Salamanders - The Olm

Olm, Proteus

Above: a model of the mysterious Olm, head-end,  a cave-dwelling salamander.

Karst landscapes are characterized by water soluble rocks that slowly dissolve, such as limestone (calcium carbonate, which slowly dissolves in acidified water). Karst covers 20 to 25% of the land surface of the Earth and frequently forms spectacular landscapes and as water seeps into the rocks, dissolving them it forms sinkholes and caves. In some cases, vast networks of caverns stretch for many miles beneath the ground and may be several miles deep. Their true extent is unknown and many must remain unexplored. These bizarre subterranean grottoes may drip with biofilms, forming hanging snottites that drip sulfuric acid on unwary passers-by. Indeed these bacteria excrete sulfuric acid and they likely helped subterranean rivers carve out the vast caverns. Bizarre cave rock formations or speleothems form breathtaking wonders, such as stalactites, stalagmites, columns, flowstone, drapers, straws and flower-like anthodites to name but some of the principal types. Plants may inhabit the entrances to these caves, which may be used as lairs for various animals that venture out onto the surface, but deeper down, where there is no sunlight at all, microbes and arthropods support an ecosystem of higher predators. Animals that dwell in caves but nowhere else are called troglobites (troglobionts). Many are unique to a particular cave system, having evolved in isolation from the outside world. Troglobite vertebrates are certain specialised species of fish and salamander amphibians. The Olm is a stygobite: a troglobite that leads an aquatic existence.

Olm, Proteus

Salamanders, in the modern broad sense of the word includes all the urodeles, lizard-like amphibians: salamanders, newts, olms, mudpuppies, amphiumas, sirens and their kin. Most are not troglobites, but several (about 13 species) are, including the Olm (the Proteus, Proteus anguinus, found in Europe, Eurcea wallacei (Georgia Blind Salamander) and Eurycea rathbuni (the Texas Blind Salamander). These are both examples of blind salamanders with rudimentary eyes and pale skin lacking pigment. In Proteus the eyes are covered in skin in the adult (though still sometimes visible as black dots beneath the dorsal surface at the base of the snout) and are not embedded in the skull (which lacks orbits) but are embedded in soft connective tissue and connected to the skin by gelatinous material.

Olm, Proteus

The Olm occurs in a region of Karst covering parts of Croatia which has more than 7000 registered caves (46% of Croatia's land is karst), Slovenia, Bosnia and Herzegovina and reaches 30 cm (12 inches) in length (compared to 13 cm or 5 inches for the Texas Blind Salamander). It is a top predator in this mysterious ecosystem.

Many cave-dwelling salamanders are surface dwellers, living near cave entrances and are pigmented with eyes, such as Eurycea troglodytes. The Black Proteus is a subspecies of Olm, Proteus anguinus subspecies parkelj that naturally possesses dark pigmented skin and clearly visible eyes - it has no troglomorphic features - and is found in the same karst habitats, e.g. in Slovenia. It is distinct from white olms exposed to sunlight. The Black Proteus also has shorter limbs, a shorter tail, a longer trunk with more trunk vertebrae and a different head morphology with a less elongated snout and fewer teeth. Although found in subterranean streams in different parts of the karst landscape it has clearly been subject to different selection pressures.

External Characteristics

The body is snake-like and cylindrical (but slightly taller than wide) and faintly grooved (due to the metamerically segmented muscle blocks and skeletal system characteristic of vertebrates). The beak-shaped mouth is flat, narrow and duck-like. The upper jaw is larger and lipped. Just above the lip, on the sides of the head is a pair of small triangular nostrils (external nares). The mouth is visible beneath the head.

The slender legs have 3 toes on the forelimbs and 2 on the hindlimbs (compared with 4 and 5 respectively in the Texas Blind Salamander). The appearance of the Olm accounts for one of its common names: 'The Human Fish'.

The skin is covered with tiny pores, some of which are mucus-secreting glands: the Olm can secrete copious mucus, especially when irritated. When exposed to light (and possibly heat) continuously, the Olm develops dark cinnamon brown or violet skin with scarlet blotches and will lose this color again after several days in darkness. This is clearly a protective stress response, but in its normal environment the Olm will not encounter light unless washed out of its cave.

