Carcharhiniformes
(Ground sharks)
Class: Chondrichthyes
Order: Carcharhiniformes
Number of families: 8
Evolution and systematics
The fossil history of ground sharks (Carcharhiniformes) is known from a handful of preserved skeletons, but long intervening periods exist in which fossil skeletons of ground sharks have not been recovered. Ground sharks first appear in the late Jurassic (some 150 million years ago) Solnhofen limestones of Germany. These early fossils (e.g., Macrourogaleus) are not well preserved, but they bear some resemblance to modern catsharks (family Scyliorhinidae). After a long absence from the fossil record, fossil ground shark skeletons reappear in the late Cretaceous chalk deposits of Lebanon (ranging in age from 84 to 95 million years ago, or mya). These sharks (e.g., Pteroscyllium and Paratriakis) are thought to be related to catsharks and hound sharks (Triakidae), respectively, but on scant evidence. A few species of fossil catsharks from Lebanon are even placed in the living genus Scyliorhinus, which would give it a remarkable longevity of some 90 million years. These fossils have been studied only superficially, however, and they probably represent extinct genera of uncertain affinity. Partial skeletons are present in the Monte Bolca beds of northeastern Italy (Eogaleus and Galeorhinus) of Eocene age (some 52 mya), again after a hiatus of more than 30 million years.
Many extinct species of ground sharks are known from isolated teeth, which are widespread and provide a fairly robust stratigraphic record. Tertiary ground shark fossils are relatively modern in their level of diversity. Ground shark fossils are present on every continent, indicating that they have been distributed widely for the past 65 million years at least. Remarkably, the fossil record of ground sharks parallels their phylogenetic history, where the most "primitive" family (Scyliorhinidae) also is the oldest.
Ground sharks are related closely to bullhead (Heterodontiformes), carpet (Orectolobiformes), and mackerel (Lamniformes) sharks among living elasmobranchs (sharks and rays), forming the larger group known as the Galeomorphii. Galeomorph sharks are characterized by several evolutionary innovations, such as the unique placement of the hyomandibula (a cartilage supporting the jaws posteriorly) on the skull. Within the Galeomorphii, carcharhiniforms are related most closely to the mackerel sharks, as they share a tripodal rostrum (the anterior extension of the skull) supporting the snout internally. All carcharhiniforms have specialized secondary lower eyelids ("nictitating" eyelids, which are absent from all other sharks) as well as unique clasper skeletons. Similarly to lamnoids (a subgroup within mackerel sharks), there is also a group of "higher carcharhiniforms" characterized by plesodic pectoral fins (with internal supports reaching the fin margin).
There are approximately 216 species, 48 genera, and eight families in the Carcharhiniformes. This amounts to slightly more than half of all shark species and about half of all shark genera. The eight families are the Scyliorhinidae (catsharks, 15 genera and some 105 species—the largest shark family of any order), Proscylliidae (finback catsharks, three genera and five species), Pseudotriakidae (false catshark, monotypic), Leptochariidae (barbeled hound shark, monotypic), Triakidae (hound sharks, 10 genera and 39 species), Hemigaleidae (weasel sharks, four genera and seven species), Carcharhinidae (requiem sharks, 12 genera and 50 species), and Sphyrnidae (hammerhead sharks, two genera and eight species). New carcharhiniform species have been described in recent years, particularly of catsharks, and additional new species await formal description. Phylogenetic relationships among ground shark genera require further study, which may result in the merging of several currently monotypic genera and even of some of the families.
Physical characteristics
There are many different morphological and ecological trends within the Carcharhiniformes, which is to be expected from a large group that inhabits waters from the intertidal zone to the lower reaches of the continental slope. However, the morphological differences among ground shark families are not as great compared with the other orders of sharks, even though some families are quite distinctive. One of these families is the hammerhead shark (Sphyrnidae), which is unique among all sharks in having a laterally expanded head (the hammerhead, or cephalofoil, with eyes on the lateral extremes). Hammerhead sharks are otherwise very similar to requiem (carcharhinid) sharks. Catsharks (Scyliorhinidae) also are recognized easily, as their first dorsal fins are situated either on the same level as or behind the pelvic fins. The false catshark (Pseudotriakidae) is unique among sharks in having a first dorsal fin that is much longer than the caudal fin. The differences among the remaining families are subtle, and one must look at their teeth, labial furrows, and even intestines to identify them.
