The hypogenic caves: a powerful tool for the study of seeps and their

Continental Shelf Research 22 (2002) 2373–2386
The hypogenic caves: a powerful tool for the study of seeps and
their environmental effects
Paolo Fortia,*, Sandro Galdenzib, Serban M. Sarbuc
a
Dipartimento di Sciencze della Terra e Ge, Istituto Italiano di Speleologia, Via Zamboni 67, I-40127 Bologna, Italy
b
Istituto Italiano di Speleologia, Sede di Frasassi, I-60040 Genga, Italy
c
Center for Ecological Research and Environmental Education, C.P. 57, Mangalia 7827, Romania
Received 1 February 1999; accepted 1 July 1999
Abstract
Research performed in caves has shown the existence of significant effects of gas seeps, especially CO2 and H2S,
within subterranean voids. Carbon dioxide causes important corrosive effects and creates characteristic morphologies
(e.g., bell-shaped domes, bubble’s trails), but is not involved in the deposition of specific cave minerals. On the other
hand, in carbonate environments, hydrogen sulfide when oxidized in the shallow sections of the aquifer generates
important corrosion effects and is also responsible for the deposition of specific minerals of which gypsum is the most
common.
Studies performed in the last few years have shown that H2S seeps in caves are associated with rich and diverse
biological communities, consisting of large numbers of endemic species. Stable isotope studies (carbon and nitrogen)
have demonstrated that these hypogean ecosystems are entirely based on in situ production of food by
chemoautotrophic microorganisms using energy resulting from the oxidation of H2S.
Although located only 20 m under the surface, Movile Cave does not receive meteoric waters due to a layer of
impermeable clays and loess that covers the Miocene limestone in which the cave is developed. In the Frasassi caves,
where certain amounts of meteoric water seep into the limestone, the subterranean ecosystems are still isolated from the
surface. As the deep sulfidic waters mix with the oxigenated meteoric waters, sulfuric acid limestone corrosion is
accelerated resulting in widespread deposition of gypsum onto the cave walls.
Both these caves have raised a lot of interest for biological investigations regarding the chemoautotrophically based
ecosystems, demonstrating the possibility of performing such studies in environments that are easily accessible and easy
to monitor compared to the deep-sea environments where the first gas seeps were discovered.
r 2002 Elsevier Science Ltd. All rights reserved.
Keywords: Karst; Hypogenic caves; Seeps; Biology; Chemoautotrophic communities
1. Introduction
*Corresponding author. Tel.: +39-051-2094547; fax: +39051-2094522.
E-mail address: [email protected] (P. Forti).
The scientific and economic interest of gas
seeping from marine sediments grew enormously
in the last few decades. Nevertheless, many of the
environmental aspects of these phenomena are not
0278-4343/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved.
PII: S 0 2 7 8 - 4 3 4 3 ( 0 2 ) 0 0 0 6 2 - 6
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P. Forti et al. / Continental Shelf Research 22 (2002) 2373–2386
well described, and most often rather unknown.
The peculiar environmental conditions on the
bottom of the sea make such research very
expensive and very difficult.
Certain karst environments, such as hypogenic
caves, can be used as natural laboratories where
such studies can be performed both easier and
cheaper. Moreover, some of these caves being
often completely isolated from the surface, ensure
that their environment is not affected by anthropogenic pollution and therefore processes taking
place inside these caves are controlled only by the
seeps.
The seep research that can be performed in
caves may be summarized as follows:
*
*
*
*
*
*
relationships with deep geological structures;
rising behaviour of the seeps;
chemical composition of the seeps;
effects on the host rock;
relationships between hydrogen sulfide,
methane, and chemoautotrophic bacteria; and
the associated ecosystems.
In the present paper, after a short characterization of hypogenic caves, the more common effects
resulting from seeps inside these cavities are
shortly described from morphological, mineralogical and biological points of view.
2. Hypogenic caves
The genesis and evolution of caves are usually
controlled by meteoric water seepage into karst
formations. The energy needed to dissolve the
limestone and to support the biological communities inhabiting the caves is entirely supplied from
the surface and carried underground by several
agents, the most important of which are water, air,
gravity and fauna (Fig. 1A).
