Lepidosireniformes (Lungfishes)

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Lepidosireniformes

(Lungfishes)

Class Sarcopterygii

Order Lepidosireniformes

Number of families 2

Evolution and systematics

The South American lungfish (Lepidosiren paradoxa) was the first lungfish species to be described (in 1837 by Leopold J. F. J. Fitzinger; 1802–1884). It was originally discovered and collected from the Amazon River by Johann Natterer (1787–1843), a dedicated and gifted Austrian naturalist who collected extensively in Brazil from 1817–1835. The first African lungfish was described shortly thereafter in 1839 by the British anatomist Richard Owen (1810–1890), who firmly believed that lungfishes were true "fishes" and not amphibians, mostly on the basis of his erroneous conviction that lungfishes did not have a second (internal) nostril (known as a choana) or a divided auricle. Zoologists of the mid-nineteenth century were divided about the ancestry of lungfishes, wondering whether they were more closely related to amphibians or to other bony fishes. It is now well established that lungfishes belong to a higher group, the Sarcopterygii, which also includes the tetrapods, coelacanths, and many other lobe-finned fossil fishes, and are therefore unequivocally more closely related to land vertebrates than to ray-finned bony fishes (Actinopterygii).

The genus Lepidosiren is monotypic, but detailed comparative studies of specimens from most of its extended range are needed (two other nominal species exist, but they are considered synonyms of L. paradoxa). Four species of African lung-fishes (Protopterus) are recognized: P. annectens, P. aethiopicus, P. dolloi, and P. amphibius. Some of these species are difficult to distinguish, and are in need of critical taxonomic evaluation, including the validity of certain subspecies (a total of 10 nominal species have been described); their evolutionary relationships to each other have yet to be fully investigated. Lepidosiren and Protopterus are placed in the same order, but are classified in distinct families. They are closely related to the Australian lungfish (Neoceratodus forsteri) and its immediate fossil relatives, while the vast majority of remaining fossil lungfishes are more distantly related (some 60 genera and 280 species and of lungfishes are known). Extant lungfishes are "living fossils," and belong to an ancient lineage, the Dipnoi, that was much more diverse in the Devonian (ca. 417–354 million years ago) and Triassic (ca. 248–205 million years ago) periods. Fossil relatives of Lepidosiren and Protopterus are known from the late Cretaceous of South America and Africa, respectively, and these genera, along with Neoceratodus, are among the oldest vertebrates living today.

Physical characteristics

South American and African lungfishes are morphologically similar, presenting elongated, eel-like bodies, with relatively small heads, and filamentous pectoral and pelvic fins. The pelvic fins are stouter than the pectorals in both genera; the pectorals are slightly more robust in Protopterus, and may resemble simple filaments in Lepidosiren. The caudal fin is confluent with the dorsal and anal fins (as in the Australian lung-fish), tapering distally. The body is compressed laterally, especially at the anus, but not as much as in Neoceratodus. The eyes are minute and the mouth is terminal, with a lateral groove extending to the sides of the head. Sensory canals on the head and cheek appear as sinuous, deep lines that extend posteriorly at midbody height towards the tail; sensory pores are also present on the head. The anus is asymmetrical, situated laterally just posterior to the pelvic fins, and not directly in the middle as in Neoceratodus (the side may vary among individuals of both Protopterus and Lepidosiren). The scales are mostly embedded in the skin and are very thin, but clearly visible. The nostrils are on the internal lip margin, and the teeth are fused into sharp tooth plates.

Both Lepidosiren and Protopterus have two highly vascularized and separated lungs (modified swim bladders), positioned on each side of the gut and connected to the esophagus ventrally,

as in tetrapods and bichirs (Polypteriformes). The lungs have many alveoli, similar to the lungs of tetrapods. The gill openings are small, not nearly as large as in Neoceratodus. Newly hatched individuals have flared external gill filaments, absent in Neoceratodus, and these may persist vestigially above the pectoral fins in subadults and adults of Protopterus. The skeleton is mostly cartilaginous. Both Protopterus and Lepidosiren vary slightly in color, from dark brown to deep gray dorsally and laterally, with many varied blotches and spots; usually dark ventrally, although Protopterus may be lighter ventrally. Lepidosiren may reach 4.1 ft (1.25 m) in length, while Protopterus varies from between 17.7 in (45 cm) (P. amphibius) to 6.5 ft (2 m) in length (P. aethiopicus, which can weigh some 37.5 lb [17 kg]).

