SCIENTIFIC INTRODUCTION TO
about the Slovene Black
not yet applicable to Bosnia & Herzegovina.
RED LIST STATUS :
in the Zoological Society of London,
one of the 10 most endangered amphibian species on the planet.
to another webpage on this Website
BiH Project No.3. [SDZB-DKRS-JI / BiH / H / SLO / UK / 140800PTPH.]
SCIENTIFIC INTRODUCTION TO Proteus anguinus anguinus (Laurenti 1768.)
Publication Abstracts are cited fully in the BIBLIOGRAPHY Section on Proteus
Project Webpage 2. A GLOSSARY is now in Section 10. on Proteus Project
is indicated by the token number of entries in the Bibliography Section
2., the amount of research that has been conducted on the animal is
both extensive and on-going.
it has been reasonable to do so, the following descriptive text has been
augmented with Abstracts of the results obtained from scientific research
by many specialists, almost always under artificial conditions.
support readers in locating the full Articles to which the Abstracts refer,
all Papers and the technical journals in which they are published, are
cited within the text and further referenced in the extensive Bibliography
2. in the next "Proteus Project" Webpage.
where it has been possible for us to do so, without compromising any Proteus
anguinus habitat locations, we have now included some of our own observations
about Proteus anguinus in its natural habitat.
Scientific name :..Proteus
anguinus anguinus (Laurenti 1768).
/ Carstvo / Царство : Animalia.
a back-bone or spinal column).
/ Razred / Разред : Amphibia.
Class of Vertebrates typically gill-breathing in the larval state and lung
/ skin breathing as adults).
/ Podrazred / Подразред : Lissamphibia.
/ Red / Ред : Caudata (Scopoli,.1777)
Urodela. (Amphibia with
/ Porodica / Породица :
/ Rod / Род : Proteus.
/ Vrsta / Врста : Proteus anguinus.
: Proteus anguinus anguinus (Laurenti,.1768).
Common / Trivial Names : "The White
Proteus"; "Human Fish"; "Cave Olm"; "Cave
= "Човјечија рибица";..Hrvatski
/ Bosanski = "Čovječja ribica";...Slovene
= "Človeška ribica" and
= "Barlangi Vakgőte";..German
= "Odmieniec Jaskiniowy".
related sub-Species : Proteus anguinus
parkelj, (Sket et Arntzen,.1994)..[=The
Black Proteus], currently
found only in Slovenia.
may be other, as yet unknown sub-species.]
are the extant descendants of the first vertebrate class to successfully
colonize terrestrial environments; hence they occupy a unique position
between fish and reptiles.
general, amphibian skin provides essentially no resistance to evaporative
water-loss and consequently, daily water turnover rates are an order of
magnitude greater than in other terrestrial vertebrate groups. This has
led to a suite of physiological, morphological and behavioural adaptations
that have allowed a successful terrestrial existence in spite of this apparently
spendthrift water retention strategy. Proteus anguinus, however,
is a mostly aquatic amphibian .......
is an ancient family of salamanders comprising just six species, commonly
referred to as the olm, mudpuppies and waterdogs. The lineage diverged
from their closest relatives 190 million years ago in the early Jurassic
period in the era of the dinosaurs.
pre-dates the first fossil bird by 40 million years! The family Proteidae
is part of a sub-order of salamanders that contains all of the internally-fertilising
species (known as the “Salamandroidea”). Most salamanders reproduce
via external ferlilsation,
in the proteids, females take the spermatophore (or sperm packet),
deposited by the male, into their bodies, allowing fertilization of her
eggs to occur within the body cavity.
of Proteus anguinus anguinus and its accepted Type Locality :
anguinus was first recorded in the literature 320 years ago by the
Slovene, Baron Janez Vajkard Valvasor.(also
Johann Weikhard Freiherr von Valvasor),
was subsequently mentioned again by Steinberg
in 1761 and also by Jeršinović von Loewengreif.in
Type Locality was originally set as Cerkniško Jezero (=Cerknica Lake)
in Slovenia, because it was mentioned in the original taxonomic description
to subsequent uncertainty and confusion about the validity of the location,
the Type Locality was re-set by the accomplished Hungarian zoologist, Baron
G.J. de Fejérváry (1926) and accepted
as being Magdalene Grotto in Črna Jama,
of the Postojna-Planina Cave System, Slovenia.
Note about Josephus Nicolaus Laurenti :
Nicolaus Laurenti (born
4 December, 1735 - died 17 February, 1805) was an Austrian naturalist.
was the author of "Specimen medicum, Exhibens
synopsis reptilium emendatum, cum experimentis circa venena et antidota
reptilium austriacorum" (1768),.[="Medical
Treatise, Exhibiting an Emended Synopsis of Reptiles, with Experiments
Concerning Venoms and Antidotes for Austrian Reptiles"] about the poisonous
function of reptiles and amphibians and their antidotes. This was an important
book in herpetology, defining 30 genera of reptiles...Carolus
defined only 10 genera.
relevant to us, in 1768, Laurenti
also published an important manuscript titled "Il
Dragone" (="The Dragon"), describing the blind
salamander (amphibian): Proteus anguinus, purportedly collected
from cave waters in Slovenia (or possibly western Croatia);
description represented the first published account of a cave animal in
the western world.
Note about the work of Dr Mauro Rusconi and Pietro Configliachi with
19th century Italian naturalists Dr. Mauro
their "Monografia del Proteo anguino di Laurenti"
the year 1819. Dr. Rusconi ,
the dentist in Pavia and he performed much anatomical research on live
and dead Proteus specimens.
results of their work was based on the deaths of many specimens of Proteus
and included dissection and experimentation on live as well as dead individuals!