Some caves, however, are formed by acidic
fluids ascending from the depth, in which cases,
the energy is supplied by the rising water and gases
(Fig. 1B). Such cavities are defined as hypogenic
because their evolution is controlled by fluids
coming from depth and not from the surface. Such
caves are known from different parts of the world
and they are believed to represent about 5–7%
(Forti, 1996) or 10% (Ford and Williams, 1989) of
all deep karst phenomena. Some hypogenic caves
are thermal (Bakalowich et al., 1987; Muller and
Survary, 1977; Forti, 1996; Galdenzi, 1997; Sarbu
and Lascu, 1997), but not all are related to hot
waters: for instance, their development can be
related to cold water (Galdenzi, 1990) or to deep
oil deposits, like the famous Carlsbad Caverns and
Lechuguilla Cave in the Guadalupe Mountains,
New Mexico (Hill, 1987), or the Las Brujas Cave,
in Argentina (Forti et al., 1993).
The geochemistry of the fluids in the hypogenic
caves is complex, reflecting the wide variation in
the origin of the rising waters (meteoric, connate,
juvenile, or, most often, a mixture of two or all
three of these). Therefore, the gases released by
seeps into the karst environment are different, the
most common of which, listed according to the
frequency of their occurrence, are:
*
*
*
*
CO2—carbon dioxide,
H2S—hydrogen sulfide,
Rn—radon,
CH4—methane.
Cave seeps associated with deep oil deposits are
usually characterized by high concentrations of
hydrogen sulfide and methane. Cavern environments allow for easy quantitative monitoring of
physico-chemical characteristics of seeps by normal laboratory apparatus (Fig. 2), while the same
analyses are very difficult and expensive on the
bottom of the sea. In this respect the deep karst
environment seems to be the ideal place for
statistical studies on the geochemistry of rising
gases and for monitoring their temporal evolution.
3. Morphological and mineralogical effects of seeps
Although hypogenic caves are developed in
different geological, morphological, and climatic
contexts, they always present some peculiar
morphologies and/or cave deposits. The effects
of seeps in the deep karst varies from cave to cave
depending on the type of host rock and the
temperature and composition of the released gases.
P. Forti et al. / Continental Shelf Research 22 (2002) 2373–2386
LIGHT
LIGHT
2375
WATER
WATER
EPIGEAN PHOTOLITHOAUTOTROPHIC PRODUCERS
ENERGY
TRANSFER
SOIL COMPARTMENT
Start of the decomposition
of organic matter by the
soil fauna and microbiota
EPIGEAN PHOTOLITHOAUTOTROPHIC PRODUCERS
Consumers
SOIL COMPARTMENT
Start of the decomposition
of organic matter by the
soil fauna and microbiota
migrations
Consumers
SUBTERRANEAN SUPERFICIAL ENVIRONMENT
Consumers
migrations
impervious
boundary
SUBTERRANEAN SUPERFICIAL ENVIRONMENT
Consumers
ENERGY
TRANSFERT
HYPOGENIC CAVE ENVIRONMENT
migrations
NORMAL CAVE ENVIRONMENT
Consumers
Consumers
cave evolution by
uplifting water and gases
CHEMOLITHOAUTOTROPHIC PRODUCERS
cave evolution by seepage
of meteoric water
WATER
(a)
GAS
ENERGY
TRANSFER
(b)
Fig. 1. Energy flow in a meteoric cave (A) and in a hypogenic cave (B) (after Sarbu, modified).
Carbon dioxide, being the most common gas
released by seeps in cavern environments, has a
great impact on the deep karst, especially in
carbonate rocks. The resulting morphologies are
similar to those produced by carbon dioxide
brought into the cave from the surface by the
seepage of meteoric waters and therefore they are
difficult, and sometimes impossible to detect.
Nevertheless, carbon dioxide from seeps may
cause the development of some peculiar forms
just along the paths of the seeps in the shallow
phreatic zone. All of these are generated by
enhanced condensation corrosion, which becomes
active when the gas bubbles come in contact with
the cave walls and ceiling. The most common of
these morphologies are: widespread corrosion
pockets, bubble’s trails (Chiesi and Forti, 1987;
Forti, 1996) (Fig. 3), and bell-shaped condensation
corrosion domes (Forti et al., 1993). The first two
forms develop on overhanging walls. Corrosion
pockets evolve when the CO2 bubbles follow
random directions, while bubble’s trails are the
result of concentrated ascent along well-defined
paths. Condensation domes evolve on ceilings,
where concavities act as traps for the carbon
dioxide bubbles, thus creating a gas chamber
where condensation corrosion causes the evolution
of rounded bell-shaped domes.
