View distribution map using BerkeleyMapper.

	Conservation Status (definitions)
IUCN (Red List) Status	Vulnerable (VU) See IUCN account.
CITES	No CITES Listing
Other International Status	Listed in Appendix II of the Convention of European Wildlife and Natural Habitats of 1979; Appendix II of the Bern Convention; Annexes II and IV of the EU Habitats Directive
National Status	On Slovenian Red List. Protected by Slovenia since 1949; Protected by Croatia; Protected by Italy
Regional Status	None

Description
Elongate and slender salamander with small, thin extremities. The front legs bear three toes, the rear legs two toes. The flattened tail is markedly shorter than the trunk. The head is elongated with a rounded snout. Eyes are poorly developed and covered by skin in the nominate subspecies. There are three pink external gills on each side of the head. The translucent skin also shows the contours of the internal organs on the ventral site of the body, making it easy to determine the sex of adults. Juveniles sometimes show a faded spotting. Dark pigmentation can be induced by exposure to light. This shows that these animals do not display albinism, as commonly thought, because they still possess the ability to produce melanin. The variant previously described as a subspecies (P. anguinus parkelj, the black olm, now shown to be phylogenetically nested well within P. anguinus; see Comments) has a permanent dark pigmentation of the skin, and probably functional eyes. It also has a shorter head than P. a. anguinus.

The average total length lies between 23-25 cm. They may grow up to 30 cm and rarely more than 30 cm. Black Proteus can grow up to 40 cm or more. Males are somewhat smaller than females. Other sexually dimorphic characteristics include the shape and size of the cloaca during breeding activity, with the males having a larger and more elongated swollen cloaca than the females.

Distribution and Habitat

Country distribution from AmphibiaWeb's database: Bosnia and Herzegovina, Croatia, Italy, Slovenia. Introduced: France.

View distribution map using BerkeleyMapper.

Proteus anguinus lives in the subterranean fresh water biotopes of the Dinaric Karst, from the Isonzo-Soca River in south-eastern Venezia Guilia, Italy through the southern half of Slovenia, southern Croatia, and parts of Bosnia and Herzegovina to the Trebisnjica River in eastern Herzegovina (Sket 1997). It has been introduced in the Parolini Grotto, Vicenza, northern Italy and Tular near Kranj in Slovenia. It may occur in Montenegro but this has not yet been confirmed (Kalezic and Dzukic 2001). The variant known as the black olm (formerly described as the subspecies Proteus anguinus parkelj; see Comments) is found in Bela Krajina, southeast Slovenia (Stet and Arntzen 1994; Griffiths 1996).

This species prefers underground water systems in karst formations, with calm, usually well-oxygenated water and a constant low water temperature between 8ºC (winter) and 11ºC (in one locality rarely up to 14ºC in summer) (Sket 1997; Honnegger 1981). It occurs in caves and may also be found in abandoned mines, from close to the surface to depths as much as 300 m underground, depending on how thick the karst formation is (Stuart et al. 2008). During periods of high rainfall and flooding it may be found in cave entrances (Stuart et al. 2008). The variant known as the black olm can be found in warmer surface waters (Stuart et al. 2008).

Life History, Abundance, Activity, and Special Behaviors
Proteus anguinus lives in subterranean waters, and is therefore a difficult subject for field observations. It does occur in caves that are accessible to humans, but as these contain hardly any adults, these accessible parts of caves must be seen as marginal parts of the biotope. Most observations on the life history of this salamander have been made in captivity. They have been bred in the Subterranean Laboratory of the CNRS, in the French Pyrenees (Station D'Ecologie Expérimental du CNRS, at Moulis, France) for more than 50 years, since 1955. The following life history account is made using data from observations on captive salamanders.

Although adults aggregate in suitable spots as in cracks and under rocks, males establish a territory when breeding, which is furiously protected from competing males. When a female enters such a territory, the courtship begins. The male fans with his tail in the direction of the female's head. The male touches the female's cloaca with his snout. The female then touches the male's cloaca with her snout and then follows the male who walks 5-10 cm forward after which the male deposits a spermatophore. The pair then moves forward again until the female can take up the spermatophore with her cloaca. Courtship can be repeated several times within a few hours. After leaving the male's territory, the female establishes an egg-laying territory. After 2-3 days the female starts to lay eggs and can continue doing so for up to 25 days, laying a total of up to 70 eggs under rocks. Eggs are guarded by the female. The diameter of the eggs directly after laying is 4-5 mm and can increase through water uptake to 8-9 mm. Unconfirmed historical observations of vivipary exist; it was long thought that female Proteus gave birth to only two well-developed young at lower temperatures and laid eggs at higher temperatures, but this has not been confirmed by rigorous observations. The eggs develop in 182 days at 8ºC, 140 days at 10ºC, 123 days at 11ºC, and in 86 days at 15ºC. Development of larvae is highly temperature-dependent. At 10ºC it takes another 14 years to reach sexual maturity. There is no clear metamorphosis; P. anguinus is a neotenic salamander, maintaining external gills, tail fin and other juvenile characteristics throughout its life.

