Heterodontiformes

(Bullhead or horn sharks)

Class Chondrichthyes

Order Heterodontiformes

Number of families 1

Evolution and systematics

The earliest fossil bullhead (or horn) shark known from articulated specimens is from the marine late Jurassic strata of Solnhofen, southern Germany (about 150 million years old). However, fragmentary remains are known from the early Jurassic of Germany, and most fossil bullhead species have been described from isolated teeth or finspines from Cretaceous and Tertiary deposits of Europe, North and South America, Australia, and Africa. These fossils indicate that bullhead sharks have occupied shallow marine environments throughout their long history.

Bullhead sharks are part of the superorder Galeomorphii, a group that also contains the carpet sharks (Orectolobiformes), mackerel sharks (Lamniformes), and ground sharks (Carcharhiniformes). These orders have the hyomandibular fossa closely adjacent to the orbit on the neurocranium (this fossa, or depression, anchors the hyomandibula, a cartilage that connects distally to the jaw joint, to the skull). Bullhead sharks were believed to be closely related to more primitive Mesozoic hybodont sharks (which also had dorsal finspines), and therefore considered to be living relics, but it is now well established that bullheads share a common ancestry with modern (galeomorph) sharks. However, the phylogenetic relationships among bullhead species have not been satisfactorily studied. All bullhead species are classified in the single family Heterodontidae.

Eight living species of bullheads are currently recognized, all in the single genus Heterodontus. Most species have been described in the mid- to late nineteenth century, but H. portusjacksoni was described in 1793, and two species have been discovered and named in the twentieth century (in 1949 and 1972). Additionally, there is one undescribed species of bullhead shark off southern Oman, in the northwestern Arabian Sea. Most living species of bullheads have been relatively well characterized, but some species (such as H. portusjacksoni) are far better known than others (such as H. ramalheira).

Physical characteristics

Bullhead sharks have a tapered profile due to their large, bulky heads. Their snouts are blunt, short, and rounded. Bullheads also have prominent supraorbital ridges (elevated crests supporting the eyes), which provide a greater range of vision, possibly an advantage for bottom-dwelling sharks. Bullheads have two relatively large dorsal fins (the first is clearly larger than the second), each preceded by a short finspine. The fin-spine in embryos is blunt so as to not harm the mother, but relatively sharp in adults. The caudal fin is robust, with a prominent notch separating the upper and lower lobes. There are five pairs of gill slits. Bullheads are covered with large, abrasive dermal denticles, which are visible without magnification.

Bullheads are the only living sharks with a finspine preceding each dorsal fin in combination with presenting an anal fin. They also have unique dentitions, with small anterior teeth endowed with small cusps for clutching prey, contrasting to the more posterior tooth rows where the teeth are flattened and enlarged (up to 0.4 in/1 cm wide), adapted for grinding hard-shelled invertebrates (hence the generic name Heterodontus, meaning "having different teeth"). Their nostrils are also unique, being very large and circular, providing

them with a well-developed sense of smell that is also important for bottom-dwelling species.

Coloration is helpful to distinguish among bullhead species. Three species present light-brown to grayish-brown background coloration with darker-brown spots on the head, body, fins, and tail (H. francisci, H. quoyi, and H. mexicanus) but the arrangement, number, and diameter of the spots is usually distinct for these species. Heterodontus ramalheira is unique in having a reddish-brown background with creamy-white, minute spots. Heterodontus japonicus and H. galeatus have dark saddlelike markings on their dorsal surfaces (and also over the eyes and underneath the first dorsal fin in the latter species), both with lighter background colors. Heterodontus portusjacksoni is unique in the genus in presenting a horizontal pattern of brownish-black stripes. However, the most spectacular of all bullhead species, and one of the most ornate sharks known, is H. zebra, with an intense, dark brownish-black vertical-stripe pattern from head to tail and over the pectoral fins, with some of the stripes coupled together along the sides of the trunk.