The presence of CO2 seeps in deep phreatic
carbonate environments cannot generate cave
deposits (i.e., speleothems). However, as the deep
water ascends towards the water table, deposition
of calcium carbonate (usually calcite) may occur as
a consequence of the progressive loss of dissolved
CO2 induced by the decrease in the hydrostatic
pressure. The resulting carbonate deposits vary in
the different sections of the cave and are controlled
by the degree of supersaturation of the rising
waters. The deepest deposits are aggregates of
large to very large disphenoid crystals which are
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Fig. 2. Movile Cave: the in situ apparatus used for measuring the physico-chemical parameters of seeps (photo Lascu).
Fig. 3. Frasassi Cave: a bubble trial (photo Forti).
P. Forti et al. / Continental Shelf Research 22 (2002) 2373–2386
characteristic for low to very low crystallization
rates (De Vivo et al., 1987). Closer to the water
table, the large macrocrystal aggregates are
gradually replaced by speleothems such as the
well-known ‘‘cave clouds’’ (Hill, 1987), while in the
epiphreatic zone, thick accumulation of sunken
‘‘cave rafts’’ are usual (Ford and Hill, 1988) and a
large variety of peculiar speleothems develop just
at the water–air interface (Hill and Forti, 1997).
In non-carbonate environments, the massive
release of CO2 may also cause morphogenetic
and mineralogenetic effects, but their extent is
much less than in carbonate rocks. Carbon dioxide
seeps cannot generate corrosional forms, but in
evaporitic environments, the presence of large
amounts of CO2 may determine the formation of
thick calcite deposits as those described from
gypsum caves (Forti and Rabbi, 1981).
The effects of methane seeps in carbonate and
non-carbonate environments are similar to those
described for CO2 seeps. Methane has no direct
interaction with the cave walls, but when it reaches
shallower sections of the aquifer, it is oxidized to
CO2 and H2O. The CO2 released from this
oxidation is responsible for the evolution of
morphologies and cave deposits, which do not
differ from those already described for CO2 seeps.
Radon does not react with any host rocks and
therefore no peculiar morphologies or cave deposits may be induced by its presence, even in massive
amounts.
In the cavern environment the hydrogen sulfide
seeps are, by far, the most important from both the
morpho-genetic and mineralo-genetic points of
view: in the majority of the hypogenic caves, the
single detectable effects induced by gas released
from seeps, are those caused by H2S (Forti, 1989).
The morphologies induced by this gas in carbonate
environments are similar to the ones induced by
CO2 seeps (corrosion pockets, condensation corrosion domes and bubble’s trials), but they occur
much more frequently, and their size is much
larger. The reason for this is that the oxidation of
H2S to H2SO4 (Eq. (1)), in the presence of oxygen
from dripping waters and from the cave atmosphere, induces two different corrosion mechanisms: the acid corrosion (Eq. (2)) is extremely
efficient (Forti, 1989) and, at the same time, causes
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the release of a large quantity of CO2, which is
responsible for an additional karst corrosion
reaction (Eq. (3)):
H2 S þ 2O2 -2Hþ þSO2
4 ;
ð1Þ
2Hþ þSO2
4 þCaCO3 þH2 O
-CaSO4 d2H2 O þ CO2 ;
ð2Þ
CO2 þCaCO3 þH2 O-Ca2þ þ2HCO
3:
ð3Þ
In the field of cave minerals, H2S seeps exhibit
most of their activity: the oxidation of the H2S to
H2SO4 (Eq. (1)) allows for the evolution of
strongly acidic conditions which are responsible
for the corrosion of the host rock and the
evolution of many secondary cave minerals.