Shortly after the publication of their Monograph, it was translated into
English and reproduced in the Edinburgh Philosophical
Journal, Vol. 5. (1821)*.
protectors of Proteus anguinus, to us involved in the "Proteus Project",
the translated text reads, in places, like a gothic horror story as it
references and details the dissection and experimentation on the live animals,
our readers' enlightenment, we shall include further extracts from the
translated work of M. Rusconi
and P. Configliachi
in the relevant Sections of text below and we especially reproduce their
anatomical drawings in Section (s)below.
you wish to aquaint yourselves with the full text of the English Translation
of their work, please refer to "Proteus Project Webpage 2." (Bibliography)
and download the relevant document.
on abandoned 19th Century Taxonomic Descriptions of Proteus :
(1850) described a series of "new species"
under the Genus "Hypochthon". Although Proteus exhibits a natural
variation in appearance and genetic composition across its geographical
range, Fitzinger's taxa were never accepted.
did provide a list of all Proteus habitats known at that time and even
falsified other entries ! We include details of his taxa here, merely
for historical interest.
various "species" he described in Slovenia, he ascribed the following taxa:..Hypochthon
zoisii (Fitzinger); Hypochthon schreibersii (Fitzinger);
Hypochthon freyeri (Fitzinger); Hypochthon haidingeri (Fitzinger);
xanthostictus (Fitzinger) and for those he described in Croatia, he
added Hypochthon carrarae (Fitzinger). In 1880, Proteus croaticus
of the Species :
archaic species. Several theories for its origin have been suggested
by various "specialists".
determining its true origins, a more thorough knowledge is required of
its actual geographical range and more work has to be undertaken in regard
to DNA profiling.
lineage supposedly diverged from its closest relatives 190 million years
ago in the early Jurassic period in the era of the dinosaurs.
theory is that it is a suspected Tertiary fauna relict, supposedly originating
as a marine animal progressing firstly into brackish then adapting to fresh
water conditions inland as a result of the Messinian Salinity Crisis in
the Meditteranean Sea
the period 7.2 to 5.33 million years ago. However, because the species
retains the ability to darken its skin colour in light conditions and because
it has atrophied eyes rather than no eyes, its previously assumed ancient
lineage is now a matter for fresh debate.
current line of thought proposes that its origin was as an epigean species
living in freshwater surface lakes, from where it was forced underground
by the increasingly cold climate of the last glacial period and where it
then had to adapt to hypogean conditions.
research in progress at the Biotechnical Faculty of Ljubljana University
is seeking to develop a gene database of Proteus anguinus to highlight
any differences in the genetic make-up of specimens across the range of
its geographical distribution.
specialists at the Faculty are also engaged upon the task of trying to
develop a plausible schema for the evolution of the species and an explanation
for its geographical distribution. More information about this can be obtained
by referring to the relevant entries in the Bibliography in.Section
2. of the "Proteus Project" Webpages.
Range of its Natural Habitats (1), as recorded in the published literature
karst water environment from Italy, (east of the River Isonzo in the areas
around Gradisca, Fogliano, Redipuglia and Monfalcone) and Slovenia, through
Croatia to Bosnia & Hercegovina.
is partly illustrated by an Abstract of Biogeography by Sket,
his Paper "Distribution of Proteus (Amphibia:
Urodela: Proteidae) and its possible explanation."
250 localities of the nominal species Proteus anguinus (Laurenti 1768)
have been evaluated and listed. The species is limited to the Dinaric Karst;
it ranges from the Tsonzo-Soca River in southeastern Venezia Giulia, Italy,
through the southern half of Slovenia, southern Croatia, and parts of Bosnia
and Hercegovina, to the Trebišnjica River in Eastern Hercegovina. In some
regions, Proteus anguinus populations have been extinguished or endangered
by pollution or human-induced hydrographical changes.
distribution of Proteus is comparable with that of some cave Crustacea:
Troglocaris (Crustacea: Decapoda), Monolistra, and Titanethes (Crustacea:
Isopoda). The similarity of distribution patterns within this ecologically
diverse assemblage supports their paleogeographic rather than ecological
foundation. The paleogeographical and paleoclimatological data, in combination
with the physiological requirements of Proteus, strongly suggest that these
animals invaded the caves, at least in the NW parts of their ranges,
after the last glaciations, within the last 10,000 years. It is suggested
that the high heterozygosity of populations can best be explained by fusion
of some locally restricted immigration waves."
: This list is grossly inaccurate in its listings for Bosnia & Hercegovina
and serves no useful purpose, either actual or comparative.]
Range of its Natural Habitats (2), as evidenced by direct observation
Project Workers and
Research Assistants within the "Proteus
generally accepted and published detailed geographical range of
anguinus in Hercegovina is substantially not in agreement with our
direct observations. Due to current in-Project restrictions with
the dissemination of this type of data,
are presently unable to clarify this statement.
unnatural Occurrences :
to ill-conceived human intervention, the animal also occurs unnaturally
in the Harz in Germany, in the CRNS underground cave laboratory at Moulis
in France and in the Grotte Oliero in Italy.
ridiculous and ill-advised attempts have also been made to establish it
in artificial environments in Hungary (Baradla barlang, Aggtelek) and in
Devon, UK (in the 1970's) without success.
PHYSICAL CHARACTERISTICS & BEHAVIOURS - supported by our own observations
of Proteus anguinus anguinus in its natural habitat :.
aquatic animal is well adapted to its underground environment. Proteus
anguinus anguinus is a true troglobiont often referred to as
body consists of a Head, Trunk, Tail, two slender but fully functional
Forelimbs and two Rear Limbs. The front legs bear 3 toes and the rear legs
have 2 toes each.
relatively large triangular head ends bluntly in a flattened snout and
in its mouth contains tiny teeth. The male of the species is usually smaller
than the female of equivalent age.
attachment to particular Residence Sites within a general Habitat Location
the progress of the Project, we have observed that Proteus anguinus.is
reliably found, most often in groups, in specific locations year after
year. It seems to favour certain "residence sites" within a given habitat
location, not only year after year but also during the year. Where it is
found in groups, this is often in cave lakes with a water surface, ie.
vadose conditions, or in shallow phreatic and/or epiphreatic cave passages.
Where the species is found in regularly used "residence sites" deep
under water in phreatic conditions, they are usually found as single representatives.
can perhaps enlarge on this by considering a recent contribution in the
field of Experimental Zoology by Guillaume,
O. (2002), in his Paper."The
Importance of Chemical Communication in the Social Behaviour of Cave Salamanders.
