Olms and Mudpuppies (Proteidae)

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Olms and mudpuppies

(Proteidae)

Class Amphibia

Order Caudata

Suborder Salamandroidea

Family Proteidae

Thumbnail description
Permanently aquatic, medium-size to large salamanders with a somewhat elongated "squared-off" snout, small limbs, reduced numbers of toes, and large, bushy, red gills; most olms are pale (rarely dark) and nearly eyeless, whereas mudpuppies are dark with large spots and small eyes

Size
12–16 in (30.5–40.6 cm)

Number of genera, species
2 genera; 6 species

Habitat
Freshwater

Conservation status
Vulnerable: 1 species

Distribution
Southeastern Europe and eastern North America

Evolution and systematics

Fossil proteids, including species of two extinct genera, are known from the Miocene and Pleistocene of Europe, the Upper Paleocene and Pleistocene of North America, and the Miocene of Asia. Fossils of Necturus date to the Paleocene of Canada and the Pleistocene of Florida. Fossils of Proteus date from the Pleistocene of Germany.

As of the year 2002, one species of Proteus and five species of Necturus were recognized. These are enigmatic salamanders that have long been shrouded in mystery in both popular and scientific circles. The European blind cave salamander or olm (Proteus anguinus) has been known for centuries as the "human fish" (because of its pale skin color), haunting the subterranean waters of the Dinaric karst in Slovenia and adjacent areas. Olms were first mentioned in the scientific literature more than 300 years ago. North American mudpuppies (species of the genus Necturus) likewise have been known for centuries as "waterdogs"; They have been familiar to scientists since at least 1799 and are one of the most extensively used vertebrates for courses in comparative anatomy and physiology. And yet the phylogenetic relationships of proteids to other salamanders and systematics within the family remain problematic.

The relationship between Necturus and Proteus has been questioned and has long been the subject of controversy. Part of the problem with this group is that it represents ancient lineages of permanently aquatic, neotenic salamanders that retain their larval morphologic characters into adulthood. Neoteny is a well-known phenomenon in which adults maintain larval morphologic features and breed in that state. Some scientists believe that the morphologic similarities between Proteus and Necturus are the result of convergent (or parallel) evolution toward neoteny in permanent aquatic habitats.

Studies of similarities in DNA sequences, proteins, and chromosomes in proteid salamanders are ongoing and have not yet produced conclusive results. In addition to general morphologic similarities, Necturus and Proteus share the same diploid chromosome number (38), which is not found in any other salamanders. All species of Necturus have distinctive X and Y sex chromosomes that are unlike those of other salamanders, but it is not known whether olms have this feature. Working out the precise phylogenetic relationships of these strange salamanders depends on additional research.

Taxonomy and evolutionary relationships within both genera are in a state of flux. In 1986 a population of dark-colored Proteus was discovered in Slovenia. Salamanders from this population have enough distinct features that some scientists consider them to be a subspecies (Proteus anguinus parkelj), but others suspect that they may constitute a different species altogether. Within the genus Necturus, comparative biochemical (protein) and karyological (chromosome) analyses indicate that individual species fall into three main lineages: N. lewisi, N. punctatus, and a group of three closely related species consisting of N. alabamensis, N. beyeri, and N. maculosus. The relationships among these three species and especially the taxonomic status of N. alabamensis are uncertain. It is clear that both genera need to be analyzed further. No subfamilies are recognized.

Physical characteristics

All proteid salamanders are permanently aquatic and have larval morphologic features, including three pairs of large, bushy, red gills; a relatively short, laterally compressed tail with a tail fin; and reduced eyes, even as adults. These are moderately large to large salamanders that can reach more than 16 in (40.6 cm) in total length (from the tip of the snout to the tip of the tail). Proteus anguinus is the most strikinglooking species. It is long and skinny with pale, pinkish white skin, and it has a flat, narrow head with tiny degenerate eyes and small limbs with only three digits on the forelimbs and two digits on the hind limbs. These features are thought to reflect adaptation to aquatic, subterranean habitats. Thus, Proteus often is described as "troglomorphic." Reportedly, Proteus has some pigment and turns darker when exposed to light. Dark-colored individuals of Proteus, which are thought to be a separate subspecies (P. a. parkelj), are less strongly troglomorphic and have larger eyes. Proteus achieves a total length of approximately 12 in (30.5 cm).

