Download Despite its inhospitable appearance and lack of

Fauna
FABIO STOCH
Despite its inhospitable appearance and
lack of any sign of life at first sight,
groundwater is populated by large
numbers of animal species of various
taxa. These animals are generally very
small, even tiny (between three-tenths
of a millimetre to one centimetre). Only a
few exceed one centimetre, and even
fewer are quite big, like the underground
Larva of stygoxene chironomid
prawns of the genus Typhlocaris or the
olm (Proteus anguinus).
● Stygoxenes. Not all organisms found in groundwater are exclusive to it: in
fact, many of them are typical of surface environments and, through either
active or passive dispersion, accidentally penetrate underground. They are
therefore occasional guests in this habitat, to which they are generally carried
by water percolating from the surface. This situation is very frequent in surface
and underground karstic aquifers, with infiltration passages which are very
efficient (sinkholes) or slower (like micro- and macro-fissures in limestone).
The accidental guests occurring in groundwater are called stygoxenes. They
do not have adaptations enabling them to survive in the harsh underground
environment, where food supply is more restricted than in their habitat of
origin. However, in particular conditions - for example if the aquifer is
organically polluted - stygoxenes find optimal conditions for their survival and
may even reproduce in hypogean (underground) habitats. Their populations
may be quite large and compete with local ones, to the point of replacing them
completely. They may also play important roles as prey or predators of
underground species.
● Stygophiles. Stygophiles are organisms that exhibit some adaptation to life
in groundwater environments, and may reproduce in both surface and
underground waters. Stygophiles live within surface water-groundwater
interfaces like springs, humid soil, wood litter and moss. These habitats share
several characteristics with the underground environment, in particular
darkness and limited living space. This is why stygophiles often have preMonolistra schottlaenderi (top) and Monolistra racovitzai (crustacean isopods, 7x)
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adaptive features to life underground, which enable them to survive in
transitional environments: they are often partially or totally depigmented and
have reduced or totally absent visual organs. From the evolutionary viewpoint,
since groundwater is a secondary colonisation environment, the species now
found exclusively here are thought to have been stygophiles in the past. But
the contrary cannot be ruled out - i.e., that all past stygophiles are now
exclusive groundwater dwellers. Evolutionary destiny depends on the
opportunities which single stygophilic species had of colonising groundwater,
surviving and successfully reproducing.
Stygophiles which regularly frequent the subterranean environment where they
can reproduce, but which do not have marked adaptive characteristics, are
called substygophiles. They include, for instance, some aquatic benthic insects
found in watercourses, where they may spend the early phases of their
development in the fluvial hyporheic environment. This is a winning adaptive
strategy as regards avoiding predators, but their life-cycle is always completed
in shallow waters, and adults often inhabit the subaerial habitat. This is true of
many ephemeropterans, plecopterans and dipterans, mainly chironomids.
Conversely, those stygophiles which show not only marked pre-adaptations
but also an elective preference for the subterranean environment, where they
are regular guests, are called eustygophiles. This is the case of many molluscs
and crustaceans.
● Stygobionts. Animal species closely associated with underground
environments, on which they depend for completing their life-cycle, are called
stygobionts. They often have marked adaptations to underground life like
depigmentation, anophthalmy (absence of eyes), well-developed sensory
organs, and a reduced fecundity rate (described in the chapter on the
ecological aspects of groundwater). These adaptations are partially shared by
terrestrial troglobionts (cave-dwelling species) and by those living in soil
(endogean species). Stygobionts may be ubiquitous and live in all types of
aquifers, and sometimes in marginal waters (for instance, under dead leaves in
humid forests), or they may be associated with specific habitats, like
phreatobionts, which live exclusively in saturated alluvial aquifers, and karstic
stygobionts, which are limited to aquifers in limestone and evaporites.
A clear distinction between these ecological categories is difficult to make,
and there are many intermediate levels. In some taxa, of which all species
appear to be pre-adapted to life in humid soil and groundwater, like
nematodes and some families of oligochaetes, it is impossible to divide them
according to morphology, and their preference for underground habitats is
evident from the frequency with which they are found there.
This chapter on groundwater fauna describes exclusive dwellers, i.e.,
stygobionts. We will discover a fascinating multitude of dark-loving organisms,
with sometimes bizarre morphological adaptations.
Paracyclops imminutus (stygophyle)
Niphargus steueri (stygobiont)
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Methods for sampling and analysing groundwater fauna
Groundwater habitats are difficult to
reach, and researchers have had to
come up with ingenious methods for
sampling and analysing underground
fauna which, according to the depth and
accessibility of aquifers, are sometimes
expensive and so complex that only
specialised research institutes can carry
them out.
In karstic waters, traditional sampling
methods include:
● continuous filtering of trickling water
funnelled into containers with filters
which are periodically emptied;
● collection of percolating water in
gours and micro-gours, by means of
rubber pumps or syringes;
filtering of concretion water with
plankton nets (60-100-µm mesh) which
are emptied with rubber piping;
● direct filtering of water from large
pools with plankton nets with handles;
in streams and small watercourses:
after coarse debris has been shaken out,
water is filtered through plankton nets
(with semi-circular openings 20-25 cm in
diameter);
● direct collection of large organisms
with aquarium nets and tweezers;
● in order to collect large predatory
crustaceans (1), traps containing meat or
tid-bits of food can be placed in suitable
positions in open cans (to avoid the
death of animals trapped inside, if the
trap itself is lost);
● placing artificial substrates (twisted
nylon netting compressed in tubes, or
tubes filled with locally collected washed
sediment) which are periodically emptied
in order to analyse the colonisation of
various types of substrates.
Collecting specimens from wells or
boreholes in alluvial soils may be carried
out with:
●
Fabio Stoch
modified plankton nets (Cvetkov nets)
with valves to prevent material from
escaping when the nets are quickly lifted
and replaced on the bottom of the well
to agitate the sediments (2);
● various types of pumps (peristaltic,
rotor, compressed-air), according to
water-table depth (rotor pumps of
greater power unfortunately easily
destroy material).
Lastly, in flooding watercourses where
collection is concentrated in upwelling or
outwelling stretches (see chapter on
ecology), two methods are used:
● Karaman-Chappuis method: a hole is
dug along the shore of a watercourse,
and the water permeating from nearby
sediments is collected and filtered
through a plankton net;
● Bou-Rouch method: a hand-pump (3)
is used to remove interstitial water from
the bed of a watercourse, by means of a
●
perforated tube inserted deeply into the
sediments (for a detailed description of
this method, see Teaching Suggestions).
Research teams with the most recent
equipment can use drills to place
piezometers at varying depths, from
which groundwater is extracted with
pumps and filtered through plankton
nets.
Other, quite expensive methods, like
freeze-coring, use liquid nitrogen to
freeze sediment cores collected from
boreholes and subsequently examined
in the laboratory.
More advanced research methods
involve inserting transparent perspex
piezometers with optical-fibre videocameras into the soil or sediment in the
river bed. In this way, researchers can
analyse large organisms in their natural
environment without disturbing the
underground community.
3
2
1
Filtering trickling water with a plankton net
Equipment for sample collection
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■ Poriferans
Among all stygobionts, sponges are certainly the least frequent and most
primitive. These essentially marine organisms (there are few freshwater
species belonging to the spongillid family) frequently colonise coastal caves
shrouded in partial darkness. There is, however, at least one exception to this
rule: Higginsia ciccaresei, a sponge which has recently been collected by
scuba divers exploring the Zinzulusa Grotto in the Salento (Apulia). The
species is endemic to the cave, and was found at a distance of 250 m from its
entrance, at a depth of 12 m, in total darkness. The morphological
characteristics of this species, like its depigmentation, have led researchers to
consider it a stygobiont.
■ Platyhelminthes
Flatworms are a primitive phylum of
free-living or parasitic organisms.