Comparison Between a
(Proteus anguinus L., Proteidae) and a Facultative (Euproctus asper D.,
Salamandridae) Cave Dweller." :-
communication is known to be a great importance in animals. It is generally
expected that chemical cues will dominate in cave forms, which cannot use
vision to regulate their behaviour. To obtain evidence that might support
or refute this hypothesis, we have studied the importance of chemical communication
in the social behaviour of a stygo-bitic salamander, Proteus anguinus,
and in a facultative cave dweller Euproctus asper.
first part of this work deals with social interactions between conspecifics.
Ethological two-choice tests and observations during rearing have shown
that adults of P. anguinus exhibit an attachment to a residence site, and
mark it using a substrate-adherent substance and faecal pellets. This marking
is used as directional information, allowing individuals to relocate their
residence site. Furthermore, this marking attracts conspecifics that then
display a gregarious behaviour. Similar tests with E. asper, together with
a field study on four populations representative of the different types
found in the Pyrenees (epigean populations from low, middle and high attitudes
and a cave population), show that E. asper do not exhibit site attachment
and do not mark the site they use. In fact, individuals travel continuously
through their environment and shelter on the way. They thus tolerate the
presence of conspecifics. The results of this study therefore indicate
that P. anguinus establishes stable open groups, while E. asper forms facultative
and unstable aggregations."
is interesting to note that Proteus exhibits a marked attachment
to particular residence sites within a habitat location. Our observations
in Eastern Hercegovina have begun to show that the type of such
residence sites can often be predicted, in that they have at least two
common characteristics, unspecified here in this text for reasons of habitat-location
to Water Depth and Pressure :
have observed and have recorded still and moving images of Proteus anguinus.at
depths of water varying from 0 - 31 metres, (0 - 98 feet).
to survive high water flow conditions :
it is interesting to note that Proteus seems to be able to maintain
its specifically-favoured residence sites year after year, often after
the most tremendous flows of water through the karst conduits that it occupies.
Therefore, it must be able to select refuge in small crevices where it
can safely shelter out of the main flow of water in the karst conduits
during the winter months.
20cm to 35+ cm (8 to 13.75+ inches) long, Proteus anguinus is the
largest permanently cave-dwelling animal in Europe.
only cave amphibian in Europe. In 2007., we successfully developed
a methodology for directly obtaining biometric data of the animal in its
natural habitat, with the result that we are now accumulating body-mass
and other useful biometric information.
SKIN COLOURING :
common with many other amphibians, including salamanders, the skin of Proteus.contains
essential mucus and waxy layers in the epidermis that protect it from dehydration,
viruses, bacteria and fungi.
to Vandel (1966b).,
the young larvae after hatching from the egg have a greyish appearance,
which, if observed under a microscope, is actually a sprinkling of black
chromatophores (pigmentation cells) covering the entire body with the exception
of the underside. He reports that in laboratory conditions, this pigmentation
develops in total darkness and persists for several months before progressively
diminishing. After one year, the appearance becomes greyish-white and it
is only near the age of 18 months that the young Proteus becomes
completely white. Vandel
also reports that if young individuals are reared in laboratory conditions
in daylight, the pigmentation persists and the Proteus keeps the
black colour it had at the very beginning of the larval development and
becomes even darker. He reports that one particular larva, which had always
been kept in the light in the Moulis Underground Laboratory in France,
had become completely black after 4 years.
has lost its dark skin-colouring when usually observed under normal conditions
underground, although the young do retain more of the skin pigmentation.
All Protei darken when exposed to light, the whole body being dermatopic.
The skin without dark pigmentation is slightly pink due to blood circulation
visible through the skin and in some places is yellowish as a result of
riboflavin. Some of the internal physiological arrangement of the Proteus
can often be observed through its skin. The overall colouration represents
the normal skin colour of white European Humans, which is why the species
is often referred to in the South Slavic Languages as Човјечија
and Bosanski); Človeška ribica (Slovene),
in the English Language, all mean "Human Fish". It should be noted
that pterin, a pigmentation typical for amphibians, is not present in the
metabolic rate of Proteus is remarkable in being unusually low,
a factor that also results in a very low growth rate. It saves energy in
every way possible by streamlining its movements and by adopting highly
efficient foraging and reproductive strategies. These are obvious specializations
to cope with a low food supply. It has been described in the technical
journals as being a "good example of a low-energy-system vertebrate", which,
from our perspective of studying the animal in its natural environment
is both glaringly obvious and a gross understatement!
can perhaps enlarge on this by considering a recent contribution in the
field of Experimental Zoology by Hervant,
F.; Mathieu, J. and.Durand,
J. (Jan 2001) in
their Paper "Behavioural, physiological and
metabolic responses to long-term starvation and re-feeding in a blind cave-dwelling
(Proteus anguinus) and a surface-dwelling (Euproctus asper) salamander.":-
effects of long-term starvation and subsequent refeeding on haematological
variables, behaviour, rates of oxygen consumption and intermediary and
energy metabolism were studied in morphologically similar surface- and
cave-dwelling salamanders. To provide a hypothetical general model representing
the responses of amphibians to food stress, a sequential energy strategy
has been proposed, suggesting that four successive phases (termed stress,
transition, adaptation and recovery) can be distinguished. The metabolic
response to prolonged food deprivation was monophasic in the epigean Euproctus
asper (Salamandridae), showing an immediate, linear and large decrease
in all the energy reserves. In contrast, the hypogean Proteus anguinus
(Proteidae) displayed successive periods of glucidic, lipidic and finally
lipido-proteic-dominant catabolism during the course of food deprivation.
The remarkable resistance to long-term fasting and the very quick recovery
from nutritional stress of this cave organism may be explained partly by
its ability to remain in an extremely prolonged state of protein sparing
and temporary torpor. Proteus anguinus had reduced metabolic and activity
rates (considerably lower than those of most surface-dwelling amphibians).
