06.04.ai 08-09-17 although a few forms to survived into the Triassic. whorl rather like a circular saw, serially trapping, piercing, 100 CHAPTER 6 Radiation and Diversification of Chondrichthyes and cutting its prey as they advanced into its mouth. Another Paleozoic group was the menaspoids, heavily armored fishes with plates of dermal bone on their heads, almost like placoderms, and numerous paired spines projecting from the side of their mouths. (A) The Mesozoic chondrichthyan radiation Members of the modern elasmobranch radiation, Neoselachii, first appeared in the Late Triassic (although molecular data would place the split between sharks and rays as Permian). Chimaeras were present as holdovers from the Paleozoic. These modern radiations will be considered in Chapter 7. Here we discuss those radiations of the stem members (none of which survived into the Cenozoic) of the extant lineages. Anterior piercing tooth Posterior crushing tooth (B) Elasmobranchs Xenacanths, freshwater eelAnal fin Basals like stem elasmobranchs, survived until the end 50 mm Fin rays of the Triassic (possibly into the Jurassic), but the Radials Mesozoic elasmobranch radiations consisted priFigure 6.6 The Late Cretaceous elasmobranch Hybodus. marily of more derived forms, with changes in (A) Dentition consisted of pointed teeth at the front of the mouth their feeding and locomotor systems. These were the hyand blunt teeth in the rear. (B) Hybodonts looked very much bodont elasmobranches, which form the stem lineage to like modern sharks except that the mouth was terminal. (After the modern sharks and rays. Hybodont “sharks” and extant Moy-Thomas and Miles 1971.) elasmobranchs are grouped together in Euselachii. Hybodonts (Hybodontiformes) first appeared in the Late Devonian and flourished until the end of the Cretaceous epicercal or heterocercal (Greek heteros, “different”; kerkos, in both marine and freshwater environments. Hybodus is “tail”). The value of the euselachian heterocercal tail lies a well-known genus of the Late Triassic through the Crein its flexibility and the control of shape made possible taceous (Figure 6.6). Complete, 2-m-long skeletons have by the intrinsic musculature. When it is undulated from been found, although many hybodonts were much smaller side to side, the fin twists so that the flexible lower lobe than this. trails behind the stiff upper one. This distribution of force Hybodonts were distinguished by a heterodont dentition produces forward and upward thrust that can lift a fish (different tooth shapes in different regions of the jaw). The from a resting position or counteract its tendency to sink anterior teeth had sharp cusps and may have been used for as it swims horizontally. piercing, holding, and slashing softer foods. The posterior Other morphological changes in euselachians included teeth were stout, blunt versions of the anterior teeth and the appearance of a complete set of haemal arches (arches may have crushed hard-bodied prey, such as crabs. below the centrum) in the caudal (tail portion) vertebral The hybodonts also showed advances in the structure of column that protected the arteries and veins running the pectoral and pelvic fins that made them more mobile below the notochord; well-developed ribs; and narrow, than the broad-based fins of earlier elasmobranchs. Both more pointed dorsal-fin spines at the leading edge of the pairs of fins were supported on narrow stalks formed by dorsal fins. These spines were ornamented with ridges and three narrow, platelike basal cartilages that replaced the grooves and studded with barbs on the posterior surface, long series of basals seen in earlier elasmobranchs. The suggesting that they were used in defense. narrow base allowed the fin to be rotated to different angles Despite the variety and success of hybodonts during the as the hybodont swam up or down, allowing greater control Mesozoic, they became increasingly rare and disappeared Pough Vertebrate Life 10E of locomotion. This narrow-based fin had shortened radials, at the end of the Mesozoic. Sinauer Associates Morales with a large extent of the fin now composed of flexible fin Studio VL10E_06.06.ai 12-6-17 rays (ceratotrichia). Holocephali A few lineages of paraselachians, such as Along with changes in the paired fins, the caudal fin Helicoprion, survived into the Early Triassic. Most of the assumed new functions, and an anal fin was now present. lineages of holocephalans were extinct by the end of the Reduction of the lower (hypochordal) lobe altered the cauPaleozoic. The survivors were mainly members of Chimaeriformes, with the modern families diverging in the Late dal fin shape so that the upper lobe was distinctively larger Jurassic to Early Cretaceous. Another holocephalan lineage than the