Carcharhiniforms are small, medium, or large sharks; adults usually range from 18 in (45 cm) to 20 ft (6 m) in length. The proscylliid Eridacnis radcliffei reaches only about 9.4 in (24 cm) in length and is one of the smallest known species of sharks. Ground sharks have two spineless dorsal fins (one species, Pentanchus profundicolus, with only one), the first larger than the second. There is a large caudal fin with a greater upper lobe, a prominent anal fin about as large as the pelvic fins (or even larger in some catsharks, especially Apristurus species), and moderately developed pectoral fins. There are five gill openings. The snout can be conical or broadly rounded (elongated in Isogomphodon). The eyes are elliptical, but they are rounded in some genera (e.g., Rhizoprionodon). The spiracles vary from a small pore to an opening just smaller than the eyes. When present, labial furrows (grooves alongside the mouth corners) vary from long to short. There is either a spiral or a scroll intestinal valve. The teeth may vary considerably between adults and juveniles of the same species, upper and lower jaws, and males and females and between species, genera, and families. A single broad, slanted, or erect cusp may be present, or there may be as many as five cusps per tooth (Proscylliidae). Many species are identified by their dental morphological features and formulas. The body is covered with small dermal denticles that do not form larger spines.
Carcharhiniforms vary widely in coloration. Shallow-water catsharks can be spectacularly colored, with many spots, saddle-like markings, and blotches, whereas deeper-water catsharks usually are drab or dark brown or black. Many species (requiem and hammerhead sharks) are gray or brown dorsally and laterally, with creamy or white ventral surfaces. Many triakids also are spotted or have other conspicuous markings similar to those of scyliorhinids. Many ground shark species have unique coloration.
Distribution
They are found worldwide in tropical to temperate waters, including cool boreal seas, but they are most abundant in tropical and warm temperate regions. Carcharhiniform sharks inhabit all major oceans except the Antarctic seas. (Deepwater catsharks of the genus Apristurus may inhabit Arctic waters.) They also are present in tropical freshwaters (rivers and lakes) in South, Central, and North America; Africa; Asia; and Australia.
Habitat
Carcharhiniforms are most abundant in tropical continental shelf regions. Most inshore, littoral habitats, including coasts, estuaries, river mouths, open bays and lagoons, atolls, and coral reefs (both coastal and barrier reefs), are occupied by ground sharks. They also are abundant offshore, off oceanic and continental islands, and are present in deeper waters along the upper continental slopes (especially species of Apristurus and Pseudotriakis). Some species are epipelagic in deeper ocean basins.
Behavior
Carcharhiniform sharks are present in many habitats, from the littoral to the oceanic; as a consequence they vary from sluggish, primarily bottom dwellers (such as many catsharks) to swift swimming, more active pelagic forms (e.g., blue shark and oceanic whitetip shark). The behavior of certain ground shark species has been studied in both captive and natural conditions (in particular, the lemon, gray reef, and bonnethead sharks). In general, pelagic species appear to cruise at low speeds, occasionally bursting into sudden activity, while bottom-dwelling species are more territorial and mostly nocturnal.
Some carcharhiniform species form aggregations, often by size or sex (except during mating season). Schooling is a very common social behavior in hammerhead sharks (e.g., the scalloped hammerhead, Sphyrna lewini, off the eastern Pacific coast of Mexico, where some 225 individuals may school together), but most carcharhiniforms spend much of their lives alone. Gray reef sharks (Carcharhinus amblyrhynchos) form schools in the Marshall Islands, as do lemon sharks (Negaprion brevirostris) in the Bimini Islands, Bahamas. Schools typically form during the day and break up for individuals to feed at night. Additionally, some species are now known to rest in caves for long periods; the whitetip reef shark, Triaenodon obesus, rests mostly during the day and sometimes in groups.
Sharks spend much of their lives as solitary predators and do not form family groups or cooperate with each other. Their types of behavior are less complex than those of marine mammals, but only a handful are known. In particular, aggressive display has been documented (e.g., for the gray reef shark), which may involve jerky head movements, arching of the back, and downward pointing of the pectoral fins. Social displays and social organization are particularly well known for the bonnethead, Sphyrna tiburo. Some of these displays are an outcome of size-dependent dominance hierarchies, such as swimming in a straight line. Bonnetheads do not show much aggressive behavior, a possible indication that more social species may be less aggressive.