These results are interpreted as adaptations to a subterranean existence
in which poor and discontinuous food supplies and/or intermittent hypoxia
may occur for long periods. Therefore, P. anguinus appears to be a good
example of a low-energy-system vertebrate."
information is given by the same Authors Hervant,
F.; Mathieu, J. and.Durand, J. (Aug 2000)in
their Paper "Metabolism and circadian rhythms
of the European blind cave salamander Proteus anguinus and a facultative
cave dweller, the Pyrenean newt (Euproctus asper)."
of circadian rhythmicity, behavior, and metabolism between surface- and
cave-dwelling salamanders allow evolutionary trends in these processes
to be elucidated. The proteid Proteus anguinus, an obligate cave-dweller,
showed no apparent daily rhythm of activity or resting metabolic rate.
In contrast, the salamandrid Euproctus asper, a surface-dweller/facultative
cave-dweller, had a circadian resting metabolic rate and activity cycle.
These circadian rhythms had an endogenous component. The lives of both
studied salamanders were characterized by long periods of inactivity punctuated
by bouts of foraging or exploratory/predatory behavior. Proteus anguinus
had reduced resting metabolic and spontaneous activity rates (considerably
lower than those of most surface-dwelling amphibians), and therefore appears
to be a good example of a vertebrate as a low-energy system. The low metabolic
and activity rates of P. anguinus are interpreted as adaptations to a subterranean
environment, where a poor and discontinuous food supply and (or) intermittent
hypoxia may be present for long period."
SYSTEM AND SENSORY ORGANS :
eyes of Proteus appear as two tiny dots in the young and are atrophied
and covered with skin in the mature animal. In the adult, it is sunk into
the skin. Effectively, Proteus anguinus is visually blind. On the
other hand, the eyes are very conspicuous in the larvae and very young
individuals, in whom it persists for a comparatively long time. Between
hatching and the age of 2 months the eyes reach their maximum size. The
development of the eyes then stops before they have acquired a normal functional
structure and therefore, never develop beyond the embryonic state. The
cornea fails to appear and a thin and fibrous sclerotic membrane covers
the eyes. The eyes are still discernable as a microscopic dot in individuals
of 2½ to 3 years of age.
retina is very thick and has a simple structure and a very small number
(ca. 2000) of degenerated sensors, which are either very poorly or
not differentiated. The lens never has any fibrous differentiation. The
optic nerve is very thin, being 5-8µ in diameter, although it is
complete and reaches the brain. The cessation of growth of the eyes is
followed by a phase of occular regression, which particularly affects the
lens. The latter usually disappears completely during the animal's Juvenile
Stage of development. In an immature Proteus
of about 100 - 220 mm. in length, the diameter of the eye ranges from 0.3mm
(1966b) reports that adult Proteus
can tolerate low-level light for extended periods of time, unlike its eggs
and embryos, which are very sensitive to illumination and are killed by
the light of a 100 watt bulb.
light-sensitive areas of the olm’s body include a “pineal body” in
the centre of the head, and even the skin registers light through the proposed
presence of the photosensitive pigment melanopsin inside specialised cells
since no light penetrates into the hypogean system, this light sensitivity
is seldom, if ever, used.
SENSORY ORGANS :
hearing, the inner ear has specially-developed crystal masses performing
as electro-receptors. 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, pers. observation).
& OLFACTORY SENSORY ORGANS :
the senses of taste and smell, there are well developed chemo-receptors
on its tongue. 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
& 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, where those near the gills probably sense
the chemical composition of water.(Istenič
& Bulog, 1979).
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
this animal stays neotenic throughout its long life span, it is only occasionally
exposed to normal adult hearing in air which is probably possible for Proteus
as with 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,
acoustical orientation in general. Experiments indicate that the best hearing
sensitivity of Proteus is from 10 Hz and up to 15.000 Hz.
lateral line supplements inner ear sensitivity by registering low-frequency
nearby water displacements (Bulog &
Schlegel 2000) and (Schlegel
et. al. 2006).
new type of sensory organs have been analyzed by light and electron microscopy
on the head of Proteus and described as ampullary organs.(Istenič
& Bulog 1984). Proteus has the ability
to register weak electric fields (Schegel
& Bulog, 1997).
electroreceptors are responsible for this ability in Urodelans. 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 3mV cm¹ at best frequencies of 30Hz.
capture is obviously performed by a combination of mechano-, chemo- and
eventually by electro-perception (Schlegel
et. al. 2006).
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 & 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, where those near the gills probably sense the chemical
composition of water (Istenič & Bulog,
locomotion out of water, two pairs of weak legs, spaced wide apart, with
three digits on the front and two on the rear pair, play a major role.
It walks with a snake-like movement. When swimming, it uses its flat tail
which is surrounded by a fin of thin skin, for propulsion, whilst simultaneously
holding its limbs in tight against its body. It is a highly efficient swimmer
and can move extremely fast.
respiration, it retains its external larval gills in the adult stage and
is thus able to live permanently underwater. It breathes through these
gills, which branch out in three bunches immediately behind and on either
side of the head.
are coloured light-pink to bright-red by the blood visible through the
gill structures. The external gills can sometimes appear larger in low-oxygen
conditions, when a greater surface-area of the gill tissue is required
for oxygen take-up.
what were thought to be secondary respiratory organs, it also has two rudimentary
internal lungs and it has been claimed that it can also breathe through
its skin, (ie. three systems in total), although claims for the skin-breathing
method are questionable.
the idea that the internal rudimentary lungs are merely "secondary" respiratory
organs has now been dispelled because groups of Proteus have been
observed leaving the cave aquatic environment and feeding in the cave's
terrestrial environment and
even at the cave entrance area!!
detailed modern study of the mechanism whereby Proteus gulps atmospheric
air through the mouth in a cave, has not yet been carried out. However,
in further regard to this matter, we now report on the work of a certain
to survive Anoxic (=hypoxic)
ability of amphibians to survive extremes of oxygen availability derives
from a core triad of adaptations: profound metabolic suppression, tolerance
of ionic and pH disturbances, and mechanisms for avoiding free-radical
injury during reoxygenation.