Proteus anguinus is thought to be the longest-lived amphibian species. Using data spanning more than 50 years from a 400-animal captive breeding colony at the CNRS in Moulis, France, the predicted maximum lifespan is over a century, and the average adult olm lifespan is 68.5 years (Voituron et al. 2010). If the predicted maximum lifespan is accurate, it is more than double that of the next longest-lived species, the Japanese giant salamander (Andrias japonicus, at 55 years. Individual specimens have been kept under semi-natural conditions in concrete basins for up to 70 years (Prof. B. Bulog, personal communication). This species reaches sexual maturity at 15.6 years and lays 35 eggs every 12 years, on average (Voituron et al. 2010).

The diet consists of insect larvae, mostly Trichoptera, Ephemeroptera, Plecoptera and Diptera larvae, molluscs (Belgrandiella), and amphipods (Niphargus, Asellus, Synurella) (Bizjak-Mali 1995; Bizjak-Mali and Bulog 2004). In captivity worms are also readily eaten (Boehme et al. 1999).

Oxygen consumption
Compared to surface-dwelling neotenic urodelans, Proteus has lower oxygen consumption at 100ºC. It uses gills and integument for respiration and in hypoxic conditions also breathes with its lungs (Istenic and Sojar 1974). The lowered oxygen consumption is probably connected with a lower metabolic rate in Proteus that is well adapted to specific conditions in the underground aquatic habitats. Hypoxic conditions have been found periodically in the individual habitats of Proteus during periods of low water levels. Oxygen content measured in these summer periods was very low (1 mg O2/l) and individual specimens of Proteus have been observed frequently in such conditions (Prof. Bulog, personal observation).

Integument
The body is covered by the skin with a thin layer of surface mucous, secreted by the outermost cell layer, the stratum mucosum. Numerous larval characteristics of amphibian skin structure are retained in pigment-less and pigmented subspecies of Proteus: numerous Leidig cells, ciliary cells, sensory organs like neuromasts and ampullary organs. Skin of the pigmented subspecies is thicker and processes of melanophores under the basement lamella are more numerous. The integument contains very little "pigment" riboflavin, making it yellowish-white or pink in colour (Istenic and Ziegler 1974). Multicellular mucous glands are found in the dermis (Kos 1992).

Sensory adaptations to cave dwelling
As cave dwelling animals, they have been prompted to develop and improve non-visual sensory systems in order to orient in permanently dark habitats (Schlegel et al. 2006). The Olm's (Proteus) sensory system is adapted to life in the subterranean aquatic environment. Unable to use vision for orientation, the Olm compensates with other senses, which are better developed than in amphibians living on the surface. Because it retains larval proportions like a long, slender body and a large, flattened head, and is thus able to carry a larger number of sensory receptors (Schlegel et al. 2006). It can detect its prey in total darkness over some distance using chemical clues (Parzefall 1992) as well as mechanoreceptors and electroreceptors (Schegel and Bulog 1997).

Photoreceptors
The eyes are regressed, but retain sensitivity to light. They lie deep below the dermis of the skin, and are rarely visible except in some younger adults. Larvae have normal eyes, but development soon stops and they start regressing, finally atrophying after four months of development (Durand 1976). The pineal body also has regressed photoreceptive cells but retains visual pigments like the regressed eyes.

Visual pigments in the regressed eye and the pineal of the depigmented and pigmented subspecies were studied by immunocytochemistry (Kos et al. 2001). The presence of visual pigments indicates retained light sensitivity in both subspecies. In the retina of the black Proteus are principal rods, red-sensitive cones and a third photoreceptor type, which might represent a blue- or UV-sensitive cone. The majority of these outer segments of the regressed eye of unpigmented Proteus showed immunolabelling for the red-sensitive cone.