Feeding ecology and diet
Ground sharks are voracious predators; none are filter feeders. Food items consist of numerous families of bony fishes, sharks and rays, marine mammals and marine mammal carrion, seabirds, marine reptiles (mostly turtles), and a wide range of invertebrates, including crustaceans, squid, octopi, cuttlefish, and shelled mollusks. Benthic ground sharks feed on items more readily available on or close to the bottom, such as hard-shelled invertebrates and certain fishes, whereas open-ocean forms feed intensely on pelagic fishes, such as tunas and their allies (Scombridae). Larger sharks prey on ground sharks, and larger species of ground sharks may feed on smaller ones. The tiger shark has the least selective diet of all sharks. Most species are not highly specialized in their feeding habits, but hammerheads are known to have a particular predilection for stingrays.
Reproductive biology
Carcharhiniform sharks are either oviparous (egg layers) or viviparous (giving birth to live young). Oviparous species deposit egg cases that contain the developing embryo along with its yolk reserves (in the yolk sac). These species include the majority of the catsharks (Scyliorhinidae, except Cephalurus and possibly some Halaelurus species) and Proscyllium habereri (Proscylliidae). The egg cases are secreted by the nidamental gland in the upper oviduct and usually are amber to greenish in color, with tendrils at the extremities that serve to anchor them to the substrate. In species with retained oviparity, the egg cases remain for a longer period in the uterus, with most embryonic development taking place inside the mother. In other oviparous species, the eggs are laid shortly after they are formed (less than one month in some cases), and most development of the fetus, which may take up to one year, occurs inside the egg cases in the environment.
Slightly more than half of carcharhiniform species are viviparous. Viviparous species can be yolk sac viviparous (ovoviviparous or aplacentally viviparous—the young deriving nourishment solely from the yolk sac, such as in the tiger shark, Galeocerdo), but many viviparous species form maternal-fetal connections in the form of yolk sac placentae. In these cases, the yolk sacs are modified into highly vascularized, nutrient-supplying structures fused to the internal uterine walls. Placentae are formed in the Hemigaleidae, Carcharhinidae (except Galeocerdo), Sphyrnidae, and some triakid species.
Gestation periods vary considerably; oviparous species lay eggs after a short gestation of just a few weeks, but some viviparous species retain the embryos for more than a year.
Litters vary from one to 135 per gestation. In many species, females give birth in shallow nursery areas. Males bite females during courtship, and mating has been observed in the wild for a few species (such as the whitetip reef shark, Triaenodon obesus). There is no parental care after birth.
Conservation status
The following species are listed by the IUCN: Glyphis gangeticus (as Critically Endangered); Carcharhinus melanopterus, C. borneensis, and Glyphis glyphis (as Endangered); Galeorhinus galeus (as Vulnerable); Mustelus antarcticus (as Lower Risk/Conservation Dependent); C. amboinensis (southwestern Indian Ocean subpopulation only), C. amblyrhynchoides, C. amblyrhynchos, C. brevipinna, C. leucas, C. limbatus, C. longimanus, C. melanopterus, C. obscurus, C. plumbeus (northwestern Atlantic subpopulation only), Furgaleus macki, Galeocerdo cuvier, Negaprion brevirostris, Poroderma africanum, Prionace glauca, Scoliodon laticaudus, Triaenodon obesus, Triakis megalopterus, and T. semifasciata (as Lower Risk/Near Threatened); C. brevipinna (northwestern Atlantic subpopulation only), C. hemiodon, C. limbatus (northwestern Atlantic subpopulation only), C. obscurus (northwestern Atlantic and Gulf of Mexico subpopulation only), and Galeorhinus galeus (as Vulnerable); and C. amboinensis and Smyrna mokarran (as Data Deficient).
