Chondrichthyes (Sharks,Rays and Chimaeras)Michael D Gottfried, Michigan State University Museum, East Lansing, Michigan, USA

Chondrichthyes is the class of vertebrates that includes sharks, rays and chimaeras.

These relatives of bony fishes are characterized by an internal skeleton of cartilage

rather than true bone.

Introduction

The chondrichthyans, or sharks, rays and chimaeras, arevery successful animals that rst appeared over 400millionyears ago, long before the age of dinosaurs. They arerelated to the bony shes, or osteichthyans, which are farmore numerous and diverse unlike bony shes, sharksand rays have an internal skeleton composed of cartilagerather than bone. Sharks and rays, while not nearly asdiverse as bony shes, have nevertheless maintained theirposition as important predators in many marine and somefreshwater environments.

Basic Design

Sharks havemaintained the same basic body plan (Figures 1and 2) throughout their 400-million-year-plus history.Sharks typically have a streamlinedbodywith a long snout,an underslungmouth, ve to seven pairs of gill slits, a smallspiracular opening, paired pectoral and pelvic ns, one ortwo dorsal ns, an anal n (absent in some groups), and acrescent-shaped caudal (tail) n which is heterocercal,meaning the vertebral column is upturned and extends outto the tip of the ns upper lobe.Male sharks have claspers paired appendages used inmating associated with theirpelvic ns. Aristotle, in 350 bc, recognized importantdierences between sharks and bony shes, including theobservation that sharks have separate gill slits while thegills of bony shes are covered by an opercular ap.

Rays, closely related to sharks, are primarily bottom-dwellers that have evolved a attened, disc-shaped body,with eyes located on top of their heads. They use theirgreatly expanded wing-like pectoral ns to glide gracefullythrough the water. Many rays have modied their teethinto at crushing plates for feeding on molluscs andcrustaceans.In addition to the sharks and rays, most modern

systematic arrangements place another group within theChondrichthyes the Holocephali (or holocephalans),more commonly referred to as chimaeras, elephantshes orratshes. There are around 35 living species, all marine andprimarily found in relatively deep cold water. Holocepha-lans share with sharks and rays a cartilaginous skeleton,and males also have claspers associated with their pelvicns. Holocephalans, however, are rather peculiar animalsthat dier markedly from sharks in a number of respects.Many have oddly shaped protruding snouts, and theygenerally have large heads and prominent eyes, ventrallypositioned mouths, jaws with ridged knobby toothplates,smooth scaleless bodies, gills covered by a single opercularap, and tapering whip-like tails. Holocephalans also have

Article Contents

Introductory article

. Introduction

. Basic Design

. Diversity

. Habitats

. Reproduction

. Special Sensory Adaptations

. Fossil History

. Phylogeny

. Sharks and Humans

. Conservation

Firstdorsalfin

Seconddorsalfin

Caudalfin

Analfin

Pelvicfin

PectoralfinGill

openings

Mouth

Nostril

Snout

EyeSpiracle

Figure 1 External features of a generalized shark.Figure 2 Blacktip shark, Carcharhinus limbatus (photograph byD. Perrine &).

1ENCYCLOPEDIA OF LIFE SCIENCES 2001, John Wiley & Sons, Ltd. www.els.net

upper jaws that are rmly fused to the cranium, as opposedto the mobile upper jaws of sharks and rays.A feature shared by all chondrichthyans is an internal

skeleton of cartilage, rather than bone as in othervertebrates the name Chondrichthyes means cartilagi-nous sh. Sharks and rays uniquely possess prismaticcartilage, in which the cartilages surface layer is composedof small crystalline prisms. Recent research has shown thatthe jaws of some mollusc-crushing rays are internallyreinforced at stress points by struts (or trabeculae) ofcartilage arranged in much the same way as the bone ofother vertebrates, and that some primitive fossil sharkspossess true bone as well as cartilage.Cartilaginous shes do not have swim bladders, which

bony shes use to maintain buoyancy, but instead rely onvery large oily livers to help keep them from sinking.However, it is not true that all sharks have to swimcontinuously to keep alive many species, including nursesharks (Ginglymostoma cirratum) which are commonlykept in aquaria, regularly rest on the bottom.Most sharks are active predators and have sharp,

