Ceratodontiformes

(Australian lungfish)

Class Sarcopterygii

Order Ceratodontiformes

Number of families 1

Evolution and systematics

The Australian lungfish is one of the most ancient living species of fishes (indeed, of vertebrates), as fossil remains belonging to Neoceratodus forsteri from the early Cretaceous of northern New South Wales are known, giving it a time span of close to 100 million years. The family Ceratodontidae, to which the Australian lungfish belongs, contains other fossil species (known mostly from toothplates), which date from the early Triassic. Many of these fossils, such as those of the genus Ceratodus, were more widespread than Neoceratodus and occurred circumglobally. Neoceratodus is therefore a survivor of a much more successful and ancient lineage. Current opinion diverges in relation to its ancestry, whether it is more closely related to extinct lungfishes of the family Ceratodontidae (the most likely scenario) or to the other living lung-fishes of South America (Lepidosiren) and Africa (Protopterus), in which case Neoceratodus would be placed in its own family, Neoceratodontidae.

When first discovered and described by Johann L. G. Krefft in 1870 (as Ceratodus forsteri), the Australian lungfish was thought to be an ("gigantic") amphibian, similar to the circumstances surrounding the description of the South American lungfish 33 years before, even though many zoologists regarded Lepidosiren as a true "fish" by the mid-nineteenth century. Neoceratodus eventually found its place among the Dipnoi, the group containing all lungfishes, both fossil and living (established previously in 1844 by the German zoologist Johannes Müller). The Dipnoi presently contains some 280 fossil species and 60 fossil genera, originating in the early Devonian, in addition to the six species and three genera that are living today. Many of these fossils are known from well-preserved skeletons (some preserved three-dimensionally, such as Griphognathus and Chirodipterus from Gogo, Australia), but at least half of the species are known only from isolated toothplates. Lungfishes achieved their greatest diversity in the Devonian, when most (if not all) lungfish taxa were marine; living lungfishes are restricted to freshwater.

The systematic position of the Dipnoi among the vertebrates is still being debated. In a landmark study in 1981, Donn E. Rosen and collaborators placed the lungfishes as the closest relatives of the tetrapods (land vertebrates), challenging the widely held belief that certain "rhipidistians" (a heterogeneous group of fossil lobe-finned fishes) were their nearest ancestors. Current views on the ancestry of the tetrapods, based on morphological studies, indicate that lungfishes are their closest relatives if only living taxa are taken into account, but that other extinct groups of lobe-finned, fish-like vertebrates (rhizodonts, osteolepids, Eusthenopteron, and "elpistostegids" such as Panderichthys) are actually more closely related to tetrapods when all fossil evidence is considered; molecular data bearing on this issue are still controversial. The exclusively Devonian group Porolepiformes, which had pectoral fins anatomically similar to Neoceratodus; e.g. Holoptychius, is considered by many researchers to be the closest relative of the Dipnoi.

Physical characteristics

Neoceratodus forsteri is morphologically unique, presenting paddle-like or leaf-like pectoral fins that are fleshy and stout at their bases; the pelvic fins are similar, but smaller and not as fleshy as the pectorals. Their heads are wide and slightly depressed, with a terminal mouth. The nostrils are internal, composed of two small openings inside the labial cavity, which are followed by a pair of posterior openings in the roof of the mouth (choanae). The trunk is long and muscular and is laterally compressed, with a protocercal caudal fin that is posteriorly pointed and continuous with both the dorsal and anal fins. Their scales are remarkably large (but rather thin),

overlapping and posteriorly rounded. The teeth are fused into toothplates, two pairs of which are positioned in the roof of the mouth, and one pair on either side of the tongue on the mouth floor; the posterior toothplates are ridged, and in juveniles they are trilobed.