Bullheads are only average-sized sharks, reaching from 28–51 in (70–130 cm) long, but a few species may reach slightly larger sizes. Most species are sexually mature when between 15.7–28 in (40–70 cm) long for males, and slightly larger for females.

Distribution

Three species are present in the tropical eastern Pacific: H. francisci; H. mexicanus, distributed in the Gulf of California, along the Central American coast down to Colombia and possibly Peru; and H. quoyi, found in the Galápagos Islands and the coasts of Ecuador and Peru. Two species are Australian: H. galeatus (eastern Australia and perhaps in Tasmania and off Cape York) and H. portusjacksoni (southern [including Tasmania], western, and eastern Australia, and possibly in New Zealand). Heterodontus ramalheira occurs along the eastern African coast extending northward to the Arabian Peninsula; H. japonicus is a western Pacific species, occurring around Japan, Korea, and off the Chinese coast; H. zebra is somewhat widespread in the western Pacific, distributed from Japan and Korea down to Vietnam, with records also in Indonesia and northwestern Australia.

Habitat

Bullheads inhabit the continental shelf, usually in shallow waters from the intertidal zone down to about 328 ft (100 m), and less frequently at greater depths (to 820 ft/250 m for H. ramalheira and H. portusjacksoni). They occur on hard and soft bottoms, including reefs, rocky, and sandy substrates, and commonly frequent caves, crevices, and kelp and sea grass beds.

Behavior

Bullheads are more active nocturnally, as are many benthic sharks. They are usually solitary, although recently born individuals may group together for a small period before going their separate ways, and aggregations of adults have been observed in some species. Their strong pectoral fins are used to "walk" over the substrate. In the most-studied species, (H. portusjacksoni), adults tend to occupy a restricted range, returning to the same resting location daily, and there is a certain degree of territoriality and competition for favored resting caves. Courtship patterns have been observed in H. francisci. At least one species, H. portusjacksoni, appears to be migratory, returning to breeding sites after periods spent in deeper waters.

Feeding ecology and diet

Bullheads consume abundant amounts of hard-shelled benthic invertebrates, including crabs, lobsters, shrimp, barnacles, starfish, urchins, gastropods, and polychaetes. Most species also eat fishes. Smaller individuals eat softer prey items while their molariform posterior teeth are still in development. Bullhead sharks commonly employ strong suction feeding. One bullhead shark has been found in the stomach of a tiger shark, but they are generally avoided as prey because of their finspines.

Reproductive biology

All bullhead sharks have internal fertilization and are oviparous (egg-laying), laying large, spiral-rimmed egg cases. The fully formed egg cases are expelled rather early by females, so that most fetal development occurs in the egg cases while in the environment, not inside the mother. Young hatch from between five and 12 months after being laid, one per egg case, and measure about 3.9–5.5 in (10–14 cm). The young often move into nursery areas or bays after hatching. The egg cases are laid in shallow water, sometimes in unguarded "nests" (H. japonicus), and usually in protected kelp beds or enclosed in protected areas (the egg may be carried and lodged by the mother, using her mouth, in a crevice). Adults have been observed to eat their own egg cases.

Conservation status

Not threatened.

Significance to humans

Their significance is mostly recreational (e.g., when observed by divers), as bullheads are not consumed on a regular basis. They are caught as bycatch in bottom trawls and usually discarded, but they may be occasionally consumed or used as fishmeal (off eastern Mexico, for example). Various species of bullheads are commonly kept in public and private aquaria, where they can be maintained successfully for over a decade.