In carbonate environments, gypsum is largely
predominant, representing more than 90% of the
total deposits induced by seeps. In hypogenic
limestone caves, the most common secondary
gypsum deposits related to seeps are the widespread thick phreatic deposits (Fig. 4). These are
formed close to the interface between reduced
(H2S-rich) rising water and the meteoric oxidized
water, or close to the contact with the cave
atmosphere (Fig. 5). Gypsum deposits are usually
white, have a microcrystalline structure, but
various characteristics and origins can be recognized (Buck et al., 1994). Gypsum is always
present where H2S actually seeps into limestone
karst (Hill and Forti, 1997) and often at least some
portions of the gypsum deposits survive long after
the emission of H2S ceases in that particular part
of the cave. Phreatic gypsum deposits are described from the Carlsbad Caverns (New Mexico,
USA), where they are considered subaqueous
replacement crusts on the cave walls or subaqueous sediments (Hill, 1987; Hill and Forti, 1997).
The most common gypsum deposits generated
by seeps activity are the crusts developed in vadose
environments through limestone replacement due
to H2S oxidation after atmospheric condensation
(Egemeier, 1981). Vadose gypsum crusts have been
observed in all the caves containing sulfidic waters
(Hill and Forti, 1997; Sarbu et al., 2002) and they
are widespread in the Frasassi caves. Some of the
large gypsum deposits found on the floor of the
Frasassi caves were considered to derive from
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P. Forti et al. / Continental Shelf Research 22 (2002) 2373–2386
Fig. 4. Frasassi Cave: a thick phreatic gypsum deposit (photo Galdenzi).
gravitational flow of vadose replacement gypsum
(Galdenzi, 1990).
It must be mentioned that, even though gypsum
is one of the most common cave minerals in many
meteoric caves (Hill and Forti, 1997), the gypsum
deposits described here are restricted to hypogenic
environments. In fact, phreatic gypsum deposits
are always absent in caves generated only by
infiltration of meteoric water because supersaturation with respect to gypsum is impossible under
phreatic conditions without the enhancing factor
(the oxidation of H2S) induced by seeps.
Vadose gypsum deposits caused by seeps are
morphologically similar to some of those produced
by meteoric seeping waters, but they may be easily
recognized due to their abundance and thickness
which may cause the complete filling of even large
cave passages (Forti et al., 1989).
Although restricted to less than 10% of the
total cave deposits induced by H2S-rich seeps, a
P. Forti et al. / Continental Shelf Research 22 (2002) 2373–2386
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Fig. 5. Model of the hydrogen sulfide reaction to form phreatic gypsum deposits in Carlsbad Caverns (after Hill, 1987, modified).
Hydrogen sulfide ascends along injection points and reacts with oxygen to form sulfuric acid. This in turn is neutralized by the
limestone far from the injection points and therefore horizontal rooms end abruptly. The sulfuric acid reaction does not occur below
the oxidizing zone and hence vertical passages are absent below large horizontal rooms. The successive lowering of the water table
leads to the development of new horizontal cave levels that may become connected with the upper older horizontal levels by spring
shafts and joint chimneys.
noticeable variety of other cave minerals develop
in practically all types of host rocks. Most of these
are sulfates, but silicates, oxides, hydroxides, etc.,
have also been reported (Hill and Forti, 1997;
Forti et al., 1989) and in many cases they may
represent the only evidence of past seep activity in
a given cave.
Finally, it is worth noting that the cavern
environment is highly conservative, being affected
by low to very low-energy flow compared to the
ocean environment, and therefore morphologies
and deposits may be maintained unperturbed
inside the caves long after their genetic factor
ceases its activity (Hill, 1987; Forti et al., 1989,
1993; Galdenzi and Menichetti, 1989, 1995;
Galdenzi, 1997), while on the bottom of the sea,
they are rapidly modified or destroyed by erosional processes or buried by thick sediments.
This allows the identification of seeps of the
past, even though the rising gas has ceased inside
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the cave thousands or hundreds of thousands of
years ago.
4. Biological effects of seeps
Besides morphological and mineralogical effects, gas seeps also induce profound biological
effects in cavern environments. Research performed in hypogenic caves in the last decade has
led to the discovery of peculiar complex ecosystems similar to those discovered on the bottom of
the ocean, around gas seeps (Ballard, 1977;
Tunnicliffe, 1992).
Hydrogen sulfide and methane are the only
seepage gases responsible for inducing biological
effects in caves, while radon and carbon dioxide do
not induce any biological effects. For biological
studies, the most interesting hypogenic caves are
those which still contain sulfide-rich and/or
methane-rich waters. When the emission of gases
ceases, the cave ecosystems are rapidly depleted of
their trophic support and they soon disappear.