Species of Necturus are somewhat larger than Proteus, reaching nearly 19 in (48.3 cm) in total length. They are fully pigmented. They are also more robust, with a wider head and a thicker body and limbs. Most Necturus species are dark rusty brown or grayish brown; they have large, irregular spots of black or blue-black on the dorsum (back) of the animal and a paler venter (belly), with a dark stripe passing through the eye. Necturus is colored cryptically against the dark bottom of lakes, rivers, and streams, but the exact color pattern depends on the species. The morphologic features of Necturus are at least somewhat reminiscent of Proteus, including small, larval eyes; a short tail; reduced limbs with four digits on both pairs; and a peculiar-looking "squared off" snout, reflecting the absence of maxillary (upper jaw) bones.

Distribution

The distribution of proteids is disjunct: Necturus is found only in the New World, whereas Proteus is exclusively Old World. All species of Necturus, with the exception of N. maculosus, are distributed along the coastal plain of the southeastern United States, from southeastern Virginia to eastern Texas. Necturus maculosus is by far the most widely distributed species, with a fanlike range extending from an apex in Louisiana and broadening northward to southeastern Manitoba in the west and southestern Quebec, Canada, in the east, essentially encompassing the entire Mississippi River drainage system. The combined ranges of these species result in a more or less continuous distribution of Necturus over most of eastern North America, interrupted in the east by the Appalachian Mountains, which form a wedge separating the two coastal species, N. lewisi and N. punctatus, from inland populations of N. maculosus. The two most enigmatic species, N. alabamensis and N. beyeri, are distributed near the southern limits of the ranges of N. maculosus to the west and N. punctatus to the east.

Proteus anguinus is known from approximately 250 localities, from the limestone cave systems along the Adriatic seaboard from western Slovenia and northeastern Italy in the north to Montenegro in the south. The majority of localities are in western Slovenia. The putative subspecies, Proteus a. parkelj, is from the Bela Krajina region of western Slovenia.

Habitat

Proteus inhabits underground streams and lakes in limestone caves in eternal darkness, where the water is cold year-round (usually about 46.5°F, or 8°C). These salamanders are thought to congregate in their main habitat in deep crevices and fissures that are largely inaccessible to exploration by humans. Most sightings and captures of olms appear to have been in marginal habitats, where the salamanders either were flushed out by heavy rains or were hunting for food. Mudpuppies inhabit a wide variety of permanently aquatic habitats, including muddy canals; ditches; large, rocky, fast-flowing streams; reservoirs; and large, cool lakes. They are most active at night and may be found during the day by lifting or disturbing rocks and other cover. Necturus may be found at all seasons of the year and are even active beneath the ice in mid-winter.

Behavior

Proteid salamanders have been neglected in terms of detailed behavioral studies. Mudpuppies often are seen crawling slowly over the bottom of streams or lakes, but they can swim rapidly when frightened. In captivity, mudpuppies are secretive and prefer to hide beneath any available objects, including each other. They appear to be repelled by light. In poorly aerated water, mudpuppies constantly fan their gills, which may become large, bushy, and bright red. Under such conditions, the salamanders often rise to the surface to take gulps of air. In well-oxygenated water the gills tend to be held motionless against the sides of the neck and eventually shrink in size. There is some evidence that mudpuppies are capable of homing behavior. Even less information is available for olms. Olms are gregarious, at least when they are not breeding, and tend to congregate in deep fissures. They apparently use chemosensory cues to mark and find their "home shelters."