Species accounts

List of Species

California bullhead shark

Heterodontus francisci

family

Heterodontidae

taxonomy

Cestracion francisci Girard, 1854, California (Monterey Bay).

other common names

English: Bullhead shark, horn shark; Spanish: Dormilón cornudo.

physical characteristics

Background gray or light brown with smaller darker brown spots (smaller than eyes) scattered over body, head, fins, and tail. The young have more intense coloration, sometimes with darker bands in between eyes and on fins. The supraorbital ridges are moderately high; finspines relatively tall, but dorsal fins are not as tall as in H. zebra and H. japonicus.

distribution

California bullhead sharks occur off central and southern California and Mexico (Baja California and Gulf of California), extending south possibly to Ecuador and Peru. During warm water influxes, they may reach as far north as San Francisco Bay.

habitat

These sharks commonly inhabit from 6.6 to 33 ft (2–10 m), even though they can be found from the intertidal zone down to about 490 ft (150 m). Juveniles are usually in shallower waters, over sandy surfaces. These fishes occur on rocky and sandy bottoms, kelp forests, and in caves and crevices.

behavior

These sharks are nocturnal, sluggish, and mostly solitary, preferring the protection of caves and shelters during the day, and

hunting mostly at night. They can remain in a relatively small home range for much of the summer, moving into deeper waters in the winter, at least in some regions. Experiments demonstrate that their diel (24 hours, including one day and night) activity patterns appear to be regulated by light.

feeding ecology and diet

California bullhead sharks eat many different invertebrates, including sea urchins, crabs, shrimp, isopods, octopuses, anemones, bivalves, gastropods, polychaetes, and occasionally fishes (at least pipefishes [Syngnathidae] and blacksmiths [Pomacentridae]). Specimens have been filmed devouring purple-colored urchins, turning their teeth and spines into a strong shade of purple. Recently born pups take about one month to begin feeding. Adults in aquaria have been observed consuming their own egg cases.

reproductive biology

The mating ritual of California bullhead sharks has been observed in captivity, particularly at the Steinhart Aquarium in San Francisco. Males pursue larger females until obtaining consent, and mating occurs on the bottom of the tank. The male grasps the female's pectoral fin with his teeth, and subsequently one clasper is inserted into the female after coiling around her. Copulation may last between 30 to 40 minutes, and in captivity the eggs are expelled one or two weeks later. In the wild, eggs can be expelled even after one to three months of copulation, as females can produce eggs for extended periods, and sperm is stored and utilized in stages. The young develop for between seven and nine months before hatching.

conservation status

A decrease in numbers of individuals has been noticed in regions of southern California where there is substantial diving activity, but the species is not listed by the IUCN as Threatened.

significance to humans

These sharks are very common in public aquaria, where mating, egg-laying, and hatching have been observed. In the wild, they are not considered a threat to humans. However, despite their apparent calm demeanor, H. francisci have been known to infrequently swim after and bite divers after being harassed by them.

Port Jackson shark

Heterodontus portusjacksoni

family

Heterodontidae

taxonomy

Squalus portus jacksoni Meyer, 1793, Australia (Botany Bay, New South Wales).

other common names

English: Bullhead shark, oyster crusher, tabbigaw.

physical characteristics

Port Jackson sharks are distinguished by a gray to brownish background with a harnesslike pattern of darker brown stripes over the pectoral fins and below the first dorsal fin, with a dark stripe across the head and eyes and a few dark oblique stripes

along the trunk. The supraorbital ridges are only moderately high. The finspines do not reach the dorsal fin tips, being rather blunt and short; and the dorsal fins are not nearly as high as in H. zebra and H. japonicus.

distribution

These sharks occur around the southern, western, and eastern Australian coast, including Tasmania. A single record exists for New Zealand, but this is possibly a stray.

habitat

Port Jackson sharks are common on the temperate Australian continental shelf and upper slope, from close inshore down to 902 ft (275 m).

behavior

Port Jackson sharks are nocturnal, occurring in caves and shelters during the day, and hunting at night. Seasonal migrations are frequent, and these may extend 528.2 mi (850 km) in one direction, after which they may return to the same localities each year. Migrations from Sydney to Tasmania have been reported. Captive juvenile Port Jackson sharks may grow 2–2.4 in (5–6 cm) per year; adults grow slightly less at 0.8–1.6 in (2–4 cm) per year. They take in water for respiration through the first gill slit while feeding, freeing their mouths for eating, as water exits from the remaining gill slits.