The back and head are described as a whitish-red in color, the sides and tail more violet, the belly white (bluish above the liver). the skin is diaphanous, that is delicate and translucent. In addition to the pores, there are minute reddish spots on the skin.

Gas Exchange

Three pairs of external gills are borne on the sides of the head. These gills are flushed with blood, which appears dark at the base of the gill stem (deoxygenated blood) and bright red elsewhere (oxygenated). The external gills of salamanders have various morphology. A single stem gives rise to a comblike array of secondary lamellae on either side in the comb-type of gill, but in the antler type of gill the main stem gives rise to secondary branches which bear small tertiary branches in a tree-like manner. Both gill types have been observed in the same species, with the antler-type occurring more often in stream-dwelling forms and the comb-type in pond-dwellers. Evidently, the morphology adjusts to the oxygen (and perhaps excretory and pH-regulation) demands of the animal. The model here has the antler-type of gills following several detailed descriptions of gills in the Olm (compare this to the lake-dwelling Axolotl, photographs of which generally show a comblike arrangement of secondary lamellae. When alarmed, the gills of the Olm turn pale (as blood is diverted away from them) and are retracted to protect them from damage. The gills of salamanders regenerate if damaged. There are three gill arches on either side of the head, each supporting a gill, but no gill slits.

The retention of external gills in aquatic forms, like the Olm, is an example of neoteny. Neoteny is a type of paedomorphism: the retention of juvenile or embryonic features in the mature adult. There are two basic types of paedomorphism: neoteny involves the retardation of development in body features, so the mature animal retains juvenile features, whereas progenesis involves an acceleration of sexual maturity so the juvenile becomes sexually mature. The Olm, like the Human Being, demonstrates neoteny. The neotenic Axolotl can be made to undergo metamorphosis into a mature animal by addition of thyroxine, but does not do so in nature (but retains the necessary genes possessed by its evolutionary ancestors, but in the OFF state due to the lack of iodine in its environment).

Salamanders may also possess lungs and can also exchange gases through their skin and perhaps also the lining of the bucco-pharyngeal cavity (oral cavity and throat). Proteus possesses a pair of lungs with the typical salamander arrangement. Air is pumped into the bucco-pharyngeal cavity through the mouth and nares (nostrils) by muscular action and enters a single aperture, the glottis, on the ventral floor towards the back of the lower jaw. The glottis opens into a short tube or trachea which opens into a small sac. This sac (air-sac) is the laryngo-tracheal chamber) from which the air enters a pair of bronchi, one on either side, which conveys the air to the pair of elongated lungs (sometimes called air-bladders in the old literature). The lungs are suspended from the dorsal body wall by pleural mesenteries (double folds of connective tissue) and attached ventrally to the liver via a ligament. The laryngo-tracheal chamber, as the name suggests, contains the larynx (the equivalent structure contains a pair of folds or vocal cords in male frogs). The cartilages of the larynx are essentially modified pharyngeal arches. In salamanders the external nares open into a pair of olfactory sacs, each of which opens by an internal nare in the front part of the roof of the mouth into the buccal cavity (oral cavity).

In fish the pharyngeal arches support the gills and the spaces between them become perforated by gill slits, with the first (frontmost) pair or two becoming modified to form the jaws and another pair are modified to form the hyoid bone which anchors the tongue. Water from the pharynx is pumped across the gills and out of the gill slits for respiration in fish and, in some species, for filter feeding too with gill rakers sieving tiny food particles from the water.

In amphibians the pharyngeal arches continue to contribute to the skeleton of the larynx, lower jaw and associated structures.The Olm has no pharyngeal slits

In mammals, including humans, the pharyngeal arches persist as the skeleton of the larynx, as the hyoid bone, the middle ear and its bones, the lower jaw and other structures in the lower jaw and neck but the pharynx does not become perforated by slits. In the mammalian embryo indentations or pockets appear appear between the pharyngeal arches but they do not complete the perforation process. In other words, humans apparently owe their ability to speak to the fact that their worm-like / fish-like ancestors once possessed pharyngeal slits used for filter-feeding and/or respiration.

The Olm is apparently not vocal, but has been noted for its ability to make a very loud hissing sound, like steam being released under pressure, and can also make smacking sounds.