The single lung (a modified swim bladder) is large; highly vascularized and internally divided into two chambers; and connects with the esophagus ventrolaterally. The gills open into a large opercular chamber just ahead of the pectoral fins. Sensory canals of the lateral-line system are visible dorsally on the head and nape (but not as much as in the South American and African lungfishes), and the lateral line runs posteriorly at midheight to the tip of the tail. Large sensory pores are present on the snout and around the eyes. Their skeletons are mostly cartilaginous, in contrast to fossil lungfishes, which were more heavily ossified. Dorsally and laterally, the Australian lungfish is olive to dark greenish brown in color, but ventrally creamy-yellow or even pinkish. Many specimens also have darker blotches dorsolaterally on the tail, especially juveniles.

Distribution

Very restricted in distribution; present only in Queensland, Australia. When the continent was first colonized, this species was already restricted to the Mary and Burnett River systems, but it was subsequently introduced, successfully, into other rivers of southeastern Queensland, such as the Albert, Brisbane, Coomer, Fitzroy and Stanley Rivers, and also in the Enoggera Reservoir, where it is reported to be abundant.

Habitat

Often found in deep pools in still, slow moving rivers. Its ability to absorb oxygen periodically directly from the air enables it to live in rather stagnant waters. The rivers inhabited by Neoceratodus are typically calm and slow moving, with mud, sand, or gravel bottoms, and with plenty of marginal and aquatic vegetation, important for spawning.

Behavior

Mostly sluggish, but capable of quick bursts of speed in pursuit of prey or when threatened. Vision is reportedly poor, as captive specimens have been known to swim into obstacles, but they are known to hunt prey items mostly at night, using electroreception and a refined sense of smell. The single lung allows Neoceratodus to breathe air occasionally, but it breathes primarily through its gills and only ascends to the surface to gulp air when water conditions are poor or when the gills are clogged with mud or other debris. In their natural habitat, individuals have been observed to swallow air at intervals of 30 to 60 minutes, emitting a particular sound when air is exhaled. Juveniles and especially hatchlings are also capable of absorbing oxygen through the skin. Neoceratodus does not estivate (bury itself in a muddy burrow to wait for the rainy season), as do the South American and African lungfishes, and consequently it cannot remain alive out of water for periods greater than a few days, even if kept wet and in the shade.

Feeding ecology and diet

Essentially carnivorous, eating frogs, other fishes, and invertebrates such as insect larvae, earthworms, snails, and freshwater crustaceans. However, it has also been reported to eat both aquatic and terrestrial plants and even native fruits that have fallen into rivers. Prey items are captured through suction and crushed by the toothplates. The pectoral fins allow them to brace themselves when foraging for prey. Larvae and juveniles of Neoceratodus are preyed upon by insect larvae, fishes, and fish-eating birds.

Reproductive biology

Reproduction occurs in shallow, warm waters before the summer rainy season. Complex courtship behaviors have been recorded; the pair is not easily distracted. A male and female remain in close association, as the male nudges the cloacal area of the female to stimulate her. Fertilization is external. Spawning may take up to one hour after the pair has chosen a site, usually a patch of aquatic plants. Fifty to 100 sticky eggs are laid on plants, to which they adhere. There is no guarding of the eggs or the young. The eggs are small, spherical, and enveloped by a gelatinous substance. Larvae emerge from the eggs after a period of some three weeks but remain close to them for shelter for some 10 days following. After 41 to 56 days, the yolk disappears and the larvae begin to feed, probably on insect larvae or other small invertebrates. The hatchlings do not have external gills but are capable of breathing air at a very small size, 0.98 in (2.5 cm). A size of 9.8 in (25 cm) is attained after six months, and 19.7 in (50 cm) after 20 months. They resemble adults after approximately six months.

Conservation status

This species is fully protected under CITES (Appendix 2) legislation and cannot be collected without special permit; it is not listed by the IUCN.