Feeding ecology and diet

Mudpuppies are generalist predators; their natural food includes fish, fish eggs, crayfish, worms, small mollusks, and aquatic insects, in short almost anything that moves and will fit into their mouths. They are especially fond of sculpins and sometimes can be found gorged with these fish. Most information about the ecology and other aspects of the biology of Proteus is based on observations of animals raised in captivity. Little is known about the feeding ecology of these salamanders in the wild, except that they seem to feed on amphipods, insect larvae, and other small invertebrates. Apparently, Proteus uses chemosensory cues to locate prey in total darkness.

Reproductive biology

Relatively limited information is available on the reproductive biology of proteid salamanders. The animals tend to

be gregarious, at least when they are not breeding. The breeding season for Necturus is in the fall or winter, depending on the species and location. Sexually active males have swollen, "inflamed" cloacas (urogenital openings), with a pair of enlarged papillae (finger-like appendages) that project posteriorly. Breeding in Proteus appears to be aseasonal, reflecting the stability of their subterranean habitat. Olms seem to be much more territorial during breeding than mudpuppies. All species for which information is known show some kind of courtship ritual in which the males and females stimulate each others' cloacas. Courtship culminates in the male depositing a packet of sperm (spermatophore), which the female picks up with her cloaca. The female may store sperm in special structures inside her cloaca called spermathecae for six months or more. The eggs usually are attached beneath some object, such as a rock or a log, and are guarded by the female. The eggs are large (0.2 in, or 5–6 mm), full of yolk, and unpigmented; they may number 100 or more per clutch.

The incubation period lasts two to six months, depending on the species and the temperature. Proteus reportedly is capable of some degree of viviparity (live-bearing), giving birth to a pair of well-developed young. The larvae, which in mudpuppies may have strikingly different pigmentation from the adults, develop gradually into the adult form, with no distinct metamorphosis. The age of sexual maturation is not known for mudpuppies, but for olms it is reported to be seven years. Little is known about longevity in proteid salamanders; reports range from nine years to nearly 60 years, depending on the species.

Conservation status

Proteus is listed by the IUCN as Vulnerable, mostly because of the restricted range and apparently small sizes of most known populations. Olms have been protected in Slovenia since 1949. The main threats to olms are economic development, industrial pollution, and overcollecting. Although it is almost impossible to assess populations of olms with certainty, given the inaccessibility of most of the natural habitat, population declines have been reported in Italy and Slovenia. None of the species of Necturus are listed by the IUCN as of 2002, and most populations seem to be doing well. Mudpuppies, however, are vulnerable to factors that are known to affect amphibians adversely, including chemical pollution, habitat alteration, and overcollecting.

Significance to humans

Proteids have long been used for scientific studies, and Necturus is the most commonly used amphibian in comparative anatomy courses. Proteids are also important in the pet trade and have been used to promote ecotourism, particularly in Slovenia. Because of their thin skin and dependence on clean, well-oxygenated water, proteids may be good indicators of water quality.

Species accounts

List of Species

Olm
Neuse River waterdog
Mudpuppy
Dwarf waterdog

Olm

Proteus anguinus

taxonomy

Proteus anguinus Laurenti, 1768, Magdalene Cave, near Adelsberg Cave, Slovenia. Two subspecies are tentatively recognized.

other common names

English: Blind cave salamander; German: Grottenolm.

physical characteristics

The body is slender, elongated, and pinkish white, with a long, angular, "squared-off" snout; degenerate eyes; a short, laterally compressed tail; and three pink external gills on each side of the head. The limbs are thin, with a reduced number of digits: three digits on the forelimb and two digits on the hind limb. The average size of adults is approximately 10 in (25.4 cm).

distribution

The species occurs in Italy, Slovenia, Croatia, Bosnia, and Herzegovina, with a captive population in France.

habitat

Olms inhabit subterranean lakes and rivers in limestone caves of the Dinaric Alps, from Slovenia and Italy in the north to Montenegro in the south.

behavior

These salamanders are gregarious except during the breeding season, when males are territorial. Generally, they are secretive and rarely seen, except in marginal habitats either when feeding or because of flooding.