triangular, cutting teeth. Sharks continuously produceand shed their teeth. It is estimated that some species mayproduce 50 000 or more in a single lifetime. The teeth arearranged in rows on the jaws, with each row alwaysadvancing toward the front edge of the jaw like a slow-moving conveyor belt, and newer replacement teeth takingthe position of the older teeth as they are shed along themargin of the jaws. It has recently been discovered thatsome sharks begin producing, shedding, and replacingtheir teeth even before they are born. Rays and holoce-phalans have fundamentally the same kind of toothreplacement but the whole process is much slower and in

holocephalans the old teeth are kept and overgrown bynewer parts of the tooth plates. Along with teeth, mostcartilaginous shes have tiny placoid scales embedded intheir skin, which gives the skin its prickly feel, and somespecies have sharp spines in front of their dorsal ns.

Diversity

Many dierent species of sharks and rays have evolvedover the course of their very long history, but at present thegroup is not exceptionally diverse. There are nearly 600living species of rays and approximately 350 shark species.In comparison, the living bony shes (osteichthyans)number more than 23 000 species (about half of all knownvertebrates).Despite their relatively low overall diversity, living

sharks and rays are important and conspicuous membersof many marine and some freshwater ecosystems. Livingsharks range in size from the tiny dwarf lantern shark(Etmopterus perryi), with a total length of 20 cm (8 in), tothe gigantic planktivorous whale shark (Rhincodon typus),which grows to a length of at least 12m (40 ft). Accordingto recent classications, living sharks and rays are dividedbetween two major groups, the Squalea and the Galeo-morphii (see Figure 3).

Habitats

Chondrichthyans are found in a wide range of aquatic,predominantly marine habitats. They are most common

Carcharhiniformes requiem, hammerhead, tiger, lemon and cat sharks

Lamniformes basking, thresher, sand tiger, mako and great white sharks

Orectolobiformes whale, nurse, bamboo and wobbegong sharks

Heterodontiformes horn and bullhead sharks

Hexanchiformes cow and frill sharks

Echinorhiniformes bramble sharks

Squaliformes dogfish and sleeper sharks

Squatiniformes angel sharks

Pristiophoriformes sawsharks

Rajiformes skates and rays

Galeomorphii

Squalea

Figure 3 Evolutionary relationships of the major groups of modern elasmobranchs or Neoselachii (adapted from de Carvalho, 1996).

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and have their greatest diversity in temperate to tropicalmarine environments, in coastal to shallow shelf areas ofthe sea. Very few species are found below 2000 metres;among those that are the gulper sharks (Centrophorus),which can occur down to 4000 metres. Many shark speciesoccupy themedium-to-largemarine predator niche, and assuch are typically found in habitats with a wide diversity ofshes and other marine animals that are their potentialprey. These habitats commonly include sandy-bottomedshallows o open beaches, lagoons, estuaries, rockycoastlines, coral and rocky reefs, and kelp forests.Particularly favoured areas include biologically rich coast-al upwelling zones and the mouths of rivers and deltas. Afew species, most notably the bull shark (Carcharhinusleucas), enter freshwater environments bull sharks arewell known for swimming up rivers and also enterfreshwater lakes. Some rays spend their entire lives infreshwater, including the river rays (Potamotrygonidae) oftropical South America.

Reproduction

Cartilaginous shes are unusual compared to most bonyshes in that they produce a relatively small number ofospring, anywhere from one to a few dozen depending onthe species (bony shes often produce thousands or evenmillions of eggs at a time). The eggs are fertilized internally;males use their claspers to transmit sperm during copula-tion. Mating has only rarely been observed in sharks. It isthought to occur seasonally for only a brief time each year,and even less frequently in some species like the spinydogsh (Squalus acanthias), which has a 2-year gestationperiod (the longest known for any animal). Female sharksare often observedwith scars around their pectoral ns andon the top of their heads, probably the result of malesseizing them during copulation.In the majority of sharks, the eggs develop inside the

female sharks uterus, with a long gestation period of up to2 years, and with nutrition supplied by large yolk sacs. In afew species, for example sand-tiger sharks (Carchariastaurus), young inside the uterus may cannibalize theirsiblings while they are developing. Alternatively, someproduce eggs covered in a tough, horny egg case. Theyoung develop inside the egg case but outside theirmothers body, and also receive nourishment via a yolksac. Many aquaria now feature exhibits in which babysharks can be watched developing inside egg cases. In bothstrategies, once born the young are fully functional andindependent from their parents.

