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.
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.
Proteus anguinus, also known as olms, are native to countries along the Adriatic Sea. They can be found as far north as Slovenia and northern Italy, continuing southward through Croatia, and Bosnia and Herzegovina. It is uncertain whether the range continues south to Montenegro and Serbia. Isolated populations of Proteus anguinus have been introduced in the French Pyrenees Mountains and northeastern Italy.
Biogeographic Regions: palearctic (Introduced , Native )
Distribution and Habitat
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).
Proteus anguinus has a slender, elongate body averaging 23 to 25 cm in length from head to tail. The torso is cylindrical and has about two-dozen costal grooves along each side. The tail is laterally compressed, with small fins running along the top and bottom. The head is elongate with a broad snout that is blunted at the end. Its eyes are very small and do not even breach the skin. The skin is usually creamy white, but may have a pinkish hue. When exposed to light, the skin turns dark violet to black. Darkening of the skin is reversed when it is returned to the darkness. On the ventral side of the body the skin is translucent and reveals the contours of internal organs. Directly behind the head on each side are three large, feathery, bright pink gills. This species exhibits little sexual dimorphism in appearance, but females are larger than males.
Juveniles may be distinguished from adults by the faint yellow or red blotches on their skin, and their better developed eyes. Black olms, a variant of this species previously known as Proteus anguinus parkelj, have permanently dark skin and a shorter head.
Range length: 20 to 30 cm.
Average length: 23 to 25 cm.
Other Physical Features: ectothermic ; heterothermic ; bilateral symmetry
Sexual Dimorphism: female larger
Proteus anguinus is found in the subterranean, freshwater lakes and streams of limestone caves in the Dinaric Alps. The water in these caves is slightly acidic, contains high concentrations of oxygen, and ranges in temperature from 5° to 15° C. Adapted to an aphotic environment, olms usually reside deep within cave systems. They may be found in open streams near the surface during times of high rainfall and flooding. They are generally found over 300 meters below surface.
Range depth: 300 (low) m.
Habitat Regions: temperate ; freshwater
Terrestrial Biomes: mountains
Aquatic Biomes: lakes and ponds; rivers and streams
Other Habitat Features: caves
Habitat and Ecology
Olms are insectivores, but will eat most anything that they can capture and fit into their mouths. They prey on arthropods and small invertebrates such as Oniscus asellus as well as organsims of the genera Belgrandiella and Niphargus. They also feed on a wide variety of insect larvae belonging to the orders Trichoptera, Ephemeroptera, Plecoptera, and Diptera. To locate and capture their prey, olms use a combination of chemoreceptors, electroreceptors, and mechanoreceptors. In captivity, olms have been recorded eating worms, tiny fish, and even small pieces of raw meat.
Animal Foods: fish; eggs; insects; terrestrial non-insect arthropods; mollusks; terrestrial worms
Primary Diet: carnivore (Insectivore )
As a predator of multiple different organisms, Proteus anguinus has a direct impact on the sizes of insect, arthropod, and other invertebrate populations within local subterranean freshwaters.
Proteus anguinus has no known predators.
Life History and Behavior
Because it inhabits permanently dark environments, Proteus anguinus has developed non-visual sensory systems to better suit an aphotic lifestyle. Its eyes still retain some light sensitivity, but they are greatly reduced. Highly sensitive chemoreceptors allow olms to detect extremely low concentrations of organic material in the water. Olms use this ability to distinguish species of prey and their abundance. Functional ears, which may register sounds from the surrounding water as well as the ground, are complemented by olms' lateral line organ, which detects low-frequency water displacement in the nearby surrounding environment. All members of the genus Proteus contain an ampullary electroreceptor which is used to detect electric fields. The main function of their ampullary electroreceptor is not known, but it is suspected top be used for locating prey. Behavioral studies suggest that Proteus anguinus is also able to detect and orient itself to magnetic fields.
Little is known about the forms of intraspecies communication of olms. Potential mates have been observed using tactile stimulation – each mate touching its snout to the others cloaca. Before this, the male waves his tail in front of the female’s head. Because visual perception is minimal in the species, the purpose of such courtship behaviors is believed to be linked to pheromones and chemoreception. To establish and defend their territories, males are not known to use chemical clues, but rely on physical competition. The specialized sensory adaptations observed in olms have led scientists to use the species as a model for studying the effects of permanent darkness on the evolution of such traits.