Stygobiont planarian worms are
generally depigmented, eyeless, with
slow reproductive cycles and high
numbers of chromosomes.
In Italy, although very little is known
about these organisms living in
phreatic environments, which are
certainly inhabited by many minute
Atrioplanaria morisii
creatures (micro-turbellarians), some
species living in karstic waters are well
documented. Dendrocoelum collinii lives in pre-Alpine caves and in France,
and D. italicum in Lombard caves, although the taxonomic position of Italian
populations of both species requires revision. The genus Atrioplanaria is found
in caves in Sardinia, central-southern Italy (A. racovitzai) and southern
Piedmont (A. morisii); Polycelis benazzii lives in Ligurian caves. The taxonomy
of these genera is uncertain, due to the fact that it requires examination of
living specimens and the use of complex histological and karyological
methods. This is why these animals are seldom included in lists of fauna.
However, being predators, their trophic role in underground ecosystems may
be of local importance.
The taxon of temnocephalid flatworms is of uncertain position. These
ectoparasitic species sometimes abound on the gills of crustaceans like
stygobiont amphipods and decapods, whose haemolymph they suck. Very
small (2 mm maximum), these animals have tentacles and adhesive discs with
which they attach themselves to their hosts. In Italy, only three genera have
been found so far (Bubalocerus, Scutariella, Troglocaridicola); they are
parasitic on stygobiont shrimps of the genus Troglocaris which live in
saturated karstic waters in the Karst areas of Trieste and Gorizia.
■ Molluscs
All Italian stygobiont molluscs belong
to the gastropod class, in particular to
the hydrobioidean superfamily (spring
snails). Although they are common in
Italian groundwater, with about 70
species described, and are found in all
types of habitats - except for the
vadose zone of karstic aquifers - spring
snails are still little known from the
taxonomic viewpoint. This is because
many species are only known by their
Hadziella ephippiostoma
shells, which are found in springs and
hyporheic water, suggesting that the elective habitat of these populations is the
deep, almost inaccessible underground environment. Many empty shells are
found in river sediments, and therefore their unknown underground habitat
may in fact be very far from where they were actually found. This is why their
genera and species described in the past need to be revised.
The shells of spring snails have various shapes. They are generally towershaped, conical and cylindrical, often truncated. Some genera have disc- and
spiral-shaped shells. Stygobiont species of spring snails are usually very small
(for example, the adults of the genus Hauffenia have a diameter of 2 mm and
are only 0.7 mm high). The opening of the shell is generally large and round,
closed with a thin, horny, egg-shaped lid, the operculum, which protects the
soft tissues of these animals. They move by means of a complex set of
muscles, the foot, which flattens ventrally and adheres to the substrate
allowing the snails to crawl. Stygobiont spring snails feed on micro-particles of
organic matter, encrusting micro-organisms and bacterial biofilms, which are
scraped and ground by their radula, an organ bearing several rows of minute
teeth. Except for a few species living in brackish water, most Italian spring
snails live in freshwater and are crenobionts (spring-loving) or stygobionts.
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Crenobiont species (genera Bythinella and Graziana) may enter groundwater
bodies and burrow into interstices, probably in search of food, and therefore
behave as stygophiles. A large number of endemic species of the genera
Bythiospeum, Iglica, Istriana, Hadziella, Paladilhiopsis and Phreatica are
strictly stygobiont, and live deep within karstic and alluvial underground
networks in northern Italy. Some species, living in Alpine-Dinaric areas, are
exclusive to the eastern Pre-Alps and are often strict endemics (like
Paladilhiopsis robiciana, Phreatica bolei, Hauffenia tellinii and Belgrandia
stochi). The area with the fewest species is the Piedmont Alps, with some
endemic species of the genera Alzoniella, Iglica and Pseudavenionia. The
Apennines host a small number of local endemics of the genera Pezzolia,
Alzoniella, Pauluccinella, Orientalina, Fissuria and Islamia. Exclusive inhabitants
of Sardinia are the genera Sardhoratia and Sardopaladilhia. Sicily hosts only
one crenobiont species, Islamia cianensis. Thermal waters contain particular
species of Bythinella and Belgrandia.
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■ Polychaetes
Shells of gastropods Iglica vobarnensis, Paladilhiopsis virei and Hauffenia subpiscinalis (from top to
bottom, ca. 30x)
Polychaete worms are generally sea animals, and only a few species colonise
anchialine coastal waters (land-locked bodies of water with a subterranean
connection to the sea), and even fewer species are adapted to underground
freshwater. Among them are two stygobiont species of great biogeographical
interest.
The nerillid Troglochaetus beranecki is an ancient thalassoid species (that is,
one with marine affinities) originating from members of psammon in Tertiary
epicontinental seas, from which it invaded underground freshwater. The
characteristic of this species is its vast distribution area. In Europe,
Troglochaetus beranecki is found in large rivers (Rhone, Garonne, Rhine,
Weser, Danube, Oder, Elbe), in Finland and in Alpine streams. It has also
been found in interstices in river beds of Colorado and Montana (up to 3050
m), although further molecular analyses are required to establish whether all
these populations are really conspecific. Fewer numbers are found in caves
of Switzerland, Germany, Poland, Hungary and Romania. In Italy, the species
has recently been found in interstitial environments (Trentino) and in caves
(Lessini Hills and Carnic Pre-Alps). This distribution is very wide, and
includes ice-covered areas where underground fauna is minimal if not totally
absent, and the rare stygobiont organisms have a remarkable capacity for
adaptation, which enabled them to colonise these areas in post-glacial
periods.
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Alkaline waters in karstic caves in Gorizia and Trieste host the second Italian
stygobiont polichaete, Marifugia cavatica. It belongs to the serpulids, which
are marine polychaete worms living in limestone tubules. Marifugia cavatica,
probably a micro-filterer, forms dense colonies that occasionally carpet
extensive areas of walls of underground streams with tubules up to 1 cm
long. The Marifugia formation is a little-known microhabitat rich in microfauna (protozoans, gastropods, oligochaetes, copepods, isopods and
amphipods) that populates, like the colonies of marine serpulids, the complex
mosaic of spaces between tubules. The species lives in the Dinaric region as
far as Albania, together with other species of ancient marine origin, like
isopods of the genus Sphaeromides and amphipods of the genus Hadzia, of
probable Tertiary origin.
Oligochaetes are freshwater and marine terrestrial annelids whose bodies are
made up of segments (metameres) without appendages, with rows of
transversal, movable bristles (setae). The shape and distribution of the setae
play an important role in the taxonomy of this group. Earthworms are usually
detrivorous and microphagous, and colonise microhabitats rich in organic
matter. In Italian groundwater, the most common are the lumbriculid and
tubificid families, together with the aquatic and semi-aquatic species of
enchytraeids.
The identity and similarity of groundwater oligochaetes have only recently been
partially established, and research is beginning. The main problem in defining
an oligochaete as stygobiont lies in the fact that many surface species (living in
sediments of surface water and sometimes in humid soil) are pre-adapted to
life in hypogean habitats (they are depigmented and anophthalmic). It is
common practice to define as stygobiont those species which, as far as is
known today, have exclusively been found in groundwater.
The parvidrilid family is certainly the most interesting among the taxa recently
found in Italy, from the Pre-Alps to Sardinia. So far, all records have been ascribed
to the same species, Parvidrilus spelaeus. They are exclusive inhabitants of
vadose zones in Italian caves, where they colonise the silty, muddy sediments on
the bottom of concretions, pools of trickling water and interstices of hypogean
streams. Presumably, the family has an ancient marine origin.