Distribution

Lepidosiren has the greatest distribution of any extant lung-fish, occurring in many tributaries of the Amazon and Paraná-Paraguay River systems, as well as in French Guiana. Species of Protopterus are slightly more restricted. P. annectens is present in central and West Africa; P. aethiopicus occurs in central and East Africa; P. dolloi is restricted to the Congo basin; and P. amphibius occurs in coastal East Africa.

Habitat

The South American and African lungfishes are generally found in lentic (slow-moving) rivers, with plenty of associated vegetation and swampy, stagnant conditions (especially L. paradoxa). They can also be found in open lakes (e.g., P. aethiopicus in Lake Victoria); floodplains (e.g., P. dolloi in the Congo River basin, and P. annectens in the Senegal, Gambia, Niger, and Volta Rivers in West Africa); near river deltas (P. aethiopicus in Lake Tanganyika, P. amphibius in the Zambesi River delta); and in small pools.

Behavior

Lepidosiren and Protopterus species are sluggish, swimming through sinuous movements or by "crawling" on their pectoral and pelvic fins, especially to scavenge the bottom. Both genera are obligate air breathers, unlike Neoceratodus, which breathes primarily through the gills. Lepidosiren and Protopterus individuals will drown if forced to stay underwater, as the gill surfaces of these fishes are not large enough to satisfy their oxygen needs. Both genera also employ estivation, being capable of remaining inside a resting chamber for protracted periods during dry seasons and emerging when wet conditions return (estivation has been documented for Permian lungfishes, in the form of fossilized burrows). The degree of estivation varies among the species, but has been particularly well documented for P. annectens. The burrows are excavated by biting the soil and expelling mud through the gill openings. The fish will then turn around and remain with its head facing the burrow opening, from where it obtains oxygen. The individual suffers metabolic changes during this period to endure the lack of moisture (detailed below for P. annectens). One individual of P. aethiopicus remained in its cocoon for four years in captivity. Lungfishes do not feed during estivation. To sustain themselves, they initially metabolize fat reserves and then muscle mass.

Feeding ecology and diet

Lungfishes are mostly carnivorous, feeding mainly on invertebrates (insects, insect larvae, mollusks, crustaceans) but also on fishes and amphibians. Both genera may occasionally feed on aquatic plants. Lungfishes approach potential prey items through ambush or stalking, capturing them by quickly opening their mouths to create negative pressure that pulls them in. Little is known concerning their natural predators, but presumably larger carnivorous fishes and other vertebrates prey on lungfishes, especially when they are juveniles.

Reproductive biology

Spawning is usually seasonal, taking place during the wet season. Fertilization is external. In both genera the adult male guards and aerates the hatchlings and young temporarily. Female Protopterus usually lay eggs in burrows excavated by the males. The eggs are small (from 0.16–0.27 in/4–7 mm in diameter), and take one to two weeks to hatch, at which time they resemble tadpoles with slender, featherlike external gills. Only after a period from one month to 55 days do the larvae breathe air. At this stage, they range from 1 in (2.5 cm) to 1.6 in (4 cm) in length, and still have external gills. The larvae remain relatively inactive and are attached to the nest through their cement glands until their yolk reserves have been depleted, at which time they begin to forage for insect larvae and crustaceans and inhale air.

Conservation status

No species of Lepidosireniformes are listed by the IUCN.

Significance to humans

Lungfishes are common in both public and private aquaria. Although they are consumed as food in some parts of Africa, they are not important food fishes. They are harmless, but if provoked can inflict painful bites because of their strong jaws and sharp teeth.