lower lobe. This tailfin arrangement is known as Summary  101 that persisted into the Mesozoic was the myriacanthids, some of which had small armored plates on their heads (modern chimaeras have none). Myriacanthids persisted only until the end of the Jurassic. Paleozoic and Mesozoic chondrichthyan paleobiology Devonian chondrichthyans shared their environment with a diversity of other fishes, including early bony fishes, plus various more ancient lineages of fishes: ostracoderms, placoderms, and acanthodians. During this time chondrichthyans were probably the most numerous and diverse types of fishes, although they were not yet playing the role of large marine predator that was the preserve of the arthrodire placoderms such as Dunkleosteus. The eel-like xenacanths may have been the apex predators in the freshwater realm, although they would have had competition from the bony fishes of the lineage that would give rise to tetrapods (tetrapodomorph fishes; see Chapter 7). By the Carboniferous, placoderms were extinct, and tetrapodomorph fishes were rare. Chondrichthyans diversified into this empty ecomorph space in both marine and freshwater environments, becoming even more diverse and numerous than in the Devonian. A rich array of fishes is known from the late Early Carboniferous Bear Gulch Limestone in Montana, which represents a shallow tropical marine bay. Here 60% of the fishes present were chondrichthyans. About one-third of these were holocephalans, one-fourth were elasmobranchs (some euselachians, but mostly more basal forms such as stethacanthids and a few iniopterygians), and the rest were paraselachians. These fishes represented nine different ecological types, including midwater predators and bottom-dwelling mollusk crunchers. A similarly diverse array of fishes is known from the middle Late Carboniferous, from the Minto Formation in New Brunswick, Canada. Here the deposits appear to represent a span of environments from marine through brackish to freshwater, favoring species that could tolerate a variety of water salinities (euryhaline species). Chondrichthyans, mostly xenacanth elasmobranchs, were found throughout the different salinity environments, making up 65% of the fauna. Also present were acanthodians, bony fishes, and tetrapods. Most of these mid-Carboniferous chondrichthyan lineages continued into the later Carboniferous and Permian, with a few stragglers making it into the Early Triassic, but aquatic faunas became increasingly dominated by bony fishes in the late Paleozoic. Neoselachians started off as nearshore predators in the Mesozoic and expanded into the open oceans by the mid-Cretaceous. This shift was probably related to the radiation of neopterygian bony fishes, which would have provided predatory neoselachians with a prey base. The hybodont radiation, prominent throughout most of the Mesozoic, was brought to an end in the Late Cretaceous, probably by competition from neoselachians. Summary Chondrichthyans are not primitive fishes, but are highly derived in their own fashion. Chondrichthyans have distinctive features of their skeleton, scales, and teeth. The first definitive chondrichthyan fossils are from the Early Devonian, although chondrichthyan-like scales are known from the early Silurian, and possibly the Ordovician. Chondrichthyans share two unique anatomical features: a cartilaginous skeleton that, if calcified, is mineralized in a unique fashion (differently from bone); and pelvic claspers in males, used for internal fertilization. The two main branches of chondrichthyans reflect a division that had occurred by the start of the Devonian. Elasmobranchii includes the extant neoselachians (sharks and rays) and extinct relatives. Sharks have 5–7 pairs of gill openings on the side of the head, whereas rays have 5 pairs of gill openings on the ventral surface of the head. Both sharks and rays have a mobile upper jaw. Holocephali includes the extant chimaeras and related extinct forms. Chimaeras have a single gill opening covered by soft tissue and an immobile upper jaw fused with the skull. Paraselachians, a mainly Paleozoic paraphyletic grouping of sharklike forms, were included within Holocephali. Chondrichthyans also have distinctive scales over their body—placoid scales, composed of enameloid, dentine, and traces of bone at their base. Their teeth are contained in a tooth whorl, in which new teeth are continually developing. Chimaeras do not have tooth whorls, and instead have grinding tooth plates that are not replaced. Extant chondrichthyans have some distinctive features of their internal anatomy and physiology, including a large, lipid-filled liver and the retention of nitrogenous compounds in their tissues for osmotic regulation in the marine environment. (Continued)