Among the numerous species of tubificids found in Italian groundwater, there
are the genera Haber (H. monfalconensis in springs of the Julian Pre-Alps and
Trieste Karst, and H. zavreli in groundwater in Umbria and Emilia Romagna),
two endemics of the genus Rhyacodrilus, recently described (R. gasparoi in
Pre-Alpine caves and R. dolcei in small concretions of the Trieste Karst),
Tubifex pescei, in phreatic waters of Umbria and Marches, Abyssidrilus cuspis,
Troglochaetus beranecki (ca.50x)
Cernosvitoviella sp. (ca. 40x)
■ Oligochaetes
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collected in phreatic waters in Umbria and caves of Liguria and Friuli Venezia
Giulia, Sketodrilus flabellisetosus in the Trieste Karst, and Aktedrilus ruffoi,
recently described on specimens found in interstitial environments of the river
Tione (Verona).
Enchytraeids are less well-known, and several species of Cernosvitoviella, found
in Pre-Alpine caves and considered to be stygobionts, are still being examined.
Ostracods (from the Greek ostrakon, shell) are a diversified group of small
crustaceans, whose body is enclosed by a bivalve carapace made of calcite,
their unmistakable characteristic. Their carapace may be egg-, bean- or
trapezoid-shaped, and is often knobbly or dimpled. The number and shape of
their appendages is generally the same.
Freshwater species have eight pairs of appendages, four of which are
cephalic (antennules, antennae, mandibles, and maxillulae), three thoracic,
and one caudal (uropod). They are generally small-sized (stygobionts
seldom exceed 1 mm in length), and are found in all types of surface- and
groundwater.
Despite their large numbers in groundwater, both in caves and alluvial
aquifers, stygobiont mussel shrimps are little known in Italy, and many
species are still being studied. Among the most interesting is Cypria
cavernae, thought to be endemic to alkaline karstic waters in Gorizia, Trieste
and Slovenia. Other species are associated with anchialine habitats, like
those in underground lakes of coastal caves in the Salento in Apulia
(Trapezicandona stammeri, Pseudolimnocythere hypogea). Specimens of
the genus Pseudolimnocythere were found in the brackish water of the
Poiano springs, which issue from Triassic evaporites in the upper Val
Secchia.
A very interesting genus from the palaeogeographical viewpoint is
Sphaeromicola. It is a commensal species living exclusively on stygobiont
isopod crustaceans of the genera Monolistra (Sphaeromicola stammeri, in the
Pre-Alps) and Sphaeromides (Sphaeromicola sphaeromidicola, in the Isonzo
Karst). The same genus includes a commensal species on marine amphipod
crustaceans, showing how both these ostracods and their hosts had marine
ancestors.
Mussel shrimps are very interesting in palaeogeographical research, because
their shells are easily conserved in sediments, where they fossilise. The large
numbers of fossil species, together with the great diversity of living ones,
provide detailed information about the evolution of the animals of this class.
Unfortunately, since stygobiont species are little known, have rarely been
used to analyse the origin and evolution of stygobiont fauna.
Cypria cavernae (ca. 100x)
Pseudolimnocythere sp. aff. hypogea (ca. 100x)
■ Ostracods
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■ Copepods
Copepods form the largest and most diversified group of crustaceans, with
13,000 species described, half of which are commensal or parasitic on other
organisms. Copepods are divided into ten orders, four of which include freeliving species in groundwater (calanoid, cyclopoid, gelyelloid and harpacticoid
copepods). Except for gelyelloid copepods, which live in the Jura mountains
between Switzerland and France, the other three orders are found in Italy.
Throughout their long evolution, copepods spread across continents,
successfully colonising any aquatic environment. In freshwater, they live in
standing waters (from lakes to transient pools), in benthic substrates of streams,
and in all types of groundwater. They are also found in moss, forest litter soil and
in wet meadows. Surface copepods spread easily thanks to their resting stages,
which have been described in previous “Italian Habitats” volumes. These
stages are also thought to exist in stygobiont species, although there is no
evidence. This is why species exclusive to groundwater spread with difficulty,
and are generally endemic. This characteristic is particularly evident in karstic
systems, whereas species living in alluvial aquifers generally occupy larger
areas, whose hyporheic habitats may easily be connected.
Stygobiont copepods are very small (0.2-1 mm) and, with the sole exception
of calanoids, have one main articulation between thoracic somites
Speocyclops sp. aff. infernus (ca. 120x)
(segments) 4 and 5, which divide their
bodies into two distinct parts, the
anterior prosome and the posterior
urosome. The prosome includes the
cephalothorax and four footed
somites. The cephalothorax bears six
pairs of cephalic appendages
(antennules, antennae, mandibles,
maxillulae, maxillae and maxillipeds),
Antennule of a male harpacticoid copepod
and each thoracic somite has a pair of
(ca. 850x)
oar-shaped limbs used for swimming
(hence the name copepod, from the Greek, meaning “oar-shaped foot”). The
urosome includes an anterior somite - bearing the fifth pair of thoracic
appendages - and four appendage-free abdominal somites, the last of which,
called anal somite, bears the two-branched furca, the unmistakable feature of
copepods.
Reproduction requires the participation of both sexes, and parthenogenesis is
rare. Males are distinguished from females by one (in calanoids) or both (in
cyclopoids and harpacticoids) antennules modified in the shape of claspers,
used to hold the female during mating. The fertilised eggs are usually
contained in one or two egg-sacs carried by the females. Groundwater
species produce very few eggs, sometimes only one, large. Some stygobiont
species do not have egg-sacs, and release their fertilised eggs directly on to
the substrate. Among crustaceans, copepods exhibit the most complete
metamorphosis. The eggs hatch into larvae called nauplii. There are six
naupliar stages and, after the fifth moult, the nauplii turn into copepodids,
which are segmented and similar to adults. Five copepodid stages follow, until
the sexually mature adult stage is completed.
Very little is known of the feeding requirements of stygobiont copepods.
Calanoids, which are part of plankton, are filterers; larger cyclopoids
(Acanthocyclops, Megacyclops) are predators and feed on other microorganisms. Most species are omnivorous, and the main source of food for
small interstitial copepods (almost all harpacticoids and cyclopoids of the
genera Speocyclops and Graeteriella) is particle-sized organic matter and its
associated microbial biofilm.
● Calanoid copepods. The only Italian stygobiont species, Troglodiaptomus
sketi, lives in caves in the Karst of Gorizia and Trieste, in Slovenia and Croatia.
It is commonly planktonic in underground lakes. Very little is known of its
ecology.
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Cyclopoid copepods. So far, only about a hundred species are known to
live in Italian freshwater, almost all of which belongs to the cyclopids. Few of
them are planktonic in free waters (some Metacyclops in caves of Venezia
Giulia, Apulia and Sardinia). Most are epibenthic or interstitial (e.g., genera
Eucyclops, Acanthocyclops, Diacyclops, Graeteriella, and several
Metacyclops and Speocyclops). Some species are exclusively associated with
the vadose zone of karstic habitats, where they inhabit the network of microfissures and trickling pools (several species of Speocyclops), and others (such
as Eucyclops, Acanthocyclops and Metacyclops) are exclusive to karstic
phreatic waters. Niche segregation is therefore marked, although their habitat
preferences may vary in different geographical areas. The most common and
diversified cyclopoids in Italian groundwater belong to the group languidoides
of the genus Diacyclops: this group of species, many of which are still being
described, is found in all Italian regions. Other cyclopoid species live in
restricted areas in the karstic waters of north-eastern Italy (Acanthocyclops
troglophilus, A. gordani, Metacyclops gasparoi, M. postojnae, Diacyclops
charon, Speocyclops infernus, to mention only a few), or are widely distributed
(like Eucyclops graeteri along the Alpine chain, and Acanthocyclops kieferi,
which colonises Pre-Alpine and Apennine areas). Noteworthy is
Acanthocyclops agamus, an exceptional endemic species living in caves of
the Alburni mountains (Salerno) and karstic areas in central Italy. It is an
interesting example of progenetic paedomorphosis, a phenomenon described
in the chapter on ecology. From the biogeographical viewpoint, other
interesting species live in anchialine coastal groundwater, like the cyclopinid
Muceddina multispinosa, recently described from caves in Sardinia, and
many species of cyclopids of the genus Halicyclops. All groundwater species
of cyclopids known so far probably derive from ancestors that used to inhabit
surface freshwater, and the same applies to species living in brackish water,
for which anchialine (and marine) environments are secondary habitats.