feeding ecology and diet

Olms feed at night, using chemosensory cues to find small arthropods and other invertebrates.

reproductive biology

Breeding is aseasonal. Fertilization is internal via spermatophores after courtship; eggs are large and yellowish and are laid under rocks and other cover and guarded by the female. The incubation period is up to six months; larvae develop directly into adults without metamorphosis.

conservation status

The species is listed by the IUCN as Vulnerable and in Appendix II of the Convention of European Wildlife and Natural Habitats of 1979. It is not considered critically endangered or endangered but faces a high risk of extinction in the wild in the not too distant future.

significance to humans

Olms are an ecotourist attraction; they are popular in the pet trade and are used in scientific research.

Neuse River waterdog

Necturus lewisi

taxonomy

Necturus maculosus lewisi Brimley, 1924, Neuse River, near Raleigh, North Carolina, United States.

other common names

English: Lewis' mudpuppy.

physical characteristics

This is a medium-size mudpuppy, 6–11 in (15.2–28 cm) in total length. It has a rusty, yellowish brown dorsum with large, dark spots scattered over the back and sides. The venter is paler, with fewer and smaller blotches.

distribution

The range is restricted to the Neuse and Tar river systems in North Carolina, United States.

habitat

This salamander prefers relatively wide, fast-flowing streams with a high oxygen content and a hard substrate.

behavior

The Neuse River waterdog is active at night and retreats into burrows in the stream bank or under large rocks during the day. Activity decreases at high stream temperatures. The skin produces noxious secretions that may defend against predation.

feeding ecology and diet

The diet consists of small invertebrates and vertebrates, including crustacea, mollusks, annelid worms, aquatic insect larvae, small fish, and other amphibians. Like other mudpuppies, Neuse River waterdogs are sit-and-wait predators that use "gape and suck" feeding mechanics.

reproductive biology

The breeding season is from December through March and possibly also in the spring. Eggs are deposited on the under-surface of large rocks in fast-flowing water. Hatching occurs in July.

conservation status

Not threatened.

significance to humans

Waterdogs are collected in great numbers by biological supply houses, probably with little regard to exact species or locality; they also are seen in the pet trade.

Mudpuppy

Necturus maculosus

taxonomy

Sirena maculosa Rafinesque, 1818, Ohio River, United States (state not recorded). Two subspecies are recognized.

other common names

English: Common mudpuppy, waterdog; French: Necture tacheté; German: Gefleckter Furchenmolch.

physical characteristics

This is the largest member of the genus, reaching 8–19 in (20.3–48.3 cm) in total length. Coloration varies from deep rusty brown to gray or even black, with scattered black or bluish black spots and blotches. The spots sometimes may form two fairly regular rows along the back. As with other mudpuppies and waterdogs, a dark bar extends through the eye to the gills. The venter is paler, with or without dark spots. The margins of the tail commonly are tinged with reddish orange.

distribution

This species has by far the widest distribution in the genus, encompassing essentially the entire Mississippi River drainage system, from southern Manitoba and Quebec, Canada, in the north to Georgia, Alabama, Mississippi, and Louisiana, United States, in the south.

habitat

These salamanders inhabit a wide variety of permanently aquatic habitats, including rivers, streams, canals, and lakes.

behavior

Mudpuppies are active all year round and have been seen moving around beneath the ice in mid-winter. Adults are mostly active at night, when they forage, and they hide under rocks and other objects or in burrows during the day.

feeding ecology and diet

Mudpuppies feed on a variety of small aquatic invertebrates and vertebrates, including crayfish and other crustaceans, mollusks, worms, insect larvae, fish, and amphibians.

reproductive biology

As with all mudpuppies and waterdogs, the sex of adults can be determined by examining the morphologic characteristics of the vent, especially during the breeding season, when the male's vent is swollen. The male's vent also is equipped with two nipple-like papillae that project posteriorly. The vent of the female is a simple slit. The mating season is in the autumn or winter, possibly extending into spring, depending on the locality. In May or June the eggs are attached to the undersurfaces of large rocks, where they are attended by the female, who apparently defends them against predators. Hatching takes place in one or two months, depending on the temperature of the water. The newly hatched larvae are approximately 1 in (25.4 mm) in length and have two lateral yellow stripes on a dark ground color.

conservation status

Not threatened.

significance to humans

Mudpuppies are collected in great numbers by biological supply companies for use in classrooms and laboratories around the world; they are seen often in the pet trade as well.