Literature on cave communities based on gas seeps
are still scarce because only very few biological
studies have so far been performed in hypogenic
caves (Sarbu et al., 1996, 2002; Southward et al.,
1996).
The presence of reduced chemical compounds
such as hydrogen sulfide and methane in a cave
results in the presence of a redox interface between
these compounds and oxygen from the cave atmosphere and from oxygen-rich waters. Chemoautotrophic microorganisms can live at this interface
deriving energy from the oxidation of the reduced
chemical compounds. Rich microbial communities
use this energy to produce organic matter in situ,
and this can represent the food base for rich and
abundant communities of invertebrates that inhabit
the deep recesses of hypogenic caves. Being able to
survive without food input from the surface, these
cave communities may thrive underground in total
isolation for very long periods of time. Animal
populations trapped in such caves, having little or
no contact with their surface relatives, often tend to
evolve into new, endemic species.
Compared to deep-sea communities thriving
around deep-sea seeps, the living communities
inhabiting hypogenic caves appear to be much
younger. A total number of about 40 new species
have so far been described from hypogenic caves,
as opposed to the over 300 new species living
around deep-sea seeps. Most of the new taxa
described from hypogenic caves represent new
species and only few belong to new genera,
compared to the many new families and even
new orders described from deep-sea seeps. So far,
no cave organisms have been shown to contain
endosymbiotic chemoautotrophic microorganisms—one of the characteristics of the deep-sea
fauna associated with gas seeps. The Frasassi caves
(Italy) and Movile Cave (Romania) are the best
studied hypogenic caves and both contain extremely rich and specialized ecosystems.
5. Geological setting of Frasassi and Movile caves
The Frasassi caves are developed in the walls of
the Sentino river gorge in Central Italy and consist
of a total of over 20 km of cave passages located at
altitudes between 200 and 360 m (Fig. 6). The
caves are developed in at least four main
horizontal levels, often overlapping. The two lower
levels, ranging between altitudes of 200 and 300 m,
were developed during the Middle–Upper Pleistocene. Taddeucci et al. (1992) dated carbonate
speleothemes from these passages showing stalagmite ages of up to 200,000 years. The development
of these cave levels can be related to the deposition
of the surface alluvial gravel terraces in the Sentino
river valley (Bocchini and Coltorti, 1990).
The lower levels, ranging between altitudes of
200 and 300 m, were developed in morphological
and hydrogeological settings similar to the present,
as shown by the similarity between their morphology and the morphology of presently forming
caves. The upper levels located at altitudes of
300–500 m exhibit partially different characteristics and their development in different hydrogeological settings has been hypothesized. Each karst
level shows a complex pattern, strongly influenced
by faults and by the hydrogeological settings.
Dendritic networks of passages with tributaries
draining into a main stream are absent in the
Frasassi caves. Instead, the size and the general
P. Forti et al. / Continental Shelf Research 22 (2002) 2373–2386
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Fig. 6. Tridimensional sketch for the Frasassi Cave system: (A) Buco Cattivo cave, (B) Frasassi Cave; (1) elevation curves, (2) main
gypsum deposits.
morphology of the cave passages change without a
clear rule. The caves exhibit a typical ramifying
pattern, which is considered to be typical for
hypogenic caves (Palmer, 1991).
Typical phreatic features are widespread
throughout the cave; phreatic tubes (1–10 m in
diameter) are present in many parts of the cave;
they are often anastomotic, forming complex
mazes. Other large rooms show wide, rounded
ceilings, while their floor consists of flat, erosional
rock surfaces. Shafts and crevices in the floor of
the passages indicate the original sources of H2Srich waters that formed the cave. Cupolas of
different sizes are present on the walls and ceilings
of the cave, both in the small passages and in the
largest rooms. They could have originated both in
phreatic and in the vadose zones as a result of
condensation corrosion. Silt and clay fills of
residual origin are wide spread in the cave
(Bertolani et al., 1977), while allochthonous
alluvial gravels are absent, except for the passages
located very close to the gorge, affected by
occasional river floods.
The watertable can be reached in the lowest cave
passages; the phreatic waters are cold (B131C)
and are enriched in sodium and chloride ions and
secondarily in sulfur ions (i.e., sulfate and sulfide).