Instead, cyclopinids probably have marine origins, although none of these
species moves far from the coastline.
● Harpacticoid copepods. Except for species living in coastal marine
groundwater, which host interesting biocoenoses, six families and 160 species
of harpacticoids are known to live in continental Italian freshwater, half of which
belong to the canthocamptids. The order includes numerous benthic and
interstitial species, commonly found in all types of underground ecosystems.
Stygobiont harpacticoid species have different origins, and include species
with recent and ancient marine origin (like ameirids and ectinosomatids), as
well as those deriving from surface freshwater ancestors, like most
●
canthocamptids. There are several endemic species, many of which are limited
to specific karstic areas (genera Nitocrella, Elaphoidella, Lessinocamptus,
Moraria, Morariopsis, Paramorariopsis). Several species - only recently
discovered or currently being described - populate microfissures in limestone
or the tiny pools formed by trickling and percolating water in the vadose zone of
caves. The nature of these environments and the isolation of limestone systems
following karstification have presumably favoured speciation by vicariance,
producing large numbers of endemics.
Most endemics in karstic waters are known to live in caves in the Pre-Alps
and on Sardinia. Recently, species of the genus Pseudectinosoma have been
found in deep karstic systems of the Gran Sasso Massif, in the Alburni and
Aurunci mountains. Before this extraordinary discovery, only two species
were known in this genus, one marine species with amphi-Atlantic
distribution and the other, stygobiont, known to live in French groundwater.
The discovery of members of this puzzling genus of ectinosomatids in Italian
groundwater has great biogeographical importance, as the genus is not
known to inhabit the Mediterranean area, and Italian freshwater stygobionts
may be relict species, the only survivors of an ancient fauna which became
extinct in the marine environment during the salinity crisis that affected the
Mediterranean in the Miocene. In addition, the surprising discovery of
Pseudectinosoma galassiae in Australian groundwater confirms the extremely
Elaphoidella pseudophreatica (ca. 50x)
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ancient origin of the genus, which perhaps dates back to a period before the
onset of continental drift in the Tertiary.
Groundwater in alluvial aquifers also hosts endemic species like those of the
genera Nitocrella, Parapseudoleptomesochra and Elaphoidella in much wider
areas than in karstic environments. A particular feature of the genus
Parastenocaris is that it fragmented into a myriad of species, most of which
are known to inhabit only one or a few sites. Italy hosts 35 species - including
those of the closely related genus Simplicaris - although many more species
must still be described. Parastenocaris are the tiniest copepods (seldom
longer than 3/10 of a mm), with worm-shaped bodies and small appendages,
which enable them to wriggle through the minute fissures between sand and
gravel grains in interstitial environments.
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■ Bathynellaceans
SEM photos of harpacticoid copepods; from top to bottom: Pseudectinosoma reductum, Nitocrella
pescei and Elaphoidella elaphoides (ca. 200x)
Bathynellaceans are an order of totally
stygobiont syncarid malacostracans of
extremely ancient origin; some
researchers believe they diversified as
long ago as the Palaeozoic in littoral
coastal waters, lagoons and estuaries,
from which they colonised continental
Bathynella skopljensis (ca. 15x)
waters before the supercontinent
Pangaea fragmented, causing them to
spread into groundwater. Although only hypothetical, this fascinating scenario
describes bathynellaceans as true living fossils, and shows how research on
the taxonomy of these stygobionts is closely associated with the great palaeogeographical events which modelled the Earth’s surface.
About 170 species of bathynellaceans are known, all of small size (between 0.5
and 3.5 mm), anophthalmic and diaphanous, with elongated, sometimes
worm-like bodies. They do not have shells or brood pouches like isopods,
amphipods and thermosbaenaceans, and their last abdominal segment (called
telson) is free; these characteristics clearly identify these malacostracans.
Italian bathynellaceans are still little known and studied: the first Italian
representative of this group (Anthrobathynella stammeri) was discovered in
1954 in the interstitial environment of the river Adige in Verona, and since
then only a few species have been described, belonging to the genera
Bathynella, Hexabathynella, Hispanobathynella, Meridiobathynella and
Sardobathynella. They include exclusively hyporheic interstitial species and
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those associated with percolating water in caves. They are stenothermal
animals, sometimes living in cold waters, as they have recently been found
at high altitudes in the Alps.
■ Thermosbaenaceans
Thermosbenaceans, like bathynellaceans, are an order of very ancient
malacostracans, with about 30
stygobiont species living in fresh and
slightly brackish water from the
Caribbean sector to the circumMediterranean area, eastern Africa,
Monodella stygicola (ca. 15x)
Asia, and Australia. This group clearly
differs from other malacostracans, due
to the dorsal egg pouch formed by the carapace.
The evolution of thermosbaenaceans is probably associated with the retreat of
the sea following uplift caused by plate tectonics. The species often live in
isolated locations and are of great biogeographical interest. Their name is
misleading, as it refers to thermal water: in fact, it derives from the first species
described, which was collected in an African thermal spring.
Italy hosts four species - three of which are endemic to the country - living in
saturated aquifers. Limnosbaena finki is found in karstic and alluvial water in
north-eastern Italy (it is distributed as far as Bosnia); Monodella stygicola only
lives in karstic habitats, occasionally in alluvial aquifers, in Apulia; Tethysbaena
argentarii is an endemic species of anchialine waters in the Grotta di Punta
degli Stretti (Argentario Promontory, Tyrrhenian), and Tethysbaena siracusae is
endemic to the karstic area of Porto Palo in south-eastern Sicily.
■ Mysidaceans
Spelaeomysis bottazzii (ca. 1x)
Mysidaceans, or opossum shrimps, are
malacostracans generally living in sea
or brackish water. In Italy, there are two
stygobiont genera, Stygiomysis and
Spelaeomysis, in anchialine and
freshwater in karstic areas in Apulia.
The Mediterranean area hosts a third
stygobiont species, Troglomysis, in the
Dinaric karst. These detrivorous and saprophagous animals are 2-3 cm long thus, unusually large compared with other mysids - and are found in small
lakes, seldom in flowing water.
A euryhaline and eurythermal species, Spelaeomysis bottazzii, usually lives in
anchialine habitats in south-eastern Italy, between the Gargano and Salento
(Apulia), even in polluted water. Stygiomysis hydruntina is rare, and
presumably lives further down, where the water-table recharges; so far, it has
only been collected on the Ionian side of the province of Lecce. The two
species may locally cohabit. Although electrophoretic analyses suggest that
the species are of recent, perhaps Pliocene origin, similar species in Mexico,
the Caribbean and eastern Africa imply a more ancient, Tethyan origin.
■ Isopods
Woodlice are a very diversified order
of malacostracan crustaceans, with
more than 10,000 known species.
They presumably colonised Italian
groundwater from marine (cirolanids,
microparasellids,
microcerberids)
and surface freshwater ancestors
(asellotans and perhaps sphaeromatids).
Each family is a microcosm in itself,
Proasellus franciscoloi (ca. 6x)
and their study reveals very interesting
biogeographical aspects.
Asellids. Almost all stygobiont species of this family are Italian endemics.
Asellus cavernicolus lives in the river Timavo (Trieste Karst). Results from
molecular studies reveal that it is a relict species deriving from pre-glacial
colonisation of the Trieste Karst by an epigean species, Asellus aquaticus. In
Italy, the genus Proasellus counts several surface as well as cavernicolous
and interstitial species.