Significance to humans

Reported to adapt well to captivity, Neoceratodus is common in public aquaria. One specimen lived for more than 50 years in captivity at the Shedd Aquarium in Chicago. It is not consumed. In a more anthropocentric vein, Neoceratodus, along with the other living lungfishes and the living coelacanths, Latimeria chalumnae and L. menadoensis, are of special interest, and are given high profiles in museum exhibits and evolutionary biology textbooks because of their close ancestral ties to land vertebrates, including humans. They are more closely related to tetrapods than they are to the remaining fishes.

Resources

Books

Allen. G. R. Freshwater Fishes of Australia. Neptune City, NJ: T. H. F. Publications, 1989.

Bemis, William E., Warren W. Burggren, and Norman E. Kemp. The Biology and Evolution of Lungfishes. New York: A.R. Liss, 1987.

Berra, Tim M. Freshwater Fish Distribution. San Diego, CA: Academic Press, 2001.

Bruton, M. N. "Lungfishes and Coelacanth." In Encyclopedia of Fishes, edited by John R. Paxton and William N. Eschmeyer. San Diego, CA: Academic Press, 1994.

Cloutier, R., and P. E. Ahlberg. "Morphology, Characters, and the Interrelationships of Basal Sarcopterygians." In Interrelationships of Fishes, edited by Melanie L. J. Stiassny, Lynne Parenti, and G. David Johnson. San Diego, CA: Academic Press, 1996.

Conant, E. B. "Bibliography of Lungfishes, 1811–1985." In The Biology and Evolution of Lungfishes, edited by William E. Bemis, Warren W. Burggren, and Norman E. Kemp. New York: A. R. Liss, 1987.

Graham, Jeffrey B. Air-breathing Fishes: Evolution, Diversity, and Adaptation. San Diego, CA: Academic Press, 1997.

Janvier, Philippe. Early Vertebrates. New York: Oxford University Press, 1996.

Kemp, Norman E. "The Biology of the Australian Lungfish, Neoceratodus forsteri (Krefft, 1870)." In The Biology and Evolution of Lungfishes, edited by William E. Bemis, Warren W. Burggren, and Norman E. Kemp. New York: A. R. Liss, 1987.

Merrick, J. R., and G. E. Schmida. Australian Freshwater Fishes: Biology and Management. North Ryde, N.S.W., Australia: J.R. Merrick, 1984.

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

Periodicals

Bartsch, P. "Development of the Cranium of Neoceratodus forsteri, with a Discussion of the Suspensorium and the Opercular Apparatus in Dipnoi." Zoomorphology 114 (1994): 1–31.

Bemis, William E. "Paedomorphosis and the Evolution of the Dipnoi." Paleobiology 10, no. 3 (1984): 293–307.

Kemp, Norman E. "The Embryological Development of the Queensland Lungfish, Neoceratodus forsteri (Krefft)." Memoirs of the Queensland Museum 20, no.3 (1982): 553–597.

Kemp, Norman E., and R. E. Molnar. "Neoceratodus forsteri from the Lower Cretaceous of New South Wales, Australia." Journal of Paleontology 55, no. 1 (1981): 211–217.

Miles, R. S. "Dipnoan (Lungfish) Skulls and the Relationships of the Group: A Study Based on New Specimens from the Devonian of Australia." Zoological Journal of the Linnaean Society 61 (1977): 1–328.

Rosen, D. E., et al. "Lungfishes, Tetrapods, Paleontology, and Plesiomorphy." Bulletin of the American Museum of Natural History 167, no. 4 (1981): 163–275.

Other

"Sarcopterygii: Dipnomorpha." Palaeos: The Trace of Life on Earth. October 6, 2002 (cited January 19, 2003). <http://www.palaeos.com/Vertebrates/Units/Unit140/200.html>

Watt, Michael, Christopher S. Evans, and Jean M. P. Joss. Use of Electroreception During Foraging by the Australian Lungfish. October 6, 2002 (cited January 19, 2003). <http://galliform.bhs.mq.edu.au/Watt_et_al.html>

Marcelo Carvalho, PhD