Olm, Proteus

Locomotion

The Olm may crawl or glide along the bottom when submerged in water by use of the limbs only, sometimes using only the forelimbs with the hindlimbs tucked against the body, although it has been reported that the limbs are generally to feeble for efficient locomotion (compare to the Texas Blind Salamander which appears to have stronger legs and a more upright posture). It has been stated that the limbs appear to be used in crawling but actually provide no propulsion: appearing to use the limbs when swimming near the bottom but the tail providing the main propulsion when creeping. different authors provide different descriptions of locomotion in the Olm. When swimming the limbs are pressed to the sides and not used. The Olm may also make serpentine lunging movements in water and has been said to move like a snake, a salamander and a fish. Apparently it possesses feeble locomotive abilities on land, pushing with its hindlimbs and lunging forward with little effect. The Olm sinks to the bottom when still.

The skeleton is membranous in parts, cartilaginous and bony in others. The cranium bones are thin and sometimes the brain can be seen through them. The hardest bones are the lower jaw and the branchial bones. the first two gill arches are supported by bone, the third by cartilage. The limb girdle bones are little developed. The cranium has no temporal fossae, no zygomatic processes and no orbits.

There are 59 vertebrae, the last of which is cartilaginous. There are 29 neck and back vertebrae, 3 sacral vertebrae (compared to 2 in some salamanders) and 27 tail vertebrae.

Nutrition

The lower jaw is horizontal, right up to its articulation with the temporal bones of the cranium. There are small conical teeth on both jaws: about 60 on the upper jaw and about 70 on the lower jaw. The muscular tongue is supported by the hyoid bone. The throat / esophagus is very short. The stomach is straight and resembles the anterior part of teh intestine. the intestine is convoluted (but may straighten in preserved specimens). the elongated liver occupies about two-thirds the length of the abdomen and is accompanied by a gall bladder. The spleen sits beside the stomach and the pancreas is about half as long as the spleen.

Food is scarce in deep caves, but the Olm can go for several years without years, perhaps 10 years or more, and apparently stays very still throughout. It is a predator and will ambush any arthropod or snail that ventures nearby. The fleshy tongue assists with the swallowing of food, but highly extendible tongues used in prey capture have not evolved in those salamanders that possess lungs, such as the Olm.

Excretion

In the Olm, the gonads and kidneys empty into the intestine, via the ureters, near the anus and hence through the cloaca. In the Olm, the kidneys are very long and traverse the length of the lower half of the trunk. A bladder, presumably for storage of urine, opens into the intestine opposite the direct openings of the ureters.

Ancestrally and embryonically the vertebrate kidney develops as a series of tubular units, originally one pair per body segment beginning anterior and proceeding towards the posterior, so that the anterior parts form first and are the oldest. The anterior units form the pronephros, which degenerates in amphibians; the middle units form the mesonephros, which persists as a segmented structure in salamanders; the rearmost units form the metanephros. The metanephros forms the kidney of adult reptiles, birds and mammals. The amphibian kidney is an opisthonephros, formed from embryonic meso- and metanephros (the latter forming the rearmost part of the kidney). A number of tubules convey urine from each kidney to a common urinary opening, hence one pair of urinary openings occur, in the cloaca region.

Circulatory System

The heart is reported to consist of a single auricle and a single ventricle, like the 'heart of a frog' (Configliachi & Rusconi, 1821; see also Schreibers, 1801) however, it is now realized that the heart of the frog consists of two auricles and one ventricle. In the frog (Rana) the left auricle receives oxygenated blood from the lungs (via the pulmonary veins) and the right auricle receives blood from the rest of the body via a triangular venous sinus (sinus venosus) into which the three venae cavae empty. (The vena cavae are the large veins returning blood from the body to the heart). Both auricles then contract together and empty into the ventricle via one-way valves.

Thus the circulation of the frog is not completely double, as in mammals with their 4-chambered hearts, nor is it completely a single circuit as in most fish (with 2-chambered hearts) but intermediate and partially double, with the ventricle pumping a mixture of oxygenated and deoxygenated blood around the body.

This type of system is also found in salamanders in general, in which the division between the two atria is not externally apparent, as it is in the frog, and the left auricle is small but internally divided from the right auricle. Again a triangular venous sinus connects the vena cavae to the right atrium.The salamander heart is in general relatively smaller than that of the frog. Not all salamanders have lungs however,indeed about two-thirds of species are lungless and so have no pulmonary veins. A recent study by Lewis and Hanken (2017) using X-ray microtomography has shown a partial septum separating left and right atria in two species of salamander from two separate lineages. This suggests that loss of the septum (whether partial or complete) evolved separately in different lineages by convergent evolution. Thus the left and right auricles fuse into a single functional atrium. Proteus does possess lungs so we would expect there to be a pair of auricles in this salamander.