The genus diversified into many phyletic lines, the taxonomy of which
requires clarification: the group deminutus in north-eastern Italy; pavani in the
central-eastern Pre-Alps; cavaticus in France, western Piedmont and Liguria,
in karstic environments (P. cavaticus, P. franciscoloi), and the group patrizii,
exclusive to Sardinian groundwater. In addition, there are many similar
species: P. ligusticus, found from Liguria to the Apuan Alps, and P. acutianus,
in Tuscany, Latium and the island of Elba are the most widely distributed
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species. Other species are only known to live in restricted areas, like P.
amiterninus, P. dianae, P. adriaticus and P. faesolanus.
The similar genus Chthonasellus includes C. bodoni, endemic to karstic and
interstitial waters in the Cuneo area (Piedmont), which is thought to be
phylogenetically close to the French genus Gallasellus.
Stenasellids. This family comprises exclusively stygobiont species of very
ancient origin, found in Tuscany (Stenasellus gr. racovitzai) and Sardinia, in
both caves and interstitial habitats. In Sardinia, techniques of molecular
biology have identified many endemics, two of which have so far been
attributed to S. racovitzai and are similar to French species, and two others
(S. nuragicus, S. assorgiai) are similar to species found in eastern Europe.
Two species collected in the area of Nuoro (Sardinia) are similar to Spanish
species.
Preliminary dating based on “molecular clocks”, suggests that the separation
of the two phyletic lines dates back about 28 million years (Upper Miocene).
This is one of the most fascinating biological pieces of evidence of the
complex Tyrrhenid history.
Microparasellids. This family of tiny isopods (a few mm long) deriving
from ancient marine ancestors which colonised interstitial habitats
during the marine regressive phases. Their distribution follows the
ancient coastline of Tertiary seas. In Italy, six interstitial species are
known, all belonging to the genus Microcharon (see drawing). Of
these, only M. marinus is associated with transient groundwater
along the Mediterranean coasts, and the geographical location of
other species - e.g. M. novariensis, found in Piedmont springs reveals that they are relicts.
Microcerberids. The family comprises mainly marine species, and only
the relict Microcerberus ruffoi (see drawing) lives in Italian underground
freshwater (water-table of the river Adige).
Cirolanids. This family includes mainly marine species, and only
two are Italian stygobionts. Sphaeromides virei inhabits alkaline
water in the Gorizia Karst. A voracious predator, it is quite large (more
than 3 cm long). Its typically Balkanic distribution and fragmentation
into endemic subspecies suggest that it originally lived in
groundwater in the Dinaric karst. Typhlocirolana aff. moraguesi is
exclusive to the karstic system near Porto Palo (Siracusa, Sicily),
and was distinguished from T. moraguesi (island of Majorca) with
molecular biology techniques. Its origin is probably palaeoMediterranean.
Sphaeromatids. Many species of the genus Monolistra, widely distributed in
the Balkans, also live between the Italian-Slovenian border and the area of
Como (north of Milan), in karstic groundwater in Pre-Alpine caves. Their
absence north of the line that marked the southern boundary of the great
Quaternary glaciers shows that they settled in groundwater during the
Pliocene, perhaps deriving from surface freshwater ancestors which have
become extinct.
Ongoing molecular research will clarify their evolution. Each species and
subspecies is endemic to a restricted karstic system. Monolistra
schottlaenderi is exclusive to saturated aquifers of the Karst in the areas of
Trieste and Isonzo, and is the only Italian member of the subgenus
Microlistra, which also lives in Slovenia and Croatia. The species of this
subgenus have knobby dorsal protrusions, and sometimes even long, robust
spines that function as efficient defensive structures when the animal curls
into a ball.
Among other species, with smooth teguments, there is Monolistra julia,
endemic to caves in the Julian Pre-Alps, where it lives in small streams of
trickling water. It has two well-developed caudal appendages (uropods). Other
species do not have uropods, which may be atrophic or barely visible. The
furthest west (Monolistra pavani) is found in the underground stream of the
Buco del Piombo (Como).
Monolistra racovitzai (ca. 5x)
63
■ Amphipods
64
Species of genus Niphargus; top: N. costozzae; centre: N. longicaudatus; left, bottom: N. pescei (top)
and N. transitivus (bottom); right, bottom: N. bajuvaricus grandii (ca. 3x)
This order of malacostracans includes
several marine and freshwater species,
sometimes sub-terrestrial, which
colonised groundwater either directly
from the sea, or from ancestors that
once inhabited limnic surface water. In
Italy, there are about 100 stygobiont
species, almost all of which are
endemic.
Bogidiellids. Italian freshwaters host
Bogidiella sp. (ca. 10x)
seven stygobiont species, most of
which are interstitial, occasionally
euryhaline. Bogidiella albertimagni (in the Po Plain) and Bogidiella aprutina are
the only continental species; the others are Tyrrhenian endemics, found in
Sardinia and on the island of Elba.
Gammarids. This family comprises exclusively surface species. Among those
which only live in groundwater and are Italian endemics, two species of
Tyrrhenogammarus live in karstic aquifers in south-eastern Sicily
(Tyrrhenogammarus catacumbae) and Sardinia (T. sardous). One species of
Longigammarus (L. planasiae) has recently been collected from a well on the
limestone island of Pianosa (Tuscan archipelago), and a specialised species,
Ilvanella inexpectata, is known to inhabit alluvial aquifers on the island of Elba
and in Tuscany.
Hadziids. The genus Hadzia - presumably a Tethyan relict - has four Italian
species. Hadzia fragilis stochi, an endemic subspecies with delicate, elongated
appendages, has been described in alkaline water in the karstic area of Trieste
and river Isonzo. Hadzia minuta inhabits karstic waters in Salento, and H.
adriatica has been collected from pools in Apulia. Another species, which is
still under description, was recently found in southern Sardinia.
Niphargids. The genus Niphargus (more than 250 known species, 70 of which
live in Italy; size between 3 and 40 mm) have complex, controversial
taxonomy, which is currently being revised by means of molecular biology
techniques. Their distribution area includes most of Europe (except for the
Iberian Peninsula and the upper northern areas) and stretches east towards
Iran. This suggests that the genus colonised European surface freshwater
from the basins of the Tertiary Paratethys, and later moved into groundwater.
However, fossils similar to present species have recently been found in Baltic
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amber, implying a perhaps more ancient origin. Almost all species are endemic
and live in the Alps and Po Plain, in several distinct, although not welldefined phyletic lines (the main groups being stygius, kochianus, aquilex and
bajuvaricus).
The diversity of the genus decreases proceeding southwards down the
Apennines, with species belonging to the groups speziae (northern and
central Apennines), longicaudatus (throughout the Apennines, Sicily,
Sardinia, and smaller islands), and orcinus. This last group includes species
similar to Balkan ones (exclusively associated with karstic aquifers), which
colonised Italy from the Julian karst in the north-east and, perhaps through
trans-Adriatic pathways, the limestone systems of the central-southern
Apennines and Apulia. In addition to these groups, there are several species
of unknown affinity, like Niphargus stefanellii (found in caves in centralsouthern Italy), which seems related to Balkan species, and colonises even
sulphureous waters.
Niphargus species, which are greatly diversified in structure and size,
colonise all types of underground habitats. In large alkaline karstic lakes,
species are large (2-4 cm) with elongated antennae and other appendages,
and large anterior claw-shaped limbs (gnathopods) for seizing prey
(Niphargus steueri, N. tridentinus). Interstitial environments host small
omnivorous species (3-10 mm) with globose (Niphargus pupetta, N.
transitivus) or elongated, worm-like bodies (Niphargus bajuvaricus grandii,
N. italicus). Other species colonise subsurface, non-karstic aquifers, and
may even be found in moist soil. They have tapering bodies, like N.
dolenianensis and various species of the group longicaudatus. Italy also
hosts the only species of the related genus Carinurella (C. paradoxa), which
has a globose body with stumpy appendages and lives in interstitial waters of
Friuli Venezia Giulia.