our own observations and results of physico-chemical determinations in
many hypogean habitat locations, the swing from oxic to anoxic and then
back to oxic conditions, can be relatively sudden. We have observed various
survival strategies at work.
long-term anoxic survival, enhanced storage of glycogen in critical tissues
is also necessary.
lifespan of Proteus can be in excess of 100 years, although the
norm is often less. Post-mortem autopsies undertaken on a deceased Proteus
body can approximate its age of its life-span by determining the number
of growth rings on the vertebrae.
longevity in the lifespan of Proteus has again been the subject of renewed
and recent investigations and has called into question the currently perceived
theories about the factors which were thought to have contributed to the
natural ageing process and the limitation
maximum age. Several physiological traits are normally associated with
long-lived animals: larger size, low metabolic rates, and high protection
against oxidative stress. Examples include giant tortoises and elephants
- animals that have large body masses and low
metabolic rates. However, Proteus does not show any of these traits. So
why does it live so long?
"free-radical / oxidative damage" theory, formulated in the early 1950's
and rose to prominence in the 1990's, was widely accepted as being the
responsible mechanism for the restriction in the age or lifespan of many
fauna. However, evidence resulting from the study
Proteus would strongly suggest that this theory does not explain the controlling
factor in the longevity of a species. In a useful overview, Speakman
and Selman (2011)
provide detailed implications of recent research carried out by Voituron,
Y. et al (2010) on Proteus, which revealed
that Proteus appears to have unexceptional defences against oxidative
research is also reported upon by PhysOrg.com.
and completely throws open to speculation the whole question of ageing.
access to the captive breeding colony in the Moulis Underground Laboratory,
together with relevant data on 400 specimens over many decades of data-collection,
the researcher Yann Voituron
estimates that the maximum age that Proteus can achieve is 103 years.
problem for members of the "Proteus Project" is that the report by Yann
Voituron is about a captive colony and is
not about observations of a colony living in any natural habitat. Whilst
we do not disagree with his general conclusions about longevity, basing
a proposed maximum age figure on data from a captive colony in a totally
unnatural living environment is already subject to much doubt. We also
do not agree with several other behavioural traits reported in his Paper
and which seem to be contradicted by observations in the field.
nutrition, it eats a variety of food. It can consume large amounts of food
at once, and store nutrients as large deposits of lipids and glycogen in
and other cave crustacea such as Troglocaris can also occasionally
feature in the natural diet of Proteus, as must phyto-plankton carried
in from the surface. We have photographic evidence that it eats cave snails.
can apparently undergo years without eating. In 1926, an experiment by
de Kerville confirmed that the animal
could not only live in captivity but could survive without being fed. He
kept a captive specimen alive for 14.5 years, during the last 8 of which
he did not feed it..However,
some more recent speleo-biologists have noticed that captive Olms regularly
"slough" and then eat the shed bacterial mucus layer, which, like an extra
skin, covers and protects their whole body. This mucus is sticky and microscopic
examination has shown that in captive amphibians, it becomes encrusted
with bacteria, algae and protozoa.
(1966b) reports that in order to support
reproduction, correct feeding was one of the essential conditions for rearing
this species in the Moulis Underground Laboratory in France. Here, the
adults were fed with crustacea, notably Gammarus, together with aquatic
insect larvae. They also ate earthworms, small fish and tadpoles! He notes
that the Proteus larvae were fed with micro-organisms contained
in the mud of wells or drinking troughs.
the matter of tissue regeneration, the animal has remarkable limb-regeneration
capabilities. A substantial amount of experimental biological investigations
have been undertaken on live Proteus specimens over a great many
years. We do not support such activities being carried out on an already
reproduction, the female has three systems of gestation according to the
most appropriate for the prevailing circumstances. It is most commonly
oviparous (egg-laying). It can lay eggs, larvae or live young. Males and
females differ only slightly in their appearance. In captivity, a female
has laid 70 eggs of about 12mm diameter.
enlarge on the reproductive behaviour, we can provide the following Abstract
from Guillaume, O. (2002),
in his Article "The Importance of Chemical
Communication in the Social Behaviour of Cave Salamanders. Comparison Between
a Strict (Proteus anguinus L., Proteidae) and a Facultative (Euproctus
asper D., Salamandridae) Cave Dweller."
communication is known to be a great importance in animals. It is generally
expected that chemical cues will dominate in cave forms, which cannot use
vision to regulate their behaviour. To obtain evidence that might support
or refute this hypothesis, we have studied the importance of chemical communication
in the social behaviour of a stygobitic salamander, Proteus anguinus, and
in a facultative cave dweller Euproctus asper. ......
P. anguinus, contrary to the non-sexually active conspecifics, sexually
active males shelter apart. The coupling between site-residence marking
and aggressive behaviour towards intruders (except sexually active females),
allows sexually-active males to establish territories for reproduction.
Mate identification requires a close contact, during which pheromones may
be released from cloacal glands. Mates may then exhibit courtship, but
differences between the descriptions of various authors do not allow the
establishment of an unambiguous pattern. After courtship, the male releases
on a stone a spermatophore composed of a peduncle topped by a spermatic
cap. The cap is composed of a coat that ensheathes the spematozoa packed
in a matrix full of mitochondria. The matrix may serve as an energetic
substrate for the sperm survey while the female introduces ther spermatophore
into her cloacae. The female then demarcates a territory for laying, and
stays near the eggs until they hatch. The eggs release a chemical signal
that repels young and adult conspecifics.
E. asper, the male initiates amplexus. He seems not to identify his partner
beforehand and often tries to mate with other males, juveniles and even
individuals of other species. However, mate identification may occur during
amplexus via behavioural interactions and/or pheromones. Then, the male
releases several spermatophores consisting of bundles of a great number
of spermatozoa, embedded in a viscous substance. Spermatophores are apparently
not introduced into the female cloacal ducts, but handled by the male near
the cloacal orifice. This manipulation may facilitate the release of the
spermatozoa from the gangue that pack them. The spermatozoa may subsequently
swim to the female cloacal orifice, using their undulating membrane.
second part of this study deals with research on the nature and localization
of the production sources of chemical signals. We have examined the cytological
structure and the development of the cloacal glands, which are good candidates
as the production sources of communication signals between conspecifics.
anguinus possesses additional tegumental cloacal glands, which are not
homologous with other glands described in salamanders. These glands occur
in both sexes, but show sexual dimorphism, being better developed in males.