Species accounts

List of Species

South American lungfish
African lungfish

South American lungfish

Lepidosiren paradoxa

family

Lepidosirenidae

taxonomy

Lepidosiren paradoxa Fitzinger, 1837, Amazon River; Brazil.

other common names

French: Anguille tété; German: Lurchfische; Portuguese: Pirambóia, peixe pulmonado.

physical characteristics

To 4.1 ft (1.25 m) in length. Usually dark brown (sometimes gray) with darker and lighter spots and blotches dorsally and laterally.

distribution

Most of the Amazon basin, from Peru to the Amazon River delta, and in the Paraná-Paraguay Rivers basin as far south as the La Plata system. Recently reported in French Guiana, and probably occurs elsewhere in tropical South America.

habitat

Swamps, slow-moving waters, floodplains, and pools.

behavior

An obligate air breather with reduced gills; can remain inactive for months during estivation, sometimes by closing the chamber

opening so as to prevent further desiccation. This species is very intolerant of the close proximity of conspecifics under aquarium conditions. It also may be hyperdispersed in the wild.

feeding ecology and diet

Feeds on insects, insect larvae, other invertebrates and fishes, as well as algae; reported to masticate prey before swallowing.

reproductive biology

Males present modified pelvic fins during reproduction, which develop featherlike protuberances that are highly vascularized and are believed to be accessory respiration organs, but it is not clear if they aid the adult or the larvae (or both). The male creates burrows in which the eggs are deposited and the larvae develop. Eggs are about 0.27 in (7 mm) in diameter. Hatchlings exhibit four pairs of external gills, and ventral adhesive glands anchor them in the burrow (both gills and adhesive glands are lost after six to eight weeks), after which they emerge to take their first breath of air, at about 1.6 in (4 cm) in length.

conservation status

Not threatened.

significance to humans

Not consumed regularly as food. Often displayed in public aquaria, where it can live for many years. Not widely kept by amateur aquarists and does not figure prominently in the ornamental fish trade.

African lungfish

Protopterus annectens

family

Protopteridae

taxonomy

Lepidosiren annectens Owen, 1839, Congo River. Two subspecies sometimes recognized.

other common names

German: Afrikanischer Lungerfische; Afrikaans: Longvis.

physical characteristics

Reaches 3.3 ft (1 m) in length. Separated from other Protopterus species by its relatively more slender head; 40–50 scales between operculum and anus, 36–40 scales around body anterior to dorsal fin origin; and 34–37 pairs of ribs. Olive to dark brown dorsally, lighter underneath, usually with spots and blotches on dorsal and lateral aspects.

distribution

Numerous rivers and lakes throughout central, South, and West Africa, e.g., the Senegal, Niger, Gambia, Volta, and Chad basins; the Chari River in Western Sudan; Bandama and Camoé basins in Côte d'Ivoire; Congo basin; the Zambezi and Incomati Rivers in South Africa. Also in Sierra Leone and Guinea, and the upper Nile basin.

habitat

Stagnant freshwater habitats, such as swamps and floodplains, also in more flowing rivers and streams.

behavior

Estivation is well documented. Individuals will "chew out" a burrow 1.2–9.8 in (30–250 mm) deep, expelling mud through their gill openings. They eventually turn to rest facing the entrance, forming a bulb-shaped chamber that contains water in its lower portion. They periodically extend forward to breathe air from the opening, returning to rest in mucus secreted in the water-filled portion of the chamber. Their metabolic activity decreases progressively as the chamber becomes drier, and the chamber may eventually solidify into a hard cocoon. They may remain for up to seven or eight months in this resting state, until moist conditions return. This species is solitary and hyperdispersed in nature.

feeding ecology and diet

Feeds on insects, their larvae, other invertebrates, and fishes, also algae or aquatic plants. May masticate food items repeatedly, and even reported to spit out and intake prey repeatedly during feeding.

reproductive biology

Males do not develop vascularized structures on their pelvic fins during breeding. Males usually guard larvae in nest sites that they dig out. Embryos hatch in one to two weeks, with conspicuous external gills, and will become obligate air breathers after about one month.

conservation status

Not listed by the IUCN.

significance to humans

Kept in public aquaria, and consumed locally but not intensely. Not widely kept by amateur aquarists and does not figure prominently in the ornamental fish trade.