Salentinellids. This is possibly a palaeo-Mediteranean amphipod family that
comprises only stygobionts deriving from marine ancestors, whose identity is
still uncertain.
Salentinella species are still undergoing revision, and the most common
species, S. angelieri, is typically interstitial and lives in brackish water near the
coastline. It is also found in caves of isolated karstic systems and in true
continental groundwater, with other species like S. franciscoloi of Liguria.
Salentinella gracillima is exclusive to groundwater in Apulia.
Ingolfiellidae. This family includes many stygobionts with elongated bodies
living in marine and freshwater interstitial environments. So far, only one
species has been found in Italian fresh groundwaters: Ingolfiella
(Tyrrhenidiella) cottarellii, from a cave on the island of Tavolara (off the northeastern coast of Sardinia).
Metaingolfiellids. The family comprises the single species Metaingolfiella
mirabilis, which is quite large (3 cm). Many specimens of this species were
collected, on a single occasion, from water pumped out of a deep karstic well
in Salento. Described in 1969, it has never been found since. It is perhaps one
of the most ancient palaeo-endemics of Italian fauna. Its body structure and
the shape of its gnathopods suggest that it is a predator.
Pseudoniphargids. This family includes only stygobionts, and is particularly
diversified in the Mediterranean area. In Italy, only a few species are known,
living in interstitial environments and caves near the coastline, showing their
marine origin. Two species (Pseudoniphargus africanus italicus, P. sodalis) live
in Sicily, and one (P. planasiae) in the Tuscan archipelago. Pseudoniphargus
adriaticus has been collected in wells near Bari, and is also known to inhabit
the Pelagian Islands (between Sicily and Tunisia), although its taxonomic
status is uncertain. Other specimens, collected in Sardinia, are still being
examined.
Metacrangonyctids. This family is distributed around the Atlantic, includes only
stygobionts, and is very diversified in the Mediterranean area. Italy hosts only
Metacrangonyx ilvanus, endemic to the island of Elba, where it was recently
found only in one well in alluvial groundwaters.
Salentinella angelieri (ca. 30x)
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■ Decapods
Italian fauna has only two stygobiont
decapod genera living in karstic waters:
Troglocaris (Isonzo and Trieste Karst)
and Typhlocaris (Apulia). Recent
research has revealed that Italian caves
actually host two species of shrimps of
the genus Troglocaris of the
anophthalmus group, morphologically
difficult to distinguish, but easily
identified by means of molecular
Troglocaris anophthalmus
biology techniques. They may belong
to T. anophthalmus (Gorizia Karst) and
T. planinensis (Trieste Karst), although
their
taxonomy
still
requires
confirmations. Stygobiont species of
the genus Troglocaris were thought to
derive from marine ancestors. Very
recent molecular biology analyses
carried out at the University of Ljubljana
(Slovenia) have dated the separation of
the western anophthalmus group from
the Dinaric-Caucasian one at between
6 and 11 million years ago, and the
beginning of speciation within the
Typhlocaris salentina
anophthalmus group between 3.7 and
5.3 million years ago. Their marine origin is therefore very ancient, and
populations colonised groundwater coming from surface freshwater.
The third species of Italian stygobiont decapods, Typhlocaris salentina, is
endemic to Apulian caves. It was discovered in the Grotta Zinzulusa at Castro
Marina in 1922, and later collected from other caves in Salento, Murge and
Gargano. This blind, depigmented prawn may reach exceptional sizes (up to
13 cm); a predator, it feeds on mysidaceans and stygoxene organisms.
The genus Typhlocaris includes two stygobiont species living in groundwater
in Israel and Libya, suggesting that it is an ancient relict of an otherwise extinct
palaeo-Mediterranean pre-Pliocene surface fauna associated with a subtropical climate. Unfortunately, molecular data on this genus are not yet
available.
■ Amphibians
The olm (Proteus anguinus) is the only stygobiont amphibian of the Palaearctic
fauna. The pétit dragon of the Postojna caves (Slovenia) - discovered by the
Slovenian nobleman Valvasor in 1689 and briefly described by Laurenti in
1768 - is the best-known underground animal described so far and, in some
ways, the most fascinating. It has a pinkish-white eel-shaped body, with
atrophic eyes concealed under the skin and outer red gill plumes which it
retains throughout its life. The olm is known for its neoteny, i.e., it reaches
precocious reproductive maturity despite its larval appearance. Olms are
predators feeding on other aquatic, even stygoxene animals; the females lay
between 20 and 80 eggs, one at a time for over one month, and place them
under rocks and stones. The greyish tadpoles have distinct eyes, which they
retain until they are two months old. Until the age of three months, olms feed
exclusively on yolk stored in the cells of their digestive tracts. In nature,
reproduction seldom occurs before the tenth year of age.
The origin of olms is debated. Fossils of proteids and iguanodonts, found at
Bernissart in Belgium, date back to the Lower Cretaceous, when olms lived in
surface water. Their colonisation of karstic groundwaters in the Dinaric area
where they now live may have started in the Pliocene, when karstification
began. In 1994, in the Slovenian Karst, a pigmented, eyed subspecies was
Olms also live in the groundwaters of the Isonzo Karst
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discovered (Proteus anguinus parkelj)
genetically similar to the stygobiont
populations of the same area, and
thus suggesting that groundwater
populations are more recent.
Recent molecular analyses reveal that
there may be more stygobiont olm
species.
In Italy, olms are known to inhabit only
alkaline water in caves of the Trieste
and Isonzo Karsts. An isolated
population, introduced from Slovenia
in 1850, still lives in Grotta Parolini at
Oliero (Vicenza).
Olms are the only Italian stygobionts
listed as priority species in the Habitats
Directive; they are also included in
Annex IV and are therefore under strict
protection.
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Some olm specimens, coming from Slovenia,
were introduced into the Oliero cave system
(Veneto) in 1850
■ Italian stygofaunal provinces
As analysis of previously described taxonomic groups suggests, the present
geographical distribution of stygobiont species in Italy is the result of a series
of events which took place in ancient times (historical factors) and, to a lesser
extent, of ecological factors, which occour in “real time”. The role played by
both is described in the chapter on ecology.
Since the evolution of many Italian taxonomic groups was similar over time,
because they were affected by the same palaeogeographical events, Italy is
divided into areas with similar fauna, particularly endemics. These areas are
called stygofaunal provinces. Although these generalisations cannot tell us
directly what the present fauna composition of a specific aquifer is, because
this is also influenced by local events, they do describe the present situation
of Italian stygobionts and explain where the most important endemic
locations are found.
Olm (Proteus anguinus)
Dinaric province. This area includes only the easternmost portion of Italy the so-called “classic” Karst - an elliptical area of 200 km2, whose
stygobionts are similar to those of the Karst in Slovenia, Istria and Dalmatia.
The area was affected by karstification
in the late Miocene, and hosts many
palaeo-endemics. Exclusive to the
karstic vadose zone are harpacticoid
copepods of the genus Morariopsis,
the
bathynellacean
Bathynella
skopljensis and the amphipod
Niphargus stygius.
Exceptional fauna, whose western
limit of distribution is the Karst,
populates large cavities filled with
alkaline karstic water.