Sulfide can reach concentrations of up to
0.4 mmol/l in the mineralized aquifer (Sighinolfi,
1990; Tazioli et al., 1990). Their chemical characteristics are the consequence of the presence of a
thick Triassic anhydrite formation which underlies
the limestone and is encountered by the phreatic
waters while they ascend to the surface. Stable
isotope ratio data (Tazioli et al., 1990) also suggest
a meteoric origin for the phreatic waters, with a
recharge area located at altitudes of 600–1000 m,
and a residence time in the aquifer of a few years.
Changes in the conductivity and temperature of
water in the sulfidic stream in the Ramo Sulfureo
section of Grotta del Fiume (Fig. 7) clearly show
the influence of the seepage recharge on the sulfidic
aquifer: a fast recharge of fresh water, deriving
from surface precipitations, dilutes the sulfuric
mineralized water (Galdenzi et al., 1998).
In the Frasassi area the oxidation of H2S is
considered the main cave-forming process since
the beginning (Galdenzi, 1990); it occurred mainly
in the upper phreatic zone, and was just favored by
the mixing of the sulfidic water with the infiltrating
oxygen-rich meteoric water. This process is still
active, and occurs in the proximity of the watertable, both in the upper phreatic zone and in
vadose conditions. In the phreatic zone, gypsum is
transported away in solution by the groundwater,
while above the watertable, gypsum forms white,
massive, finely grained replacement crusts on the
cave walls and ceilings. The present rate of sulfuric
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P. Forti et al. / Continental Shelf Research 22 (2002) 2373–2386
Fig. 7. Hourly records of conductivity and temperature of the water in a sulfidic stream inside the Frasassi caves, compared with the
surface precipitation (April 1996–January 1997).
acid speleogenesis was determined with standard
limestone tablets exposed to H2S in the deep
sulfidic sections of the Grotta del Fiume (Galdenzi
et al., 1997). The weight loss reached values of up
to 20 mg/cm2/year, both in the phreatic and in the
vadose zones.
Gypsum deposition may have been more intense
during some periods of the cave’s history, as
shown by the presence of very abundant old
gypsum replacement crusts, as well as white, finely
grained, vast floor deposits of gypsum (over
1000 m3) in the upper cave levels (Fig. 4) (Galdenzi, 1990).
Movile Cave is located in south-eastern Romania, close to the Black Sea shore. It is developed in
Miocene limestones (12.5 MYA) covered by a
thick impermeable layer of loess that confines the
karst aquifer, stopping any infiltration of meteoric
water (Sarbu, 2000). During the cave history,
however, some periods of fresh water flow inside
the cave were documented (Engel et al., 1997). The
cave’s total length is 240 m and it consists of small
size passages. The upper cave level is dry, while the
lower level is partially flooded with thermal sulfidic
waters. Several air-bells are present in the lower
cave level. At present Movile Cave has no natural
entrance and it was discovered in 1986 when an
artificial shaft intercepted a natural cave passage at
a depth of 20 m under the surface of the ground.
The absence of radioactive artificial nuclides (e.g.,
137
Cs) from the Chernobyl accident in Movile
Cave shows that the deep karst is well isolated
from the surface.
Water flow inside the Movile karst system is the
result of the ascent of deep waters, characterized
by a low thermalism (about 251C). The total
mineralization of the water is of about 1 g/l, it
contains high amounts of hydrogen sulfide
(0.3 mmol/l) and methane (0.3 mmol/l), while
dissolved oxygen, nitrates, and sulfates are absent.
These waters originate from the Danube (over
100 km to the West) and their mean residence time
in the karst aquifer exceeds 25,000 years. Their
flow rate is extremely low and their physicochemical properties are not affected by seasonal
climatic changes. Gas release (H2S and CH4)
within the cave atmosphere allows the bacterialcontrolled oxidation of H2S to H2SO4 with the
consequent deposition of gypsum on the cave
walls. The cave atmosphere is depleted in oxygen
and rich in CO2 and CH4 (Table 1) (Sarbu, 2000).