Communication Channels: tactile ; chemical
Other Communication Modes: pheromones
Perception Channels: tactile ; acoustic ; vibrations ; chemical ; electric ; magnetic
Unlike those of most amphibians, olm larvae do not go through a distinct period of metamorphosis. Instead, the hatchling juveniles have developed directly into adults, retaining some of their larval characters such as gills and tail fins. Environmental temperature plays an important role in the development of eggs as well as juveniles. Within the range of 8° to 15°C, development time is relatively shorter (86 days) in warm temperatures and longer (182 days) in cold temperatures.
Development - Life Cycle: neotenic/paedomorphic; metamorphosis
Because olms live in such secluded environments, little is known about their lifespan or longevity in the wild. In fact, much of the information available concerning Proteus anguinus has been gathered from observing populations in captivity. The average age of an individual in captivity was 68.5 years, and the expected life expectancy is over 100 years.
Status: wild: 100+ (high) years.
Status: wild: 68.5 years.
Status: captivity: 68.5 years.
Lifespan, longevity, and ageing
Proteus anguinus is an aseasonal breeder. During times of breeding, males become territorial and physically defend their territories. The qualities of an ideal territory are unknown. Once a mating territory is established by the male, he waits for females. Eventually a female will approach a male within his territory and courtship begins. It is unclear whether males and/or females release pheromones to communicate with each other. A male may potentially mate with multiple females, but a female mates with just one male.
The courtship process is distinctive. A female approaches a male, and he fans his tail towards her head. The male then touches the female's cloaca with his snout, and she reciprocates. The male walks in front of the female and deposits a spermatophore, which the female immediately picks up with her cloaca and stores in a special structure called a spermathecae.
Mating System: polygynous
Proteus anguinus breeds every 12 years, on average. The female begins laying her fertilized eggs 2 to 3 days after courtship, and may continue to lay eggs for up to 25 days. Before laying her eggs, the female establishes an egg-laying territory away from the male's territory. Clutch size averages 35 eggs. Eggs incubate for two to six months, hatching into juveniles that develop directly into adults. Olms become sexually mature at 14 to 15 years old.
Breeding interval: Proteus anguinus breeds every 12 years, on average.
Breeding season: The breeding season for Proteus anguinus is unknown.
Range number of offspring: 70 (high) .
Average number of offspring: 35.
Range time to hatching: 2 to 6 months.
Range age at sexual or reproductive maturity (female): 14 to 15 years.
Range age at sexual or reproductive maturity (male): 14 to 15 years.
Key Reproductive Features: iteroparous ; gonochoric/gonochoristic/dioecious (sexes separate); sexual ; fertilization (Internal ); oviparous
A female olm guards her eggs while they incubate (2 to 6 months). She does not provide food or protection once the eggs are hatched. Males exhibit no parental investment beyond the initial sperm.
Parental Investment: female parental care ; pre-fertilization (Provisioning, Protecting: Female); pre-hatching/birth (Protecting: Female)
Molecular Biology and Genetics
Barcode data: Proteus anguinus
Below is the sequence of the barcode region Cytochrome oxidase subunit 1 (COI or COX1) from a member of the species.
See the BOLD taxonomy browser for more complete information about this specimen.
Other sequences that do not yet meet barcode criteria may also be available.
-- end --
Download FASTA File
Statistics of barcoding coverage: Proteus anguinus
Public Records: 1
Specimens with Barcodes: 1
Species With Barcodes: 1
Proteus anguinus is currently listed as Vulnerable on the IUCN Red List. The main cause for reduction in olm populations is habitat destruction. This may include water pollution and changes to the land above its underground habitat, such as economic development and tourism. There is also illegal capture of olms for the pet industry. Currently, Proteus anguinus mostly resides in national parks and land protected by the governments of Italy, Croatia, and Slovenia. Variant black olms are limited to a small area in Slovenia and are in need of protection.
CITES: no special status
IUCN Red List of Threatened Species: vulnerable
IUCN Red List Assessment
Red List Category
Red List Criteria
- 1994Vulnerable(Groombridge 1994)
- 1990Vulnerable(IUCN 1990)
- 1988Vulnerable(IUCN Conservation Monitoring Centre 1988)
- 1986Vulnerable(IUCN Conservation Monitoring Centre 1986)
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).
Compared to surface-dwelling neotenic urodelans, Proteus has lower oxygen consumption at 10 ºC. 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).