Resources

Books

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

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

Britski, H. A., K. Z. S. de Silimon, and B. S. Lopes. Peixes do Pantanal, Manual de Identificação. Brasília: Embrapa, 1999.

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

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

Gosse, J. P. "Protopteridae." In Check-List of the Freshwater Fishes of Africa (CLOFFA), edited by J. Daget, J. P. Gosse, and D. F. E. Thys van den Audenaerde. Paris: ORSTOM; Tervuren: MRAC, 1984.

Graham, J. B. Air-Breathing Fishes. San Diego: Academic Press, 1997.

Greenwood, P. H. "The Natural History of African Lungfishes." In The Biology and Evolution of Lungfishes, edited by W. E. Bemis, W. W. Burggren, and N. E. Kemp. New York: A. R. Liss, 1987.

Janvier, P. Early Vertebrates. Oxford: Oxford University Press, 1996.

Lévêque, C. "Protopteridae." In Faune des poissons d'eaux douces et saumâtres d'Afrique de l'Ouest. Tome 1, edited by C. Lévêque, D. Paugy, and G. G. Teugels. Paris: ORSTOM, 1990.

Merrick, J. R., and G. E. Schmida. Australian Freshwater Fishes, Biology and Management. North Ryde, Australia: Macquarie University, 1984.

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

Planquette, P., P. Keith, and P. Y. LeBail. Atlas des Poissons d'Eau Douce de Guyane, Tome 1. Paris: Museum National d'Histoire Naturelle, 1996.

Skelton, P. Freshwater Fishes of Southern Africa, 2nd edition. Cape Town: Struik, 2001.

Periodicals

Atz, J. W. Narial. "Breathing in Fishes and the Evolution of Internal Nares." Quarterly Review of Biology 27, no. 4 (1952): 366–377.

Bemis, W. E. "Morphology and Growth of Lepidosirenid Lungfish Tooth Plates (Pisces: Dipnoi)." Journal of Morphology 179 (1984): 73–93.

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

Bertmar, G. "The Olfactory Organ and the Upper Lips in Dipnoi, a Comparative Embryological Study." Acta Zoologica 46 (1965): 1–40.

Carter, G. S., and L. C. Beadle. "Notes on the Habitat and Development of Lepidosiren paradoxa." Journal of the Linnaean Society, Zoology 37 (1930): 197–203.

Coates, C. W. "Slowly the Lungfish Gives Up Its Secrets." Bulletin of the New York Zoological Society 40 (1937): 25–34.

Cunningham, J. T., and D. M. Reid. "Pelvic Filaments of Lepidosiren." Nature 131 (1933): 913.

Dollo, L. "Sur la phylogénie des dipneustes." Bull. Soc. Belge Geol., Paleont. Hydrologie. 9, no. 2 (1896): 79–128.

Johnels, A. G., and G. S. O. Svensson. "On the Biology of Protopterus annectens (Owen)." Ark. Zool. Stockholm 7, no. 7(1954): 131–164.

Littrell, L. "African Lungfishes." Tropical Fish Hobbyist 19, no. 8 (1971): 40–57.

McMahon, B. R. "A Functional Analysis of the Aquatic and Aerial Respiratory Movements of an African Lungfish, Protopterus aethiopicus, with Reference to the Evolution of the Lung-ventilation Mechanism in Vertebrates." Journal of Experimental Biology 51, no. 2 (1969): 407–430.

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.

Poll, M. "Revision systématique et raciation géographique des Protopteridae de lÁfrique centrale." Ann. Mus. R. Afr. Cent., Zool., 8, no. 103 (1961): 1–50, pls. 1–6.

Rosen, D. E., P. L. Forey, B. G. Gardiner, and C. Patterson. "Lungfishes, Tetrapods, Paleontology, and Plesiomorphy." Bulletin of the American Museum of Natural History 167, no. 4(1981): 163–275.