feeding ecology and diet

These sharks primarily eat benthic invertebrates, especially echinoderms, but prey items include crabs, shrimp, starfish, bivalves, gastropods, polychaetes, and small fishes.

reproductive biology

These sharks segregate by size after hatching, but adults have been reported to segregate by sex. Adult males move into deeper water toward the end of the breeding season in winter, and adult females migrate shortly thereafter. Females lay from 10 to 16 egg cases in rocky substrates, in sheltered, shallow areas (ranging from 4 to 98 ft [1–30 m], but more commonly from 4 to 16 ft [1–5 m]). Females may utilize the same nesting sites repeatedly, and some have been observed to purposely wedge their egg cases into crevices. Adults may eat their egg cases. The young hatch after nine to twelve months, and quickly move into nursery areas. Maturity ages vary from eight to ten years for males and from eleven to fourteen years for females.

conservation status

Not threatened.

significance to humans

Port Jackson sharks are taken as by catch in benthic or demersal fisheries, but are not generally consumed. They are very common in public aquaria. The Port Jackson shark is perhaps the best known of all bullhead species, and is not dangerous to humans, although caution is necessary when approaching them.

Resources

Books

Cappetta, H. Chondrichthyes II, Mesozoic and Cenozoic Elasmobranchii. Stuttgart: Gustav Fischer Verlag, 1987.

Compagno, L. J. V. Sharks of the World. An Annotated and Illustrated Catalogue of Shark Species Known to Date. Vol. 2, Bullhead, Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes). Rome: Food and Agriculture Organization of the United Nations, 2001.

Hennemann, R. 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.

Nelson, J. Fishes of the World, 3rd ed. New York: John Wiley & Sons, 1994.

Springer, V. G., and J. P. Gold. Sharks in Question. The Smithsonian Answer Book. Washington, DC: Smithsonian Institution Press, 1989.

Whitley, G. P. The Fishes of Australia. Part 1, The Sharks, Rays, Devil-Fish, and Other Primitive Fishes of Australia and New Zealand. Sydney, Australia: Royal Zoological Society of New South Wales, 1940.

Periodicals

Compagno, L. J. V. "Phyletic Relationships of Living Sharks and Rays." American Zoologist 17 (1977): 303–322.

Edmonds, M.A., P.J. Motta, and R.E. Hueter. "Food Capture Kinematics of the Suction Feeding Horn Shark, Heterodontus fancisci." Environmental Biology of Fishes 62 (2001): 415–427.

Luer, C. A., and P. W. Gilbert. "Elasmobranch Fish: Oviparous, Viviparous, and Ovoviviparous." Oceanus Magazine 34, no. 3 (1991): 47–53.

Maisey, J. G. "Fossil Hornshark Finspines (Elasmobranchii; Heterodontidae) with Notes on a New Species (Heterodontus tuberculatus)." Neues Jahrbuch für Geologie und Paläontologie 164, no. 3 (1982): 393–413.

Smith, B. G. "The Heterodontid Sharks: Their Natural History, and the External Development of Heterodontus japonicus Based on Notes and Drawings by Bashford Dean." In Bashford Dean Memorial Volume: Archaic Fishes, vol. VIII. New York: American Museum of Natural History, 1942: 649–770, plates 1–7.

Organizations

American Elasmobranch Society, Florida Museum of Natural History. Gainesville, FL 32611 USA. Web site: <http://www.flmnh.ufl.edu/fish/Organizations/aes/aes.htm>

Other

FishBase. August 8, 2002 (cited October 10, 2002). <http://www.fishbase.org/search.cfm>

The Catalog of Fishes On-Line. February 15, 2002 (cited October 17, 2002). <http://www.calacademy.org/research/ichthyology/catalog/fishcatsearch.html>

Marcelo Carvalho, PhD