Special Sensory Adaptations

Sharks and rays are often regarded as very primitive, andtherefore simple, animals. While they are primitive withrespect to their systematic position, they neverthelesspossess a number of very specialized and highly sophisti-cated sensory capabilities. Perhaps the most intriguing istheir ability to detect the weak electrical signals producedby muscular activity in other animals, which helps them todetect and track prey and in some cases to locate potentialmates. Sharks detect electrical signals using specialelectroreceptors called the ampullae of Lorenzini, smallchambers lled with a gelatinous substance and lined withspecial sensory cells. These ampullae, which are clusteredin the head region particularly on the sides and undersur-face of the snout, can detect electric signals as weak as ve-billionths of a volt. Along with electroreception, sharksalso have a highly sensitive lateral line system for detectingmovements andvibrations in thewater, another very usefuladaptation for amarine predator. The lateral line receptorsrun along the body on both sides, and have branches on thehead. Sharks also have acute hearing, balance and vision,and an especially keen sense of smell capable of detectingjust a few molecules of blood in seawater.

Fossil History

Our knowledge of fossil sharks is limited in many cases totheir teeth,which are covered in hard enamel andproducedin great numbers, supplemented by occasional spool-likecalcied vertebral centra. Less commonly n spines arefound. The cartilaginous skeleton of sharks rarely fossi-lizes, although some preserved skeletons (ironically,usually of early primitive sharks, and also of some raysand chimaeras) have been found.Cartilaginous shes are a very ancient groupwith a fossil

record that extends back into the Palaeozoic era, to theSilurian period approximately 420 million years ago (Ma).The earliest fossil chondrichthyans are known only fromisolated scales the exact nature of these rst representa-tives is a mystery, as is the origin of the group as a whole.Chondrichthyans may be closely related to an extinctPalaeozoic group of jawless shes called thelodonts whichhave somewhat similar scales, or possibly to the placo-derms, early jawed shes with bony armour. Under-standing the early evolution of sharks remainsproblematic due to the lack of informative specimens ofthe earliest basal forms.The oldest well-known shark is Cladoselache, from the

Devonian ofOhio (about 380Ma).Cladoselache resemblesmodern sharks, with a streamlined body, ve pairs of gillslits, paired large pectoral and smaller pelvic ns, twodorsal ns (each with a large spine), and a cartilaginousskeleton. If Cladoselache were alive today there would be

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no diculty in identifying it as a shark. The teeth ofCladoselache and a number of related primitive sharks aredistinctive, with a high central cusp anked on either sideby smaller lateral cusps.Following the Devonian, the Carboniferous and Per-

mianperiods (c. 360250Ma) sawagreat early radiationofsharks, including a number of bizarre forms characterizedby unusually modied ns and odd dentitions. One groupcalled the iniopterygians developed very long, wing-likepectoral ns, possibly used to y above the water like theliving ying shes. The stethacanthids and falcatidsinclude species with elaborately modied dorsal nelements that project out over their heads, probably usedby males in courtship and/or as a threat display. Theedestids have teeth arranged in a spiral whorl with thenewest and largest teeth on the outside of the whorl. Someedestids may have grown very large, but only their peculiartooth whorls are well known. Among themost unusual arethe petalodontids, poorly known until recent discoveries,which have shown them to have deep bulbous bodies, shortheads and strongly ridged teeth suitable for crushingshellsh and coral. Many of the unusual sharks of this eraare known from superb specimens found at two veryimportantCarboniferous sites theBearGulchLimestoneof Montana, USA, and the Bearsden deposit nearGlasgow, Scotland. Along with these, freshwater depositsfrom this time interval commonly contain remains of thexenacanths large, elongate sharks with tapering tails andprominent spines immediately behind their heads. Somexenacanths are known from well-preserved completeskeletons.The unusual sharks of the Palaeozoic largely disap-