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).
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).
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).
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).
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).
Life History, Abundance, Activity, and Special Behaviors
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).
Relevance to Humans and Ecosystems
There are no known adverse effects of Proteus anguinus on humans.
As a very distinguishable and unique creature, Proteus anguinus serves as a popular ecotourist attraction in the Dinaric Alps. It is a national treasure of Slovenia, and is so recognized by being pictured on one of the countries coins. Olms are sometimes collected for the pet trade, but doing so is illegal within the countries that protect the species. Proteus anguinus is also used in scientific research as a model for studying the evolution of highly specialized sensory adaptations in aphotic environments.
Positive Impacts: pet trade ; ecotourism ; research and education
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).
The olm, or proteus (Proteus anguinus), a salamander, is the only cave-dwelling chordate species found in Europe. In contrast to most amphibians, it is entirely aquatic; it eats, sleeps, and breeds underwater. Living in caves found in Dinaric Alps, it is endemic to the waters that flow underground through extensive limestone of karst of Central and Southeastern Europe, specifically southern Slovenia, the Soča river basin near Trieste, Italy, southwestern Croatia, and Herzegovina.
It is also occasionally called the "human fish" by locals because of its skin color, similar to that of white people (translated literally from Slovene: človeška ribica and Croatian: čovječja ribica), as well as "cave salamander" or "white salamander." In Slovenia, it is also known by the name močeril, which translates as "the one that burrows into wetness." It was first mentioned in 1689 by a local naturalist Valvasor in his Glory of the Duchy of Carniola reporting that after heavy rains the olms were washed up from the underground waters and made local people believe they saw a cave dragons' offspring.
This animal is most notable for its adaptations to a life of complete darkness in its underground habitat. The olm's eyes are undeveloped, leaving it blind, while its other senses, particularly those of smell and hearing, are acutely developed. It also lacks any pigmentation in its skin. It has three toes on its forelimbs, but two toes on its hind feet. It also exhibits neoteny, retaining larval characteristics like external gills into adulthood, like the American amphibians, the axolotl and the mudpuppy. The olm is the only species in the Proteus genus, the only European species of the Proteidae family.
The olm's body is snakelike, 20–30 cm (8–12 in) long, with some specimens reaching up to 40 centimetres (16 in). The trunk is cylindrical, uniformly thick, and segmented with regularly spaced furrows at the myomere borders. The tail is relatively short, laterally flattened, and surrounded by a thin fin. The limbs are small and thin, with a reduced number of digits compared to other amphibians: the front legs have three digits instead of the normal four, and the rear have two digits instead of five. Its body is covered by a thin layer of skin, which contains very little of the pigment riboflavin, making it yellowish-white or pink in color. The internal organs can be seen shining through on the abdominal part of the body. The resemblance in color to that of white humans is the reason why the Proteus is called human fish in some languages. However, the olm's skin retains the ability to produce melanin. When exposed to light, it will gradually turn dark, and in some cases the larvae are also colored. Its pear-shaped head ends with a short, dorsoventrally flattened snout. The mouth opening is small, with tiny teeth forming a sieve to keep larger particles inside the mouth. The nostrils are so small as to be imperceptible, but are placed somewhat laterally near the end of the snout. The regressed eyes are covered by a layer of skin. The olm breathes with external gills that form two branched tufts at the back of the head. They are red in color because the oxygen-rich blood shows through the non-pigmented skin. The olm also has rudimentary lungs, but their role in respiration is only accessory. The sexes are very similar in appearance, with males having a somewhat thicker cloaca than females.
Cave-dwelling animals have been prompted, among other adaptations, to develop and improve non-visual sensory systems in order to orient in and adapt to permanently dark habitats. The olm's sensory system is also 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. 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.
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. The pineal body also has photoreceptive cells which, though regressed, retain visual pigment like the photoreceptive cells of the regressed eye. The pineal gland in Proteus probably possesses some control over the physiological processes. Behavioral experiments revealed that the skin itself is also sensitive to light. Photosensitivity of the integument is due to the pigment melanopsin inside specialized cells called melanophores. Preliminary immunocytochemical analysis support the existence of photosensitive pigment also in the animal's integument.
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. The nasal epithelium, located on the inner surface of the nasal cavity and in the Jacobson's organ, is thicker than in other amphibians. 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, where those near the gills probably sense chemicals in the surrounding water.