Among these, there are polychaetes
(Marifugia
cavatica),
gastropods
(Belgrandia stochi), ostracods (Cypria
cavernae), calanoids (Troglodiaptomus
sketi), and several cyclopoids and
Sphaeromides virei (ca. 1x)
harpacticoids (like Acanthocyclops
troglophilus and Nitocrella stochi). This area hosts the only Italian stygobiont
isopods of the genus Asellus, those of the subgenus Microlistra, and the large
Sphaeromides, as well as amphipods, which are highly diversified, with many
endemics (e.g., Niphargus stochi, Hadzia fragilis). Other remarkable
inhabitants are decapods of the genus Troglocaris, and the most famous
stygobiont species, the olm (Proteus anguinus). Aquifers in marl and
sandstone also host very interesting fauna, with very different species from
those found in adjacent karstic aquifers. Among the main biogeographical
markers, there is the gastropod Istriana mirnae, and the large amphipods
Niphargus spinulifemur and N. krameri.
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Stygofaunal provinces in Italy
Alpine province. The Alpine stygofaunal province includes a very complex
area associated with Alpine orogenetic events. It is divided into a northern part
(strictly Alpine), above the southern limit of the great Quaternary glaciations,
and a southern Pre-Alpine one, below which is the recent alluvial area of the
Po Plain. The Alpine area is populated by only a few stygobionts: cold-loving,
stenothermal species which followed the retreat of Quaternary glaciers and
colonised aquifers in carbonate and crystalline rocks in the Alps. In particular,
a number of amphipods (Niphargus forelii, N. similis, N. strouhali) even live at
high altitudes, above 2000 m, together with a few copepods and
bathynellaceans.
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In the Pre-Alps, the situation changes completely, as there are large numbers
of endemics living in the numerous karstic systems. The main
biogeographical component is of eastern origin and stretches westwards as
far as the Pre-Alps near Como, with a few genera living on Mount Fenera
(Piedmont) (hydrobioid gastropods of the genus Iglica, harpacticoids of the
genus Paramorariopsis). Typical genera of this area are several hydrobioids
(Bythiospeum, Hauffenia, Hadziella, Iglica, Paladilhiopsis), harpacticoids
(Lessinocamptus, Paramorariopsis, and several species of the genus
Elaphoidella), amphipod crustaceans (Niphargus of the stygius group) and
isopods (Monolistra, Proasellus). The western and Ligurian Pre-Alps have
fewer stygobionts, and their fauna is more similar to that in France (Proasellus
of the cavaticus group) and the Apennine province (Alzoniella, Niphargus of
the longicaudatus group).
several cyclopoids of the groups languidus and languidoides of the genus
Diacyclops, the bathynellacean Anthrobathynella stammeri, and the
amphipods Bogidiella albertimagni and Niphargus bajuvaricus grandii. There
are also more ancient organisms of pre-Quaternary marine origin, relict
species survived to Pliocene events, perhaps also to Miocene sea retreat, like
the recently discovered ectinosomatid harpacticoids and isopods of the
genera Microcerberus and Microcharon.
Padanian province. The alluvial areas of the Po Plain, which stretch into the
Alpine and Apennine valleys, have many endemics. Here, as in the nearby
Alpine province, there are many species from the east, such as the isopod
Proasellus intermedius, and several endemic amphipods (Niphargus italicus,
N. pupetta, N. transitivus, N. longidactylus, Carinurella paradoxa). Other
species are associated with the fauna of the extensive plains of centraleastern Europe, and probably migrated towards Italy in more recent times, like
Apennine province. Despite its extent, from the Colle di Cadibona (Savona) to
the Madonie in Sicily (excluding Apulia), the fauna of this area is well
characterised. There are areas rich in endemics (Ligurian Apennines, Alburni
mountains, Gran Sasso Massif) that are widely distributed in the Apennines.
The apparent monotony of this fauna may be related to historical events, as
karstification here is a recent event, and the fragmented limestone outcrops in
the Apennines were covered by little permeable soil in the interval between the
Pliocene and Miocene, and were only uncovered in the Quaternary. These
palaeogeographical events are very similar from Latium to Calabria, and the
areas are inhabited by endemics which are found along the Apennines and do
not have particular habitat preferences (cyclopoid copepods of the genus
Diacyclops, harpacticoids like Attheyella paranaphtalica and Nitocrella
stammeri, and the amphipod Niphargus longicaudatus, which live in recent tufa
Diacyclops gr. languidus, females with egg-sacs (ca. 70x)
Harpacticoids of the genera Lessinocamptus (left) and Paramorariopsis (right) (ca. 100x)
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aquifers in the Sabini mountains and in
karstic water in Cilento and evaporites
in Calabria as well). These recent
populations settled where palaeoendemics were already living and
characterised Apennine areas. Thus,
groundwater percolating in Triassic
evaporites in Emilia hosts Niphargus
poianoi; the karstic systems of the
Aurunci, Gran Sasso and Alburni
ranges are inhabited by the
extraordinary copepod Acanthocyclops
Stygiomysis hidruntina (ca. 2x)
agamus and species of the genus
Pseudectinosoma, which are perhaps
Messinian relict. As regards gastropods, the genera Alzoniella, Avenionia and
Fissuria live in the northern Apennines, and Arganiella, Orientalina and
Pauluccinella in the central Apennines; the genus Islamia is divided into
northern and central-southern species.
Apulian province. Apulian groundwater is clearly different from that of the
Apennines, and is rich in specialised endemics, especially in often brackish,
saturated, karstic habitats. This is due to the extent and ancient origin of
karstification, as well as to the geological history of Apulia, which palaeogeographers consider as part of a different tectonic micro-plate from those
that shaped the Italian peninsula. These waters host exceptional specialised
organisms of marine origin, like the sponge Higginsia ciccaresei, the
gastropod Salenthydrobia ferrerii, the ostracods Trapezicandona stammeri
and Pseudolimnocythere hypogea, the thermosbaenacean Monodella
stygicola, the extraordinary metaingolfiellid amphipod Metaingolfiella
mirabilis, the hadziid amphipod Hadzia minuta, the salentinellid Salentinella
gracillima, mysids of the genera Spelaeomysis and Stygiomysis, and the large
decapod Typhlocaris salentina.
Tyrrhenian and Sardinian provinces. This province includes Sardinia, part of
the Tuscan archipelago and isolated coastal areas in Italy deriving from the
fragmentation of the Tyrrhenid, which started in the Oligocene. PalaeoTyrrhenian endemics are phylogenetically similar to evolutionary lines in the
areas of Provence, the Pyrenees and Corsica. Among the several Sardinian
endemics, the gastropod genera Sardhoratia and Sardopaladilhia, many
species of cyclopoid and harpacticoid copepods, the bathynellacean
Sardobathynella, the entire phyletic line of isopods related to Proasellus patrizii,
and isopods of the genus Stenasellus, are also found along the Tuscan coast.
Also presumably of palaeo-Tyrrhenian origin are the thermosbenacean
Tethysbaena argentarii of Mount Argentario (Tuscany) and the amphipod
Metacrangonyx ilvanus of the island of Elba. Other animals associated with local
anchialine water are many amphipods of marine origin of the genera Bogidiella
and Pseudoniphargus, and the subgenus Thyrrenidiella of genus Ingolfiella.
More doubtful are the relationships between some gammarid genera, like
Longigammarus, Tyrrhenogammarus, and the puzzling Ilvanella.
Iblean province (Sicily). Sicilian stygobionts are biogeographically composite
and little known, especially those living in the alluvial plains and karstic
aquifers that sometimes develop in chalk. Clearly identified organisms are
found in the Iblean area, especially in the water-table of the karstic system
near Porto Palo. Although this small area is jeopardised by man-made
alterations, exceptional, perhaps palaeo-Mediterranean endemics inhabit it,
like the thermosbaenacean Tethysbaena syracusae, the cirolanid isopod
Typhlocirolana aff. moraguesi, and the amphipods Tyrrhenogammarus
catacumbae and Pseudoniphargus duplus.