Sarbu and Lascu (1997) have shown that
condensation corrosion is currently affecting the
limestone walls in the upper sections of Movile
P. Forti et al. / Continental Shelf Research 22 (2002) 2373–2386
Table 1
Chemical composition of the atmosphere in Movile Cave
Lake room
Air-bells
O2 (%)
CO2 (%)
CH4 (%)
19
7–10
1.5
3.5
0
1
Cave. This process is favored by the high
concentration of CO2 in the cave’s atmosphere
and by the temperature differences between the
warm mineralized water in the lower sections of
the cave and the colder walls in the upper cave
passages. Sulfuric acid speleogenesis takes place in
the vicinity of the sulfidic water in Movile Cave
(Sarbu, 2000). The limestone walls are covered by
gypsum replacement crusts. The speleogenetic
evolution caused by sulfuric acid is far slower in
Movile Cave compared to the Frasassi caves where
both the water flow and the gas exchange rates are
higher.
6. Living communities in the Movile and Frasassi
caves
A redox interface is present in the lower,
partially flooded sections of the Frasassi caves
and of the Movile Cave, between the hydrogen
sulfide and methane in the water and the oxygen in
the atmosphere. Chemoautotrophic microorganisms thrive along this interface using chemical
energy that results from the oxidation of H2S and
CH4. Sulfur oxidizing microorganisms (e.g., Thiobacillus sp., Beggiatoa sp., Thiotrix sp.) were
identified in both caves. They form microbial mats
covering the water surface, the sediments, and the
cave walls (Sarbu, 2000). Incubations with radioactively labeled bicarbonate have shown that
carbon is being fixed at the redox interface. The
presence and activity of ribulose-bis-phosphate
carboxylase/oxygenase (RuBisCO) also support
the hypothesis that food is being produced in situ
within the cave system. In the process of chemosynthesis, sulfur- and methane-oxidizing bacteria
produce organic matter in situ providing a rich
source of food for the rest of the species inhabiting
the caves. Stable isotope investigations using
2383
carbon and nitrogen isotopes provided conclusive
evidence that the cave ecosystems are indeed
chemoautotrophically based (Sarbu et al., 1996).
In Movile Cave as well as in the Frasassi caves, the
chemoautotrophically produced food is isotopically lighter both with respect to carbon and
nitrogen, compared to the photoautotrophic food
produced by green plants at the surface. This is
evident of the fact that the majority of the food
base of the ecosystem is produced within the cave
and that insignifican amount of food is brought in
from the surface.
Compared to cave ecosystems that depend
entirely on allochthonous food of photosynthetic
origin, chemoautotrophically based cave ecosystems tend to be both rich and abundant as a
consequence of the rich and constant autochthonous food supply. Cave communities live only in
the proximity of the redox interface, while the
upper dry non-sulfidic cave passages are usually
completely devoid of fauna. Although in both
caves, the distance between the surface and the
sulfidic cave passages is very small (tens to a few
hundreds of meters), the gene flow between surface
and cave populations is very small or absent. This
genetic isolation between surface and cave populations sets the premises for the formation of new
species in these caves.
The invertebrate communities inhabiting the
deep sulfidic sections of both Movile and the
Frasassi caves consists of numerous endemic
species. Thirty-three new species have been identified in Movile Cave (Tables 2 and 3) and seven
new species have been identified so far in the
Frasassi caves (Sarbu et al., 2002) (Table 4). This is
a consequence of a long history of underground
evolution in complete isolation from the surface.
7. Final remarks
Although only a few hypogenic caves have been
studied so far and most of these studies are in their
early stages, they show the importance of these
environments for the investigation of the effects of
gas seeps from the microbiological, ecological,
speleogenetic, and mineralogenetic point of view.
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P. Forti et al. / Continental Shelf Research 22 (2002) 2373–2386
Table 2
Terrestrial cave-limited species, endemic to the Movile Cave
groundwater ecosystem
Table 3
Aquatic cave-limited species, endemic to the Movile Cave
groundwater ecosystem
Crustacea, Isopoda, Trichoniscidae
Caucasonethes n.sp.
Haplophtalmus n.sp.
Crustacea, Isopoda, Trachelipodidae
Trachelipus troglobius
Crustacea, Isopoda, Armadillidiidae
Armadillidium tabacarui
Arachnida, Pseudoscorpiones, Chthoniidae
Chthonius monicae
Arachnida, Pseudoscorpiones, Neobisiidae
Roncus dragobete
Roncus ciobanmos
Arachnida, Araneae, Theridiidae
Marianana mihaili
Arachnida, Araneae, Linyphiidae
Lepthyphantes constantinescui
Arachnida, Araneae, Clubionidae
Agraecina cristiai
Arachnida, Araneae, Nesticidae
Nesticus n.sp.