Mechano- and electroreceptors
The sensory epithelia of the inner ear are very specifically differentiated, enabling 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. 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 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 between 10 Hz and up to 15,000 Hz. The lateral line supplements inner ear sensitivity by registering low-frequency nearby water displacements.
Like some other lower vertebrates, the olm has the ability to register weak electric fields. Some behavioral experiments suggest that the olm may be able to use Earth's magnetic field to orient itself. Recently, Proteus anguinus has been found to align itself with natural and artificially modified magnetic fields.
Ecology and life history
The olm's embryonic development takes 140 days, after which it takes another 14 years to reach sexual maturity. The larvae gain adult appearance after nearly four months, with the duration of development strongly correlating with water temperature. Unconfirmed historical observations of vivipary exist, but it has been shown that the females possess a gland that produces the egg casing, similar to those of fish and egg-laying amphibians. It was long thought that female olm gave birth to live young at lower temperatures and laid eggs at higher, but rigorous observations have not confirmed that. The olm appears to be oviparous.
The female lays up to 70 eggs, each about 12 millimetres (0.5 in) in diameter, and places them between rocks, where they remain under her protection. The tadpoles are 2 centimetres (0.8 in) long when they hatch and live on yolk stored in the cells of the digestive tract for a month.
Development of the olm and other troglobite amphibians is characterized by heterochrony – the animal does not undergo metamorphosis and instead retains larval features. The form of heterochrony in the olm is neoteny – delayed somatic maturity with precocious reproductive maturity, i.e. reproductive maturity is reached while retaining the larval external morphology. In other amphibians, the metamorphosis is regulated by the hormone thyroxine, excreted by the thyroid gland. The thyroid is normally developed and functioning in the olm, so the lack of metamorphosis is due to the unresponsiveness of key tissues to thyroxine.
The olm swims by eel-like twisting of its body, assisted only slightly by its poorly developed legs. It is a predatory animal, feeding on small crabs, snails and occasionally insects. It does not chew its food, instead swallowing it whole. The olm is resistant to long-term starvation, an adaptation to its underground habitat. It can consume large amounts of food at once, and store nutrients as large deposits of lipids and glycogen in the liver. When food is scarce, it reduces its activity and metabolic rate, and can also reabsorb its own tissues in severe cases. Controlled experiments have shown that an olm can survive up to 10 years without food.
Olms are gregarious, and usually aggregate either under stones or in fissures. Sexually active males are an exception, establishing and defending territories where they attract females. The scarcity of food makes fighting energetically costly, so encounters between males usually only involve display. This is a behavioral adaptation to life underground.
Reproduction has only been observed in captivity so far. Sexually mature males have swollen cloacas, brighter skin color, two lines at the side of the tail, and slightly curled fins. No such changes have been observed in the females. The male can start courtship even without the presence of a female. He chases other males away from the chosen area, and may then secrete a female-attracting pheromone. When the female approaches, he starts to circle around her and fan her with his tail. Then he starts to touch the female's body with his snout, and the female touches his cloaca with her snout. At that point, he starts to move forward with a twitching motion, and the female follows. He then deposits the spermatophore, and the animals keep moving forward until the female hits it with her cloaca, after which she stops and stands still. The spermatophore sticks to her and the sperm cells swim inside her cloaca where they attempt to fertilize her eggs. The courtship ritual can be repeated several times over a couple of hours.
Longevity is estimated at up to 58 years. A study published in Biology Letters estimated that they have a maximum lifespan of over 100 years and that the lifespan of an average adult is around 68.5 years. When compared to the longevity and body mass of other amphibians, olms are outliers, living longer than would be predicted from their size.
Olms from different cave systems differ substantially in body measurements, color and some microscopic characters. Earlier researchers used these differences to support the division into five different species, while modern herpetologists understand that external morphology is not reliable for amphibian systematics and can be extremely variable, depending on nourishment, illness, and other factors even varying among individuals in a single population. Proteus anguinus is now considered a single species. The length of the head is the most obvious difference among various populations – individuals from Stična, Slovenia, have shorter heads on average than those from Tržič, Slovenia, and the Istrian peninsula, for example.