peared by the Mesozoic era (25065Ma). One Palaeozoicgroup that survives into the Mesozoic, the hybodonts,supercially look like Cladoselache but have a number ofadvanced skeletal features that link them more closely tomodern sharks. By the middle of the Mesozoic, the rstremains of rays are found, and by the latter part of theMesozoic the new sharks, or neoselachians, becomeestablished as the dominant chondrichthyans. Neosela-chians are characterized by more mobile jaws relative totheir primitive ancestors. A number of neoselachianspecies die out at the close of the Mesozoic era, 65Ma,but some lineages survived into the next era theCenozoic.All Cenozoic sharks and rays, including those living today,are neoselachians (the group also includes some fossilforms that are now extinct).The most notorious neoselachian, and the most specta-

cular marine predator to have ever evolved, is the giantCarcharodonmegalodon, or Megatooth, a close relative ofliving greatwhite sharks (C. carcharias).Megatooth sharksare found worldwide in fossil marine deposits from about25 to 3Ma. These superpredators reached over 16m (50 ft)in total length, but not 100 ft or more as claimed in earlierexaggerated accounts, and may have had a mass in excessof 50 000 kg (the equivalent of several Tyrannosaurus rex

dinosaurs!). Particularly notable are their enormousserrated triangular teeth, which grew up to seven inchesin length and were used to catch baleen whales and otherlarge prey. The megatooth is probably the largest sharkever to have evolved only the living whale shark(Cetorhinus maximus), a placid lter-feeding giant, reachesa comparable size.Holocephalans have a fossil record extendingback to the

Devonian, suggesting a split from sharks and raysapproximately 350400Ma.

Phylogeny

According to recent analyses, all living sharks and rays,and a few close fossil relatives, are members of a singlemonophyletic group, the Neoselachii (Figure 3). The oddfossil forms that appeared in the Palaeozoic are consideredto be more primitive and lie outside the Neoselachii.Neoselachians are united as a monophyletic group byseveral shared characters, including features of the gillarches, jaw musculature, pectoral girdle and teeth. Withinneoselachians, two main lineages of living sharks arerecognized the Galeomorphii, which includes theheterodontiforms, orectolobiforms, lamniforms andcarcharhiniforms, and the Squalea, comprising the hexan-chiforms, echinorhiniforms, squaliforms, squatiniforms,pristiophoriforms and rajiforms. The monophyletic statusof both the Galeomorphii and the Squalea is supported byseveral shared derived features.This current framework elaborates on and somewhat

modies what was the prevailing view for many years,which postulated four main groups of extant sharks theGaleomorphii, Squalomorphii, Squatinomorphii and Ba-toidea. This earlier hypothesis left unresolved the questionof the interrelationships of the batoids (Rajiformes),which are now considered to be members of the Squalea,closely related to the pristiophoriforms (sawsharks).Sharks and rays are grouped together within Chon-

drichthyes as the Elasmobranchii (or elasmobranchs), withholocephalans as their next most closely related (or sister)group.

Sharks and Humans

Sharks are a subject of great fascination to humans, nodoubt because of the perception that they pose a threat tous. In fact, given themanymillions of peoplewho engage invarious forms of aquatic recreation, the number ofconrmed deadly shark attacks is actually relatively low(although the attacks that do occur receivewide attention).Attacks have most commonly happened along the coast-lines of Australia, South Africa and the USA, all of whichhave large populations of coastal shark species. In an