Arachnida, Araneae, Hahniidae
Hahnia caeca
Arachnida, Acarina, Nicoletiellidae
Labidostoma motasi
Diplopoda, Julida, Julidae
Archiboreoiulus n.sp.
Insecta, Collembola, Onychiuridae
Onychiurus movilae
Insecta, Collembola, Cyphoderidae
Onchopodura vioreli
Insecta, Diplura, Campodeidae
Plusiocampa isterina
Plusiocampa euxina
Insecta, Coleoptera, Staphylinidae
Medon dobrogicus
Insecta, Coleoptera, Pselaphidae
Tychobythinus n.sp.
Decumarellus sarbui
Insecta, Coleoptera, Clivinidae
Clivina subterranea
Platyhelminthes, Turbellaria, Dendrocoelidae
Dendrocoelum n.sp.
Aschelminthes, Nematoda, Rhabditidae
Protorhabditis n.sp.
Aschelminthes, Nematoda, Panagrolaimidae
Panagrolaimus n.sp.
Aschelminthes, Nematoda, Leptolaimidae
Chronogaster troglodytes
Annelida, Hyrudinea, Haemopidae
Haemopis caeca
Mollusca, Gastropoda, Moitessieriidae
Heleobia dobrogica
Crustacea, Ostracoda, Cyprididae
Pseudocandona sp. cfr. eremita
Crustacea, Copepoda, Cyclopidae
Eucyclops subterraneus scythicus
Crustacea, Amphipoda, Gammaridae
Pontoniphargus racovitzai
Crustacea, Isopoda, Asellidae
Asellus aquaticus infernus
Insecta, Heteroptera, Nepidae
Nepa anophthalma
Speleogenetic research shows that although the
majority of the karst voids result from the
interaction between meteoric seeping waters and
the carbonate bedrock, gas seeps may also
generate dissolution caves. These results led to
the reconsideration of the speleogenetic evolution
of some large, presently inactive karst systems, the
genesis of which was difficult to explain by the
normal karst cycle.
Table 4
List of species of invertebrates endemic to the sulfidic sections
of Grotte di Frasassi
Annelida, Clitellata, Oligochaeta, Lumbriculidae
Rhynchelmis n. sp.
Crustacea, Amphipoda, Gammaridae
Niphargus ictus
Arachnida, Pseudoscorpiones, Chthoniidae
Chthonius n. sp.
Arachnida, Araneae, Linyphiidae
Porrhomma n. sp.
Lepthyphantes n. sp.
Insecta, Collembola, Onichiuridae
Deuteraphorura n. sp.
Insecta, Coleoptera, Carabidae
Duvalius bensai lombardi
The existence of several new cave minerals
related to seeps is extremely important because
they are normally generated by low enthalpy,
biologically induced, reactions: therefore, the
possibility to study in situ the evolution of such
deposits will allow for a better understanding of
these processes. The caves in which seeps are still
P. Forti et al. / Continental Shelf Research 22 (2002) 2373–2386
active are certainly the best and easiest accessible
places to perform such studies.
But perhaps the most important interest of the
hypogenic caves is represented by the chemoautotrophically based ecosystems present in hypogenic
caves that contain active redox interfaces. Rich
and abundant communities are present in very
different karst cavities such as Movile Cave and in
the Frasassi caves.
The existence of ecosystems based upon chemosyntesis in very different environmental conditions
suggests that the likelihood of finding living
communities underground is far higher and more
diversified than supposed and observed until
recently.
Future research must try to identify new
hypogenic caves in different areas of the world
and to improve the understanding of the different
effects of seeps in a given cave. This will show that
hypogenic caves can be used as natural laboratories in which seeps may be studied from all
points of view, easier and cheaper than the
traditional one.
Acknowledgements
The authors want to thank the members of
GESS Team for the help with the work and the
Consozio Frasassi, the VolksWagen Foundation,
the National Geographic Society, the National
Science Foundation, the Romanian Academy of
Sciences for financial support.
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