One artery leaves the top of the ventricle as an expanded bulb that branches into two large arteries that supply the branchial apparatus with branches coursing through the branchial arches and then leave the arches to enter the external gills where they branch in a tree-like manner. The branchial veins leave the gills, entering back into the body to supply the rest of the head and body. That leaving the first arch becomes the 'common carotid' supplying the head. The vertebral artery travels inside the spin along the tail.

Nervous system and Senses

The tiny eyes are covered by skin but still receptive to light. The general skin (or underlying nerves?) is also receptive to light, though only about half as sensitive as the eyes. light is a noxious stimulus for the Olm which will do its best to avoid it. The degree of degeneration of the photoreceptors in the eyes of Ohms depends on the population. Generally the outer segments of the sensory cilia are degenerate and the inner segments also in some cases and in addition to rhodopsin the red-sensitive cone opsin may be present (Schlegel et al. 2009).

The Olm is electroreceptive, possessing individual ampullae in its skin: pits with a mucilaginous material filling the entrance canal and which encloses a sensory cell or neuromast. The skin also contains sensors that will detect the movements of potential prey under water and perhaps the presence of nearby obstacles. these are adaptations to the dark environment of the Olm, though these abilities may be found in other salamanders. Olms are also sensitive to the Earth's geomagnetic field which they can utilize for navigation and orientation. The external nares open into the pair of olfactory sacs which presumably have an olfactory function in the Olm and in amphibians generally each olfactory sac has a vomeronasal organ, which in mammals is known to be important in detecting pheromones.

Typical of amphibians, the salamander brain has the grey matter (neuronal cell bodies) towards the inside (around the ventricles) and the white matter on the outside, such that the brain is really an expansion of the spinal cord. In mammals this state occurs in the embryonic brain, before the neuronal cell bodies migrate outwards to the cortex, leaving trailing axons to form the white matter underneath in the medulla. This allows them to occupy a larger surface area in the convoluted cerebral cortex, increasing the number of neurones that can be packed into a given volume. (Failure of this process causes a number of recognized brain developmental abnormalities in humans and is suspected in a number of other mental disorders). Lacking this development, the white matter cortex of the amphibian brain appears smooth. The salamander brain is much elongated and at the front a pair of olfactory bulbs connect to a pair of cerebral hemispheres. The cerebellum (largely responsible for coordinating and learning movement) at the back is small in the Olm.

Life-Cycle

The Olm reproduces about every 12 years or so. It is oviparous (lays eggs) and an earlier observation regarding live births was erroneous. The Olm lives an estimated average of about 70 years, but some individuals are thought to live about 100 years.

In the female Salamandra a pair of ovaries release yolky eggs that make their way into the pair of oviducts through their funnel-like openings situated near and to the side of the bases of the lungs. The oviducts are convoluted tubules that extend the whole length of the abdominal cavity. Movement of eggs into the funnels and down the oviducts is probably assisted by ciliary action. The oviducts connect to the pair of ovisacs, each of which opens into the cloaca by its own genital opening. In the male multiple tubules from the elongated testes connect to a single common pair of urogenital pores, borne on urogenital papliiae, in the cloaca. In the female the kidneys connect to a separate pair of urinary pores borne on urinary papillae. In the Olm, however, the gonads and kidneys reportedly empty into the intestine near the anus, and hence through the anus. The pair of gonads enters the intestine via a common aperture. these two descriptions sound very different until one recalls that the cloaca of an amphibian is a common portal for the intestine and urogenital exits.