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average year, about 20 human deaths worldwide can beattributed to sharks (while at the same time we catch andkill millions of sharks, often as incidental, wastefulbycatch).Shark attacks are, therefore, uncommon, and in many

cases may even be accidental on the part of the shark. Theattacks can be divided into two types provoked, in whichthe shark is reacting to aperceived threat, andunprovoked,which are more mysterious. Certain species, such as thegrey reef shark (Carcharhinus amblyrhynchos), are moreaggressive than others, and may attack if approached tooclosely. Other aggressive species include the tiger (Galeo-cerdo cuvier), bull (Carcharhinus leucas), blue (Prionaceglauca), hammerhead (Sphyrna species) and great white(Carcharodon carcharias) sharks. Often aggressive speciessignal their intent by body language, including archingtheir back into a hump. One hypothesis is that sharksmistake people in the water for favourite prey, includingthe observation that surfers resemble seals when viewedfrombelow.This idea remains controversial andmay be anoversimplication.Some simple precautions will reduce the unlikely

possibility of being attacked by a shark. Swimmers, divers,surfers, etc., should avoid shallow, murky water near rivermouths at dawn or dusk, or at night, conditions underwhich a number of attacks have occurred. Recently,researchers in South Africa have experimented withelectromagnetic elds as a means of repelling sharks; whilesome promising results have been obtained, the eective-ness of these devices is still inconclusive.Sharks are also benecial to humans in many ways. A

number of species are caught for food, and shark meat hasgained in popularity in recent years (to the detriment ofsome overharvested species). Shark skin is an eectiveabrasive, and is also used to make wallets, shoes and otherproducts. Shark liver oil is thought bymany to have healthbenets, and the corneas from shark eyes have been usedfor corneal transplants in humans. Recent research has,however, cast serious doubt on the eectiveness of sharkcartilage derivatives as a treatment for cancer.Sharks occupy an important position in the art and

traditional religious beliefs of many sea-based cultures.Such beliefs are particularly strong among the nativeislanders of the Pacic, and in the Aboriginal culture ofAustralia, where sharks are greatly revered and respected.

Conservation

In recent years it has become increasingly clear that thepopulations ofmany shark species are in sharpdecline. The

primary cause of this is commercial overshing; sharks arecaught deliberately in very large numbers, and are alsokilled as accidental bycatch in other sheries. Much of thementality that contributed to this current state of aairsarose in the 1970s, when sharks were both popularized anddemonized in the popular media, most notoriously in thebook and lm versions of Jaws.We nowhave a better andmore sophisticated appreciation of the crucial role thatsharks and rays play as predators, and in some casesscavengers, in helping to maintaining healthy balancedecosystems.Reduced population levels are of particular concern in

sharks because of their long gestation periods and lowreproductive rates. To address this issue, shark biologistsand marine conservation groups have strongly urged thatshark shing be reduced to sustainable levels, that thewasteful practice of nning (killing sharks only for theirns) be halted, and that critical habitats, such as shallow-water nursery areas, be preserved and protected. There aresome promising recent signs that this problem is beingtaken seriously. For example, South Africa, Australia andthe USA have taken steps to protect the spectacular butthreatened great white shark Carcharodon carcharias, anda number of countries are working towards restricting thecommercial catch of declining shark species so that theirpopulations have a chance to recover. Organizationsactively involved in shark research and conservationinclude the American Elasmobranch Society, the Eur-opean Elasmobranch Association and the Pelagic SharkResearch Foundation.

Further Reading

Compagno LJV (1984) FAO Species Catalogue. Sharks of the World.

FAO Fisheries Synopsis 125, volume 4(12): 1655.

Compagno LJV, Simpfendorfer C, McCosker J et al. (1998) Readers

Digest Explores Sharks. Readers Digest: Pleasantville, NY.

de Carvalho MR (1996) Higher level elasmobranch phylogeny, basal

squaleans, and paraphyly. In: Staissny M, Parenti L and Johnson G

(eds) Interrelationships of Fishes, pp. 3562. San Diego: Academic

Press.

GottfriedMD,CompagnoLJVandBowmanSC (1996) Size and skeletal

anatomy of the giant megatooth shark Carcharodon megalodon. In:

Klimley AP and Ainley DG (eds) Great White Sharks: the Biology of

Carcharodon carcharias, pp. 5566. San Diego: Academic Press.

Klimley AP andAinleyDG (eds) (1996)GreatWhite Sharks: the Biology

of Carcharodon carcharias. San Diego: Academic Press.

Paxton JR and Eschmeyer WN (1994) Encyclopedia of Fishes. San

Diego: Academic Press.

Tricas TC, Deacon K, Last P et al. (1997) The Nature Company Guide:

Sharks and Rays. Hong Kong: Time-Life Books.

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