Significance to humans
Ground sharks are fished intensely, both for food and recreationally. Because they are abundant in shallow and oceanic waters, ground sharks frequently are fished by trawlers and longlines and are either targeted directly or captured as bycatch. Their flesh is marketed frozen, fresh, dried-salted, smoked, and even canned for human consumption. Their skin is used for leather products, their fins for the Chinese shark fin soup industry, their carcasses for fishmeal, and their liver oil for the extraction of vitamin A (in decline as vitamins are synthesized). Tourists often procure trophies, in the form of jaws and teeth. Recreational fisheries and angling tournaments capture large quantities of ground sharks, especially tiger sharks in shallow waters and blue sharks in oceanic settings. Internal fertilization, long gestation periods, production of few offspring, and relatively advanced ages at sexual maturity are all factors that constrain the exploitation of shark populations.
Ground sharks have been implicated in numerous shark attacks, especially the tiger and bull sharks, which account for more than 50% of shark attacks worldwide. This proportion is to be expected because of the high number of carcharhiniform species and their shallow-water predominance.
Carcharhiniforms also are very important in the growing ecotourism market. Many species can be encountered in the wild through commercial operations that specialize in taking tourists to areas where specific carcharhiniform species are common. These operations are worldwide, and surveys indicate that shark watching is a highly profitable enterprise. Certain ground shark species are common in public aquaria as well, especially Triaenodon obesus, Carcharhinus plumbeus, and Triakis semifasciata.
Species accounts
Gray reef sharkBull shark
Oceanic whitetip shark
Tiger shark
Ganges shark
Lemon shark
Blue shark
False catshark
Swellshark
Pajama catshark
Chain catshark
Great hammerhead shark
Bonnethead shark
Leopard shark
Resources
Books:Bigelow, H. B., and W. C. Schroeder. "Sharks." In Fishes of the Western North Atlantic, edited by J. Tee-Van, C. M. Breder, S. F. Hildebrand, A. E. Parr, and W. C. Schroeder. New Haven, CT: Sears Foundation for Marine Research, Yale University, 1948.
Branstetter, S., ed. Conservation Biology of Elasmobranchs. NOAA Technical Report, NMFS 115. Seattle: U.S. Department of Commerce, 1993.
Cappetta, H. Chondrichthyes II: Mesozoic and Caenozoic Elasmobranchii. Handbook of Palaeoichthyology, vol. 3B. Stuttgart and New York: Gustav Fischer Verlag, 1987.
Carwardine, Mark, and Ken Watterson. The Shark Watcher's Handbook: A Guide to Sharks and Where to See Them. Princeton: Princeton University Press: 2002.
Compagno, L. J. V. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. FAO Species Catalogue, vol. 4, part 1. Rome: Food and Agriculture Organization of the United Nations, 1984. ——. Sharks of the Order Carcharhiniformes. Princeton: Princeton University Press, 1988.
Compagno, L. J. V., and V. H. Niem. "Families Scyliorhinidae, Proscylliidae, Pseudotriakidae, Triakidae, Hemigaleidae, Carcharhinidae, Sphyrnidae." In Western Central Pacific Identification Sheets to Species, edited by K. E. Carpenter and V. H. Niem. Rome: Food and Agriculture Organization of the United Nations, 1999.
Compagno, L. J. V., C. Simpfendorfer, J. E. McCosker, K. Holland, C. Lowe, B. Wetherbee, A. Bush, and C. Meyer. Sharks. Pleasantville, New York: Reader's Digest Association, Inc., 1998.
Hamlett, W. C., ed. Sharks, Skates, and Rays: The Biology of Elasmobranch Fishes. Baltimore: Johns Hopkins University Press, 1999.
Hennemann, Raof M. Sharks and Rays: Elasmobranch Guide of the World. Frankfurt: Ikan, 2001.
Last, P. R., and J. D. Stevens. Sharks and Rays of Australia. Melbourne, Australia: CSIRO, 1994.
Myrberg, Arthur A., Jr., and Donald R. Nelson. "The Behavior of Sharks: What Have We Learned?" In Discovering Sharks, edited by S. H. Gruber. Highlands, NJ: American Littoral Society, 1990.
Perrine, D. Sharks and Rays of the World. Stillwater, MN: Voyager Press, 1999.
Pratt, H. L. Jr., S. H. Gruber, and T. Taniuchi, eds. Elasmobranchs as Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries. Proceedings of the Second United States–Japan Workshop East-West Center, Honolulu, Hawaii, 9–14 December 1987. NOAA Technical Report NMFS 90. Seattle: U.S. Department of Commerce, 1990.