E. asper possesses tegumental glands that, on the basis of the present
knowledge, must also be considered as forming an additional type. However,
there is no evidence that these glands are homologous with those of P.
data clearly show a preponderant influence of chemical communication on
social behaviour in P. anguinus, while this cue is less developed in E.
asper. Despite this difference, gregariousness is a common character of
both species. This characteristic is also found in some cave fishes, which
supports the hypothesis that gregariousness may be propitious to cave life.
According to some authors, attraction towards conspecifics increases the
chances of finding a mate and helps in the search of food."
observing the behaviour of captive specimens, Parzefall
(1962) have attempted to demonstrate that
males only show aggressive behaviour and territoriality for a very short
reproductive period. Normally the animals rest under stones in groups of
both sexes without any aggressive reaction. Also, during breeding activity,
males have a larger and more elongated swollen cloaca (urinogenital opening)
than the females. When a male becomes sexually active it starts to control
its conspecifics by contacts with the snout and allows only females in
the reproductive state to remain in the hiding place. All the females had
well-developed eggs visible in their oviducts. Intruders were attacked
by tail-beating, ramming and biting. It was also observed that males patrol
along territorial borders with oscillating tail movements. Such territories
may exist for only a few days and animals being attacked in such a territory
avoid it thereafter on the basis of a substrate-specific chemical signal.
This avoidance reaction also persists for only a few days.
report that adult Protei congregate in suitable areas such as cracks and
under rocks. The males establish a territory when breeding, which is furiously
defended against competing males. When a female enters such a territory,
the courtship commences. The male fans with his tail in the direction of
the female's head (possibly even secreting a female-attracting pheromone)
and touches the female's cloaca (the combined reproductive and urinogenital
opening) with his snout. The female then touches the male's cloaca with
her snout and then follows the male who walks 50-100 mm forward and deposits
a spermatophore (a small packet of sperm). The pair then moves forward
again until the female can take up the spermatophore with her cloaca. Courtship
may be repeated several times within a few hours. After leaving the male's
territory, the female establishes her own egg-laying territory.
anguinus anguinus (Laurenti 1768) in its egg development stage in a
optimum water temperature for this species is 7º -10º C. Females
normally lay up to 80 eggs, but curiously enough if the water is warm enough
(about 15º C) they can give birth to two larvae instead.
female has been observed undertaking egg-guarding and defending behaviour.
(1966b) again reports that under laboratory
conditions at a temperature of 11.9º C, eggs were not all laid at once
but over a period of 1 to 3 weeks. He noted that under his artificial conditions,
he obtained 10 egg-laying events producing batches varying from 20 to 60
eggs. The eggs were always laid on the undersides of large flat stones.
The parents remained close by thereafter, maintaining a circulation of
water around the eggs by the regular waving of their tails to prevent the
settling of mud on the sticky mucilage which envelops the eggs. He reports
that these eggs were from 8mm to 9mm in diameter, each surrounded by a
layer of mucilage, by which the egg adhered to the stone on which it was
that just as the egg-laying process in artificial conditions at a temperature
of 11.9º C was gradual, the hatching was also spread over several weeks.
He determined an estimated embryonic period of 111 days.
anguinus anguinus (Laurenti 1768) in its Larval Stage of development
in a vivarium.
Post-embryonic Development :-..At
hatching, the young Proteus retains an important reserve of yolk,
which appears as a whitish mass on the underside of the body. This is progressively
yolk and its resorption enabled Vandel et al to distinguish two
distinct stages in the post-embryonic development of
Durand and Bouillon, 1966.).
Stage is the first, when the animal
lives on the reserve of yolk. Vandel
reports that under his artificial conditions, this lasted for about an
average of 36 days.
reports that total duration of both the Embryonic and Larval stages was
on average about 5 months and that in the other group of Proteidae, Necturus,
which is a non-cavernicolous form, it is only 2½ months.
is a neotenic or “paedomorphic” salamander. It does not undergo metamorphosis
but permanently retains the physical characteristics of its larval stage
retention of the external gills and its long finned-tail into adulthood
are evidence of neoteny
Stage is the second, during which
it extracts its food from its surroundings. It is from the Juvenile
Stage onwards that Proteus begins
to lead an active life.
increase in size is very slow during this Stage with the growth curve showing
a strong deflection after the age of 2 to 3 years.
reports that the largest of the specimens reared in the Moulis Underground
Laboratory was only 200mm long and therefore, as Proteus does not
become sexually mature until it reaches a length of 240mm.,
seems likely that these cave salamanders do not reproduce until they are
at least 10 years old.
do not have a fixed number of vertebrae. Proteus anguinus anguinus
has 29–32 vertebrae.
have now appended images of old diagrams of
the anatomical structure of the
Proteus anguinus anguinus, drawn
by the Italian explorers
and P. Configliachi.and
published in "Monografia del Proteo anguino
di Laurenti", (1819).
make the information more widely accessible to our readers, we have drawn
the Explanations of the Plates from the English Language Translation as
published in the Edinburgh Philosophical Journal,
Vol. 5. (1821).
(left) as PLATE VI.
quote the following explanatory text of PLATE VI., with some modernizing
of Old English words.
All sizes quoted herein relate to the scaled drawings in the original publication.]
(Figs 1. and 2.)
of the Head from below, 8x greater than natural.
two branches of the Lower Jaw;
of the Temporal Bones to which they unite;
roof of the Palate;
three Branchial Arches of the right side;
the intermediate bones of the 1st and 2nd arches;
the 1st three Vertebrae;
the branches of the os hyoides.
Skeleton of the Proteus of its natural size.
three cartilages forming the Shoulder;
Digestive, Excretory and Reproductive Systems (Fig 3.)
lower half of the trunk of a Female Proteus laid open.