The pineal organ influences skin pigmentation, metamorphosis and gonadal development, and controls circadian rhythms through secretion of pineal hormones. The pineal structure is very similar in all Proteus individuals analyzed. In Proteus the pineal organ is reduced in size; it has degenerated photosensitive cells and can be found only by serial sectioning of the brain. The pineal organ probably possesses some control over the physiological processes also in Proteus, taking into account the presence of visual pigments (Kos et al. 2001). Behavioral experiments revealed that the skin itself is also sensitive to light, and immunocytochemical analysis also supported the existence of photosensitive pigment in Proteus' integument. Photosensitivity of the integument is due to the pigment melanopsin inside pigment cells called melanophores. (Kos et al. 2001).

Chemoreceptors
The Olm is capable of sensing very low concentrations of organic compounds in the water. They are better at sensing both the quantity and quality of prey by smell than related amphibians (Guillaume 2000). The nasal epithelium, located on the inner surface of the nasal cavity and in the Jacobson's organ, is thicker than in other amphibians (Dumas and Chris 1998). The taste buds are in the mucous epithelium of the mouth, most of them on the upper side of the tongue and on the entrance to the gill cavities. Those in the oral cavity are used for tasting food, while those near the gills probably sense the chemical composition of water (Istenic and Bulog 1979).

Mechanoreceptors
The sensory epithelia of the inner ear are very specifically differentiated and enable the Olm to receive sound waves in the water, as well as vibrations from the ground. The complex functional-morphological orientation of the sensory cells enables the animal to register the sound sources (Bulog 1989). Little is known about the hearing of Proteus, but occasionally observed reactions to sounds have indicated the possibility of a hearing capability under water (Prof. Bulog, personal observation). As this animal stays neotenic throughout its long life span, it is only occasionally exposed to normal adult hearing in air which is probably also possible for Proteus as in most salamanders. Hence, it would be of adaptive value in caves, with no vision available, to profit from underwater hearing by recognizing of particular sounds and eventual localization of prey or other sound sources, i.e., acoustical orientation in general. The ethological experiments indicate that the best hearing sensitivity of Proteus is from 10 Hz up to 15,000 Hz. The lateral line supplements inner ear sensitivity by registering low-frequency nearby water displacements (Bulog and Schlegel 2000; Schlegel et. al. 2006).

Electroreceptors
A new type of sensory organ has been analyzed by light and electron microscopy on the head of Proteus and described as ampullary organs (Istenic and Bulog 1984). Like some other lower vertebrates, the Olm has the ability to register weak electric fields (Schegel and Bulog 1997). Ampullary electroreceptors are responsible for this ability in Urodelans as well as Gymnophiona. Proteus senses electrical current fields and their polarity. It reacts to current density of 100 nA/cm2 and the lowest threshold of its ampullary organs is 3 mV/cm at best frequencies of 30 Hz. Prey capture is obviously performed by a combination of mechano-, chemo-, and, eventually, electro-perception (Schlegel et al. 2006).

Geomagnetic sense
Some behavioral experiments suggest that the Olm may use the earth's magnetic field to orient itself. Recently it was shown that Proteus aligns itself to natural and artificially modified magnetic fields. A round arena of 30 cm diameter was placed in the center of Helmholtz coils. This is a system of coils through which (by altering DC) a fairly homogeneous magnetic field around the arena can be created and controlled. The animal's movements were observed by an infrared video camera (Schlegel 1996).

Trends and Threats
The subterranean biotope is not closed. The Olm's survival is dependent on large aquatic cave systems and the conservation of sylvatic and pastoral land above, as well as clean water. Tourism, economic changes and industrial pollution are the main threats. Other threats to local populations may include water extraction and hydroelectric constrution. The decline of the known populations in Gorizia (Italy), and Postojna (Slovenia) is well established. The scientific needs can be provided by the Proteus breeding program carried out by the Subterranean Laboratory of the CNRS, France. This species must be more strictly protected by law (Gasc 1997).

The Olm is extremely vulnerable to changes in its environment due to its adaptation to the specific conditions in caves. Water resources in the karst are extremely sensitive to all kinds of pollution (Bulog et al. 2002) . The contamination of the karst underground waters is due to the large number of waste disposal sites leached by rainwater, as well as to the accidental overflow of various liquids. The reflection of such pollution in the karst underground waters depends on the type and quantity of pollutants, and on the rock structure through which the waters penetrate. Self-purification processes in the underground waters are not completely understood, but they are quite different from those in surface waters. Among the most serious chemical pollutants are chlorinated hydrocarbon pesticides, fertilizers, polychlorinated biphenyls (PCBs), which are (or were) used in a variety of industrial processes and in the manufacture of many kinds of materials; and metals such as mercury, lead, cadmium, and arsenic. All of these substances persist in the environment, being slowly, if at all, degraded by natural processes. In addition, all are toxic to life if they accumulate in any appreciable quantity.