Dwarf waterdog

Necturus punctatus

taxonomy

Menobranchus punctatus Gibbes, 1850, southern Santee River, South Carolina, United States.

other common names

English: Southern waterdog, Carolina waterdog.

physical characteristics

This is the smallest species of Necturus, reaching only about 7 or 8 in (17.8–20.3 cm) in total length. The coloration is slategray to dark brown or black, with no spots or only a few small, pale spots. The venter is pale and has no spots. Unlike other species of Necturus, the larvae are not striped.

distribution

This species occurs along the coastal plain from southern Virginia to central Georgia in the United States. The distribution overlaps that of N. lewisi.

habitat

The dwarf waterdog prefers small and medium-size streams, especially in deeper, slower sections with leaf beds and other debris.

behavior

Little is known about the life history and behavior of this species. Adults have been observed to congregate in leaf beds during winter.

feeding ecology and diet

Dwarf waterdogs feed on a variety of small invertebrates and vertebrates, including crayfish, worms, arthropods, mollusks, and other amphibians. They may compete for food with N. lewisi where the two inhabit the same streams.

reproductive biology

Little is known about the reproductive biology of this species, but it is thought that mating occurs in winter, followed by egg laying sometime between March and May.

conservation status

Not threatened.

significance to humans

Dwarf waterdogs are probably not collected in large numbers for educational or scientific purposes, but they may enter the pet trade.

Resources

Books

Arnold, E. N., and J. A. Burton. Field Guide to the Reptiles and Amphibians of Britain and Europe. 2nd ed. London: HarperCollins Publishers, 1998.

Bishop, S. C. Handbook of Salamanders. Reprint. Ithaca, NY: Cornell University Press, 1994.

Conant, Roger, and Joseph T. Collins. A Field Guide to Reptiles and Amphibians, Eastern and Central North America. New York: Houghton Mifflin, 1991.

Duellman, William E., and Linda Trueb. Biology of Amphibians. New York: McGraw Hill Book Company, 1986.

Noble, G. K. The Biology of the Amphibia. New York: Dover Publications, 1954.

Petranka, James W. Salamanders of the United States and Canada. Washington, D.C.: Smithsonian Institution Press, 1998.

Periodicals

Arntzen, J. W., and Boris Sket. "Morphometric Analysis of Black and White European Cave Salamanders, Proteus anguinus." Journal of Zoology (London) 241 (1997): 699–707.

Bishop, Sherman C. "The Salamanders of New York." New York State Museum Bulletin 324 (1941): 1–365.

Guttman, S. I., L. A. Weight, P. A. Moler, R. E. Ashton Jr., B. W. Mansell, and J. Peavy. "An Electrophoretic Analysis of Necturus from the Southeastern United States." Journal of Herpetology 24 (1990): 163–175.

Hecht, M. K. "A Case of Parallel Evolution in Salamanders." Proceedings of the Zoological Society Calcutta, Mookerjee Memorial Volume (1957): 283–292.

—— "A Synopsis of the Mud Puppies of Eastern North America." Proceedings of the Staten Island Institute of Arts and Sciences 21, no. 1 (1958): 1–38.

Sessions, S. K., and J. E. Wiley. "Chromosomal Evolution in Salamanders of the Genus Necturus." Brimleyana 10 (1985): 37–52.

Sket, Boris. "Distribution of Proteus (Amphibia: Urodela: Proteidae) and Its Possible Explanation." Journal of Biogeography 24 (1997): 263–280.