Life History, Abundance, Activity, and Special Behaviors
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 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).
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).
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).
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