Slovenian caves became famous for the animals they contained and which could not be found elsewhere. Due to its rarity the Olm is also popular among collectors, leading to possible overcollection. Honnegger (1981) also lists overcollecting, for scientific use or as pig-food by farmers, as a threat to this species.

The Olm is included in Appendices II and IV of the EU Habitats Directive (92/43/EEC). Appendix II seeks to preserve favorable conservation status in animal and plant species along with their habitats by protecting the species or defining special areas of conservation. These areas of conservation form the Natura 2000 network. Appendix IV further defines "animal and plant species of community interest in need of strict protection." Hunting or keeping a limited number of Olms is allowed only under strictly controlled circumstances, determined by local authorities.

The Olm was first protected in Slovenia in 1922 along with all cave fauna, but the protection was not effective and a substantial black market came into existence. In 1982 it was placed on a list of rare and endangered species in Slovenia. This list also had the effect of prohibiting trade of the species. After joining the European Union, Slovenia had to establish mechanisms for protection of the species included in the EU Habitats Directive. The Olm is included in the Slovenian Red List of endangered species. The Postojna cave and other caves inhabited by the Olm were also included in the Slovenian part of the Natura 2000 network.

On the IUCN Red List, the Olm is listed as Vulnerable because of its fragmented and limited distribution and ever-decreasing population.

In Slovenia much of the range lies within proposed national or international protected areas (Kocevski Regional Park; Kraski Regional Park; NATURA 2000 sites). In Italy it occurs within the Riserva Naturale Regionale dei Laghi di Doberdò e Pietrarossa (Stuart et al. 2008).

Relation to Humans
Proteus is considered a national treasure by the government of Slovenia, which honors the species by placing it on one of its coins. There is also the Proteus Postojna Speleobiological station, a museum which features Proteus along with other invertebrate cave fauna. This museum is visited by thousand of Slovenian school children and tourists every year.

Nearly 300 years after the first written mention of the unpigmented Proteus in Janez Vajkard Valvasor's “The Glory of the Duchy of Carniola (1689)”, a pigmented form (described as a subspecies, Proteus anguinus parkelj, the black olm) was discovered at Jelsevniscica in Jelsevnik near Crnomelj in Slovenia. This limited area is the unique locality of the black olm. A presentation on the unique black population has been prepared by the research group for functional-morphological studies of vertebrates, under the guidance of Prof. dr. Bulog. This presentation is located in the house of the family Zupancic in Jelsevnik and is prepared on ten color panels with texts and photo documentation. The presentation is intended for tourists and also for teaching and research purposes, for better recognition of the unique part of Slovenian natural heritage.

A popular scientific film dealing with our studies of biological peculiarities of endemic cave salamander supports this presentation and was recently created in collaboration with National TV of Slovenia (Bulog et al. 2003).

Possible reasons for amphibian decline

General habitat alteration and loss
Local pesticides, fertilizers, and pollutants
Long-distance pesticides, toxins, and pollutants
Intentional mortality (over-harvesting, pet trade or collecting)

Comments
Sket and Arntzen (1994) described black populations of Proteus as a separates subspecies, and defended this taxonomic decision based on the limited amount of morphological (morphometric) differentiation that Arntzen and Sket (1997) observed between the two subspecies. However, Goricki and Tronteltj (2006) found little differentiation between the two subspecies at the molecular level and questioned whether the designation of subspecies was appropriate. Subsequently Tronteltj et al. (2007) reported that both "subspecies" were nested within a southeastern Slovenian clade of P. anguinus and that the division was in fact simply intra-lineage diversity.

Proteus is the only cave-adapted vertebrate in Europe. Current genetic research under the direction of Dr. Boris Sket of the University of Ljubljana suggests that Proteus anguinus is actually a complex of several species, with phylogenetic analysis revealing six cryptic lineages (see Trontelj et al. 2007).

Functional-morphological and environmental studies of Proteus have been performed at the Department of Biology, Biotechnical Faculty (BF), University of Ljubljana, Slovenia for more than thirty years, with the most recent twenty years under the guidance of Prof. dr. Boris Bulog.

References
 

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Bizjak-Mali, L. and Bulog, B. (2004). ''Histology and ultrastructure of the gut epithelium of the neotenic cave salamander, Proteus anguinus (Amphibia, Caudata).'' Journal of Mophology, 259, 82-89.  

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