Alimentary Canal shortened and straightened from the action of ardent spirits:--
at its termination, it is slit up to show the common
focus of the
Ureters and Oviducts;
which two pins are inserted, the opening from the Urinary-Bladder is indicated
by a single pin.
the left ovarium, containing minute ova, and drawn back to
one side to display the Kidney underneath;
a portion of the Oviduct straightened by the action of the spirits;
the left Kidney;
the Ureter running along its margin and terminating with the Oviduct in
a portion of the left Air-bladder, in this instance remarkably enlarged;
the corresponding one of the right side was very small."
Central Nervous System (Fig 4.)
Cranium laid open to show the cerebral mass and certain nerves springing
the two hemispheres of the Cerebrum;
the medulla oblongata;
the right olfactory nerve;
the origin of the fifth pair of nerves;
the vestibule of the organ of hearing, laid open, in which the little sac
is seen, and the origin of the acoustic nerves;
the facial nerve;
the entrance of the carotid [artery] into the Cranium, from which springs
the opthalmic going to the eye (n);
the origin of the par vagum."
Head and Trunk (Fig 5.)
of the Head and Part of the Trunk.
external aperture of the Nostrils surrounded by Pores;
the doubling of the Inferior Lip, which is in part covered by the Superior;
the swelling or protuberance produced by the Heart."
(left) as PLATE VII.
quote the following explanatory text of PLATE VII., with some modernizing
of Old English words.
Digestive, Excretory and Reproductive Systems (Fig 1.)
Male Proteus laid open, to exhibit the relative size and position of the
Heart, with its pericardium, opened and turned back;
the Liver drawn aside, to show the viscera beneath it;
the Alimentary Canal;
the Testicle of the left side;
a part of the left Kidney;
the left Air-bladder, with its tube, opening into the conical cavity above;
Anus or Cloaca;
the sinus of the vena cava."
Heart and Air-bladder (Fig 2.)
Heart reversed and turned upward;
the short conical canal cut longitudinally, which communicates anteriorly
with the Glottis and posteriorly with the cavity from which the two tubes,
terminating in the Air-bladder, proceed."
Head (Fig 3.) :
of the Proteus viewed from below, 8x greater than natural, displaying
the circulating and respiratory systems.
arterious trunk springing from it;
the two primary trunks arising from the bulb, and again subdividing;
the first branch of the primary trunk, or artery corresponding to the common
carotid [artery], and which subdivides into two, one branch (f)
being continued to the first or exterior Gill, and the other (g)
proceeding to the muscles of the os hyoides;
the vein which carries back the florid blood from the Gill.
second branch of the primary trunk (d)
soon also subdivides, sending off the branch (i)
to the third Gill, and another (l)
to the middle Gill. To these two branchial arteries, the two veins (m-m)
which carry back florid blood, correspond.
principal trunk of this second branch, after receiving this florid blood,
sends off the artery (n),
which, descending along the air-tube, supplies the Air-bladder and generative
organs in each sex; it then curves upward, and from its curvature gives
off the vertebral artery (o),
which, after sending some twigs to the Occiput, enters the vertebral canal,
and descends along it; it also gives off another branch (p)
to the Temporal bone, and then making another curvature downwards, it becomes
a branch (q)
of the Aorta, which by uniting with its fellow of the opposite side, it
contributes to form. The Aorta (r) gives off the branchial arteries (s-s),
the mammary (u)
and the vessel (t)
going to the Stomach; the letter x
denotes a portion of the vena cava cut off."
Gills (Fig 4.) :
Leaflet of the Gill highly magnified,
the branchial artery (a),
conveying dark blood to the Gill, and the branchial vein (b),
returning florid blood to the Aorta."
is one of Rusconi & Configliachi's original anatomical
drawings, showing far more detail than the drawings reproduced in the English
Language Translated version.
AND INFECTION :
well as being susceptible to various infections, the adults also suffer
are aware that populations of certain European amphibians have succumbed
to a fungal virus. We are currently trying to obtain more information about
this and will publish the results of our search when completed. In August
2005., we have extracted the stomach contents of 2 animals, together with
body tissue from the tip of the tail of one animal for laboratory tests
for the presence of fungal viruses.
- Proteus retains a highly developed and endocrinologically active
Thyroid Gland system, producing thyroxine. It has been proven under laboratory
conditions that in Proteus and other cave salamanders, this is not
to help control the process of metamorphosis, unlike in other types of
salamanders. Therefore in Proteus, the thyroxine must have another use.
Information in the Public Domain from various sources :
Olm is listed as "Vulnerable" in the IUCN Red List of Threatened
Species because its area of occupancy is less than 2,000 km². Its
distribution is severely fragmented and there is a continuing decline in
the extent and quality of its habitat and in the number of mature individuals.
The Olm is thought to be in decline by the IUCN Red List of Threatened
is currently little information available on the abundance of this species.
However the IUCN Red List of Threatened species states that the Olm is
apparently most common in Slovenia and Croatia, although a decline has
been observed in the populations of Goriza (Italy) and Postojna (Slovenia).
Specifically, the number of individuals of the subspecies Proteus anguinus
parkelj is thought to be very low.
our own perspective in Bosnia & Hercegovina, we would suggest that
the status of Proteus anguinus anguinus should be set at because of the very
low number of extant viable hypogean ecosystems that are able to support
its existence in the
and because of the increasing threats to those that are still able to support
this animal and associated species.
AND CONSERVATION OF THE SPECIES,
of what the Society is doing :
long-term protection and conservation of the species can only be
achieved through the protection and conservation of its natural karst
species is greatly endangered within its natural habitats from over-collection
by so-called "cave scientists" and by the industrial chemical pollution
of karst groundwaters, together with anthropogenic changes in natural hydrographic
Society's Joint International Programme
Bosnia & Hercegovina is the only known project that is fully underway
(and has been for 10 years) and which has been specifically designed to
protect Proteus anguinus by understanding its behaviour and the
remaining natural habitats ... and then addressing those problems. The
30-year Programme, (about which this is the second of four dedicated Webpages),
is in 3 Phases. With only minimal voluntary-sector funding but enormous
quantities of voluntary-sector effort, the current
1. has been overwhelmingly successful
and has produced a great wealth of information about the behaviour of Proteus
and the characteristics and problems of its natural habitats across a whole
region within its geographical range.
have designed and implemented a successful strategy for identifying previously
unknown Proteus anguinus Habitat Locations across a whole region.