Randall, J. E. "Review of the Biology of the Tiger Shark (Galeocerdo cuvier)." In Sharks: Biology and Fisheries, edited by J. G. Pepperell. Melbourne, Australia: CSIRO, 1992.
Springer, S. "Social Organization in Shark Populations." In Sharks, Skates, and Rays, edited by P. W. Gilbert, R. F. Mathewson, and D. P. Rall. Baltimore: Johns Hopkins University Press, 1967.
Springer, Victor G., and Joy P. Gold. Sharks in Question: The Smithsonian Answer Book. Washington, DC: Smithsonian Institution Press, 1989.
Tricas, T. C., and S. H. Gruber. The Behavior and Sensory Biology of Elasmobranch Fishes: An Anthology in Memory of Donald Richard Nelson. Developments in Environmental Biology of Fishes, vol. 20. Dordrecht, Netherlands: Kluwer Academic Publishers, 2001.
Whitley, G. P. The Fishes of Australia. Part 1. The Sharks, Rays, Devil-fish, and Other Primitive Fishes of Australia and New Zealand. Sydney: Royal Zoological Society of New South Wales, 1940.
Wetherbee, B. M., S. H. Gruber, and E. Cortes. "Diet, Feeding Habits, Digestion, and Consumption in Sharks, with Special Reference to the Lemon Shark, Negaprion brevirostris." In Elasmobranchs as Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries. Proceedings of the Second United States–Japan Workshop East-West Center, Honolulu, Hawaii, 9–14 December 1987, edited by H. L. Pratt, S. H. Gruber, and T. Taniuchi. NOAA Technical Report, NMFS 90. Seattle: U.S. Department of Commerce, 1990.
Wourms, J., and L. Demski. Reproduction and Development of Sharks, Skates, Rays and Ratfishes. Developments in Environmental Biology of Fishes, vol. 14. Dordrecht, Netherlands: Kluwer Academic Publishers, 1993.
Periodicals:Johnson, R. H., and D. R. Nelson. "Agonistic Display in the Gray Reef Shark, Carcharhinus menisorrah, and Its Relationship to Attacks on Man." Copeia 1973, no. 1 (1973): 45–55. ——. "Copulations and Possible Olfaction-Mediated Pair Formation in Two Species of Carcharhinid Sharks." Copeia 1978 (1978): 539–542.
Motta, Phillip J., Robert E. Hueter, and Timothy C. Tricas. "An Electromyographic Analysis of the Biting Mechanism of the Lemon Shark, Negaprion brevirostris: Functional and Evolutionary Implications." Journal of Morphology 210(1991): 55–69.
Myrberg, A. A., and S. H. Gruber. "The Behavior of the Bonnethead Shark, Sphyrna tiburo." Copeia 1974, no. 2(1974): 358–374.
Nelson, D. R. "Aggression in Sharks: Is the Grey Reef Shark Different?" Oceanus 24, no. 4 (1981): 45–55.
Nelson, D. R., and R. H. Johnson. "Behavior of Reef Sharks of Rangiroa, French Polynesia." National Geographic Society Research Reports 12 (1980): 479–499.
Strong, W. R. Jr., F. F. Snelson Jr., and S. H. Gruber. "Hammerhead Shark Predation on Stingrays: An Observation of Prey Handling by Sphyrna mokarran." Copeia 1990, no. 3 (1990): 836–840.
Tricas, T. C., Taylor, L., and G. Naftel. "Diel Behavior of the Tiger Shark, Galeocerdo cuvier, at French Frigate Shoals, Hawaiian Islands." Copeia 1981, no. 4 (1981): 904–908.
Wourms, J. P. "Reproduction and Development in Chondrichthyan Fishes." American Zoologist 17 (1977): 379–410.
Organizations:American Elasmobranch Society, Florida Museum of Natural History. Gainesville, FL 32611 USA. Web site:
Other:"2002 IUCN Red List of Threatened Species." (26 Dec. 2002).
"Fish-Base." 16 Dec. 2002 (26 Dec. 2002).
"Catalog of Fishes On-line." 12 Nov. 2002 (26 Dec. 2002).
"Reef Quest Expeditions." (26 Dec. 2002).
[Article by: Marcelo Carvalho, PhD]