The black olm (Proteus anguinus parkelj Sket & Arntzen, 1994) is the only recognized subspecies of the olm, endemic to the underground waters near Črnomelj, Slovenia, an area smaller than 100 square kilometres (39 sq mi). It was first found in 1986 by members of the Slovenian Karst Research Institute who were exploring the water from Dobličica karst spring in the White Carniola region.
|Feature||Proteus anguinus anguinus||Proteus anguinus parkelj||Notes|
|Skin||Not pigmented.||Normally pigmented, dark brown, or black in color.||The most obvious difference.|
|Head shape||Long, slender.||Shorter, equally thick. Stronger jaw muscles visible as two bulbs on the top of the head.|
|Body length||Shorter, 29–32 vertebrae.||Longer, 34–35 vertebrae.||Amphibians do not have a fixed number of vertebrae.|
|Tail||Longer in proportion to the rest of the body.||Shorter in proportion.|
|Eyes||Regressed.||Almost normally developed, although still small compared to other amphibians. Covered by a thin layer of transparent skin, no eyelids.||Regressed eye of White Proteus shows first of all immunolabelling for the red-sensitive cone opsin. The eye of Black Proteus has principal rods, red-sensitive cones and blue- or UV- sensitive cones.|
|Other senses||Specific and highly sensitive.||Some sensory organs, particularly electroreceptors, less sensitive.||Not very obvious.|
These features suggest that the black olm has probably colonized underground habitats more recently and still retains some nontroglomorphic characteristics.
The first written mention of the olm is in Janez Vajkard Valvasor's The Glory of the Duchy of Carniola (1689) as a baby dragon. Heavy rains of Slovenia would wash the olms up from their subterranean habitat, giving rise to the folklore belief that great dragons lived beneath the Earth's crust, and the olms were the undeveloped offspring of these mythical beasts. In The Glory of the Duchy of Carniola, Valvasor compiled the local Slovenian folk stories and pieced together the rich mythology of the creature and documented observations of the olm as "Barely a span long, akin to a lizard, in short, a worm and vermin of which there are many hereabouts".
The first researcher to retrieve a live olm was a physician and researcher from Idrija, G.A. Scopoli; he sent dead specimens and drawings to colleagues and collectors. Josephus Nicolaus Laurenti, though, was the first to briefly describe the olm in 1768 and give it the scientific name Proteus anguinus. It was not until the end of the century that Carl Franz Anton Ritter von Schreibers from the Naturhistorisches Museum of Vienna started to look into this animal's anatomy. The specimens were sent to him by Žiga Zois. Schreibers presented his findings in 1801 to The Royal Society in London, and later also in Paris. Soon the olm started to gain wide recognition and attract significant attention, resulting in thousands of animals being sent to researchers and collectors worldwide. The basis of functional morphological investigations in Slovenia was set up by Lili Istenič in the 1980s. More than twenty years later, the Research Group for functional morphological Studies of the Vertebrates in the Department of Biology (Biotechnical Faculty, University of Ljubljana), is one of the leading groups studying the olm under the guidance of Boris Bulog. There are also several cave laboratories in Europe, where olms have been introduced and are being studied. These are Moulis, Ariège (France), Kent's Cavern (England), Han-sur-Lesse (Belgium) and Aggtelek (Hungary). They were also introduced into the Hermannshöhle (Germany) and Oliero (Italy) caves, where they still live today.
Far from feeling surprise that some of the cave-animals should be very anomalous...as is the case with blind Proteus with reference to the reptiles of Europe, I am only surprised that more wrecks of ancient life have not been preserved, owing to the less severe competition to which the scanty inhabitants of these dark abodes will have been exposed.
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. 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. The olm is illegally taken by collectors.
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 olm 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. 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 a Slovenian Red list of endangered species. Postojna Cave and other caves inhabited by the olm were also included in the Slovenian part of the Natura 2000 network.
In Croatia, the olm is protected by the legislation designed to protect amphibians – collecting is possible only for research purposes by permission of the National Administration for Nature and Environment Protection. Conservation status in Bosnia and Herzegovina and Montenegro has not yet been defined.
The olm is a symbol of Slovenian natural heritage. The enthusiasm of scientists and the broader public about this inhabitant of Slovenian caves is still strong 300 years after its discovery. Postojna Cave is one of the birthplaces of speleobiology due to the olm and other rare cave inhabitants, such as the blind cave beetle. The image of the olm contributes significantly to the fame of Postojna Cave, which Slovenia successfully utilizes for the promotion of ecotourism in Postojna and other parts of Slovenian karst. Tours of Postojna Cave also include a tour around the speleobiological station – the Proteus vivarium, showing different aspects of the cave environment.
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