As such, we are able to preliminarily identify such locations before we
actually enter them for the first time to eventually confirm their status.
The same strategy also allows us to predict the location of once-viable
habitats that have now become degraded and non-viable.
work includes regular water-quality monitoring of the hypogean habitats
and of all those locations where it is no longer found. Population monitoring
and a species biometric programme are included. Vulnerability
assessments are made about each habitat location and Habitat Viability
studies are also undertaken.
Restoration and Habitat Protection schemes have been successfully
designed and implemented at various locations, restoring some to their
former "viable habitat" condition, whilst others are the subject of on-going
habitat locations of Proteus anguinus in Eastern Hercegovina vary
greatly in their hydrological functionality and other prevailing conditions.
We have found that Conservation Action Plans have to be designed
to be site-specific and that the concept of a "universal conservation model"
is inappropriate. Our Project has designed and implemented site-specific
Action Plans with great success.
a necessary adjunct to all of our practical work with Proteus anguinus,
we have identified critical issues that must be observed by all Project
Workers undertaking work in all parts of the Project. These have been realised
through the implementation of a Code of Ethics, Operational Protocols
& Procedures and Methodology, detailing what work can be undertaken
with Proteus anguinus and how the work must be conducted. A Prime
Directive has been included in this document.
Project recognizes the need to work with many sectors of the local population
and with its political representatives. As such, we are fully engaged with
all of them in support of our objectives. Public Education Programmes
at various times throughout the year support our connection with the local
population and "stakeholders".
are well placed to succeed in our final objectives of protecting this incredible
animal through the protection and conservation of its natural habitats
and in knowing how to restore the viability of many of its previous habitats,
which are currently degraded.
details about the Society's work on this Project can be found in the Proteus
Project Webpage 3., which is subject to continuous updating.
from studying the species in its natural habitat, we do not think it is
possible to use the system of "captive breeding" of the Proteus as a viable
contribution towards ensuring the survival of the species. This may be
appropriate for some amphibians but we are of the opinion that it is not
necessarily so for Proteus. We have learned that the natural variations
in the characteristics of some Proteus habitats differ greatly from others.
We are not even contemplating the idea yet of restocking habitat locations
by translocating some specimens from one location to another, because of
the natural variations in conditions that exist between individual habitats!
anguinus is indeed a critically endangered species. However, due care
must be undertaken by anyone or any organization who thinks that it is
a wise and practical idea to just "dive in" and to do "something or anything"
to help save this species.
really is not that easy. More harm than good will arise as a result of
such ill-considered "knee jerk" decisions. This is not an animal like any
other. This is not an amphibian like any other.
is a unique and highly adapted hypogean species, endemic to a comparatively
tiny area of our planet and which seems to have further adapted to prevailing
localised conditions within and across its geographical range.
AND CONSERVATION OF THE SPECIES (continued ....),
of the status of Proteus in the European Union's Habitats Directive :
anguinus is mentioned in the List of animal species covered
in EU Directive 92/43/EEC, Annexes II, IV and V.
species is a "priority species" of Annex II - "Species of Community
Interest whose Conservation Requires the Designation of Special Areas of
anguinus is not listed on CITES.
Red List :
Olm is listed as vulnerable because of its fragmented and limited distribution
and ever-decreasing population.
in Slovenia since 1949. 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, which continues to exist. In 1982 it
was placed on a list of rare and endangered species in Slovenia. This list
also had the effect of theoretically 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. Although
the Olm is included in a Slovenian red list of endangered species and notwithstanding
the aforementioned protection mechanisms, Slovene and collectors from other
countries such as Italy, France, the Czech Republic and Slovakia continue
to remove specimens for private collections or for illegal trading for
onward use in Asia or for "scientific study".
Biodiversity Information Facility (GBIF) :
for the Proteus anguinus species in this database are either mostly
useless or misleading.
AND CONSERVATION OF THE ENVIRONMENT & BIODIVERSITY,
Summary of what R. BiH has agreed do :
NATIONS DEVELOPMENT ASSISTANCE - FRAMEWORK FOR BOSNIA AND HERCEGOVINA 2010
UNDAF has been prepared by the United Nations Country Team in Bosnia and
Hercegovina in consultation with the Government of Bosnia and Hercegovina
and other partners, with the aim of
the lives of the people of BiH, and particularly the most vulnerable. This
was signed by Mr. Nikola Spirić in Sarajevo, Bosnia and Hercegovina
in March 2009 on behalf of the Council of Ministers of Bosnia & Hercegovina.
main goals have been identified that will set the direction and scope of
action of UN system development assistance in the next 5 years. One of
the end of 2014, BiH Government meets requirements of EU accession process
and multi-lateral environment agreements (MEA), adopts environment as a
cross-cutting issue for participatory
planning in all sectors and at all levels, strengthens environmental management
to protect natural and cultural resources and mitigate environmental threats."
the document on p.13., we note the statement : "While environmental
protection is emerging as a priority for the Government, there is a lack
of sufficient capacities, strong policy and a legal framework at the state-level."
both the Bošnjiak-Croat
Federation-BiH and the Bosnian-Serb RS-BiH Entity Governments have their
own separate Cultural, Historical and Nature Protection Institutions, none
exists at a Central State level for the entire Republic.
the case of F-BiH., they have a Culture and Sports Ministry, whilst in
RS-BiH., the responsibility for Cultural and Natural Heritage operates
within the Ministry for Education.
Summary of what the RS-BiH Government is doing :
November 2011., we are very pleased to be able to announce that the "Proteus
Project" has at last been able to engage with the RS-BiH Government's Nature
Protection authority within the Ministry for Education.
details about this exciting progress will be published on these webpages
in January 2012.