Some salamanders use external fertilization in water, but most rely on internal fertilization without the use of an intromittent organ by means of transferring a spermatophore (a packet of spermatozoa). Very little is known about the courtship behavior of the mysterious Olm. The elaborate courtship rituals of some salamander species, such as the European Smooth Newt, Triturus vulgaris, are well documented. In this case it takes place on the bottom of a pond and the sequence is as follows:

  1. When the male encounters a female he approaches her and sniffs her to ensure she is a receptive female of the same species.
  2. Orientation phase. The male moves in front of the female to block her path, but she frequently turns away from him. The male may repeat this behavior and if the female is receptive she will eventually stop and face the male.
  3. Static display. The male displays to the stationary female with a variety of vigorous tail movements such as fanning, waving and whipping.
  4. Retreat display. If the female is interested she begins to move towards the male who retreats, walking backwards, whilst continuing his display for about half a minute.
  5. Creep and follow. The male now turns and walks slowly away from the female who follows the male.
  6. Spermatophore transfer. The male will position himself and quiver his tail until the female touches it and then he will deposit a spermatophore onto the substrate. The male needs to position the female correctly so she can take up the spermatophore into her cloaca. He creeps forwards, stops and touches the female with his tail and pushes her back into the correct position. If this step is unsuccessful and the male is carrying more than one spermatophore he may quickly deposit one and then return to step 4.

Such an elaborate ritual ensure no mistakes are made and every species has a significantly different courtship ritual. Such rituals are an important mechanism of speciation (the evolution of new species) since if a male or female adopts a slightly different ritual they may only be successful with a sub-population of the opposite sex that responds correctly and in the fullness of time this breeding group could potentially become a new subspecies and eventually a new species.

Newts exchange gases across their skin and across their lungs, but strenuous muscle activity requires the newt to surface to breathe air. In the courtship of the Smooth Newt, the male exerts himself more and may need to surface for oxygen. However, he risks losing the female to a rival and if at the crucial stage of spermatophore transfer he will resist surfacing even when low on oxygen for as long as possible.

Suggested Reading

Aljancic, G., 2019. History of research on Proteus anguinus Laurenti 1768 in Slovenia. Folia Biologica et Geologica 60/1.

Configliachi, P. and Rusconi, M., 1821.Observations on the natural history and structure of the Proteus anguinus (BHL: https://www.biodiversitylibrary.org/page/32499225#page/5/mode/1up).

Francis, E.T.B. 1934. The anatomy of the Salamander.Oxford: The Clarendon Press. (https://www.biodiversitylibrary.org/item/29021#page/9/mode/1up)

Hawes, R.S. 1945. On the Eyes and Reactions to Light of Proteus anguinus.

Konrad, K. and Šarić , K.K. The deepest finding of an Olm (Proteus anguinus): Zagorska Pec, Ogulin, Croatia. Acta Carsologica 46(2-3): DOI: https://doi.org/10.3986/ac.v46i2-3.5152

Istenic, L. and Bulog, B., 1984. Some evidence for the ampullary organs in the European cave salamander Proteus anguinus (Urodela, Amphibia). Cell tissue Res. 235: 393-402.

Lewis, Z.R. and Hanken, J. 2017. Convergent evolutionary reduction of atrial septation in lungless salamanders. J. Anat. 230: 16-29. DOI: https://doi.org/10.1111/joa.12535

Mali, L.B. and Sket, B. History and biology of the Black Proteus (Proteus anguinus parkelj Sket & Arntzen 1994: Amphibia: Proteidae): a review.

Mattes, J. Traveling Olms: Local and Global Perspectives on the Research on Proteus anguinus (1700 - 1930). DOI: org/10.26337/2532-7623/MATTES

Schlegel, P.A.,  Steinfartz, S. and Bulog, B., 2009. Non-visual sensory physiology and magnetic orientation in the Blind Cave Salamander,  Proteus anguinus  (and some other cave-dwelling urodele species). Review and new results on light-sensitivity and non-visual orientation in subterranean urodeles (Amphibia). Animal Biology 59: 351–384.

Schreibers, C. 1801. A Historical and Anatomical Description of a Doubtful Amphibious Animal of Germany, Called, by Laurenti, Proteus anguinus. Philosophical Transactions of the Royal Society of London. 91: 241-264.

Soares, D. and Niemiller, M. L. 2020. Extreme adaptation in cabes. The Anatomical Record 303: 15-23.
 
Voituron, Y., de Fraipont, M., Issartel, J., Guillaume, O. and Clobert, J. 2011. Extreme lifespan of the human fish (Proteus anguinus): a challenge for ageing mechanisms. Biol. Lett. 7: 105-107.

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Article created: 23 Oct 2020.

24 Oct 2020 - This article is still being developed