Examples of distribution of endemic stygobiont species; left: gastropods of the genus Paladilhiopsis
(Eastern Pre-Alps, red circles) and Arganiella (Apennines, green circles); right: crustaceans of genera
Stenasellus (Tyrrhenian, red circles), Spelaeomysis (Apulia, blue circles) and Tyrrhenogammarus
(T. catacumbae, Iblean Mts, Sicily, green circles)
77
Ecology
DIANA MARIA PAOLA GALASSI
Although Stygobiology - the science
that studies groundwater biology dates back to the 18th century, it was
only in 1994 that the ecological
importance of this environment was
finally acknowledged and exhaustively
described
in
the
monograph
Groundwater Ecology (see select
bibliography). No matter how surprised
we may be to learn that findings in
groundwater ecology are recent, our
surprise turns to shock on hearing
that, although groundwater protection
and management are of paramount
importance for human survival, current
legislation does not take into account
the ecology of this particular
Bottom of an old well for drinking-water
environment.
This is probably due to the unique characteristics of groundwater: invisible to
most, not perceived as part of the territory, a totally dark world populated
almost exclusively by tiny creatures. The biodiversity of this environment is
truly “hidden”, as the subtitle of this volume suggests. This is perhaps the
reason, albeit not a justifiable one, why man, in both law and culture, has
always considered the exploitation of groundwater as more important than its
ecology. It is a narrow-minded view, as we realise when reading the previous
chapter on the complexity, diversity and scientific importance of stygofauna.
It therefore comes as no surprise that, while there are only a few books to
describe the geological and speleological aspects of these habitats, almost
none has yet been published in Italy on underground ecology. This chapter is
an attempt at overcoming the anthropocentric view of groundwater, at
illustrating how the ecosystem works, and analysing the ecological factors
that regulate the structure of groundwater communities and biodiversity.
Waterfall produced by the karstic spring of Col del Sole (Friuli Venezia Giulia)
79
80
■ The ecology of aquifers
According to their hydrogeological and hydrological characteristics, aquifers
are divided into three groups.
Karstic aquifers are the most intensively studied from the biological
viewpoint, perhaps because caves allow scientists easy access to them.
These aquifers develop in large bedrock cavities, generally limestone,
through a complex network of micro-fissures formed by the dissolution of
carbonates.
This group includes waters that penetrate chalk, and that flow into
conglomerate, in which dissolution acts on evaporites and the cementing
matrix of breccia and puddingstone. In the hydrological cycle, karstic
aquifers undergo great variations in flow and, therefore, from the ecological
viewpoint, they are less predictable systems.
Unsaturated (vadose) karstic systems, which are more directly influenced by
rainfall, are less stable than saturated ones. However, the stability and
predictability of saturated karstic systems in turn depend on the age and
depth of aquifers. Generally, ancient, deep aquifers are ecologically more
stable than young, shallow ones.
Porous and alluvial aquifers develop in unconsolidated sediments where
interstices between sediment particles vary according to the particle size of
the sediment itself.
Porous aquifers may be divided into unsaturated or semi-saturated and
saturated (water-tables). Medium-fine porous aquifers have greater physical
inertia and, as water lasts in them for longer than in karstic aquifers, they are
ecologically more stable and predictable.
In non-karstic lithoid (stone) aquifers, water circulates in fractures (as in
crystalline rock), between layers (marl-sandstone in flysch facies) and
cavities of other origin (e.g., the lava flows of Mt. Etna). Water percolates in
fissures whose size depends on the events that created them, and on the
solubility and erodibility of rocks.
Practically unknown from the ecological viewpoint, these aquifers are very
similar to karstic ones if their fractures or cavities (as in lava tubes) are large,
or behave like porous ones in the surface cortex, where soil and
disintegrated rock host communities typical of porous systems.
Lastly, a particular mountain environment is found in leaf litter with trickling
water underneath, the so-called hypotelminorheic habitat. This does not
represent a true aquifer, but is surface water flowing a few centimetres deep.
Sketch showing the three main types of aquifers: fractured lithoid (A), porous (B), karstic (C)
Hypotelminorheic habitat
81
82
Although the ecology of this unsaturated habitat is similar to that of porous
surface aquifers, it is very unstable and unpredictable.
Organisms from adjacent and underlying aquifers may migrate to these
habitats to feed.
The same aquifer often hosts more than one of the above categories: for
instance, there are streams in cavities between flysch and limestone (in
Friuli Venezia Giulia), between limestone and conglomerate (Veneto PreAlps), travertine and tuff (Latium), limestone and chalk (Grotte di Frasassi),
limestone and lava (Lessini mountains), and limestone and granite
(Sardinia).
In addition, the water of karstic aquifers often drains to alluvial beds in
valleys with complex hydrogeological and ecological relationships.
The main ecological aspect deriving from the classification described above
is that the various types of aquifers provide fauna with a complex availability
of living space, with changes in structural complexity, food resources,
stability of hydraulic conditions and water chemistry. Basically, different
aquifers develop different habitats, and may host completely different
animals.
For instance, locally or extensively saturated karstic aquifers often have
large hydric spaces (underground rivers or lakes), and therefore contain
larger organisms which may reach a few centimetres in size, like large
cirolanid isopods, mysids, decapods and the olm, the only Italian stygobiont
vertebrate.
Unsaturated karstic environments host smaller animals because the pools in
caves - large pools or lakes of trickling water - are only transient habitats for
fauna living in limestone micro-fissures above, adjacent to or underneath the
pools.
Medium-fine porous aquifers provide little living space, and only small
animals - less than 1 cm long, often smaller than 1 mm, according to the
size of particles - with particular adaptations have been able to colonise
them.
Fractured aquifers, in line with their nature, may offer different extension of
living spaces, and therefore host relatively large animals (in flysch, amphipods
of the genus Niphargus are up to 4 cm long) as well as microscopic organisms
typical of porous systems.
Unsaturated karstic habitat (micro-concretions)
Porous habitat with (detail) a specimen of Niphargus in its environment
■ Groundwater habitats
83
84
The discovery of a new submerged world: anchialine environments
Anchialine environments were first
discovered in 1966, when the Austrian
scientist Rupert Riedl described them
as “marginal caves”. Since then,
experts have debated the correct
definition of anchialine systems. Today,
they agree on defining them as caves
or other underground aquatic habitats
near the coastline of islands and
continents, supplied by continental
freshwater and with underground
connections to the sea. Consequently,
the water of anchialine pools is
brackish, and light-weight freshwater
generally floats on top of heavier
seawater.
The most typical feature of anchialine
environments is the absence of a
surface connection with the sea, which
manages to reach far inland through
deep infiltration passages in limestone
and volcanic rocks.
The most fascinating, extraordinary
examples are the well-known Mexican
cenotes, small bodies of crystalline
brackish water, like blue eyes glittering
in the tropical forests of Mexico and
Belize, not far from the coast. In Italy,
typical anchialine pools are found in
the Grotta Zinzulusa, Abisso and Buco
dei Diavoli (Salento), together with
other water-tables in Apulia,
groundwater in Porto Palo (Sicily), the
Grotta Verde, Grotta di Nettuno and
Grotta del Bue Marino (Sardinia) and
the Grotta di Punta degli Stretti
(Argentario, Tuscany).
Anchialine pools are marked by few
food resources, total darkness, and
vertical gradients of salinity and
oxygen concentrations. Although in the
past anchialine ecosystems were
believed to support themselves on
allochthonous organic matter (deriving
from the rock above and from
seawater), today we know that part of
the organic matter is locally
synthesised by chemo-autotrophs.
The most fascinating aspect that
makes these environments true treasure
troves of biodiversity is their exclusive
fauna. Examples are remipedes, the
most primitive class of living
crustaceans, which have been found in
anchialine caves on the Bahamas, in
lava tubes on the island of Lanzarote
and, more recently, in Australia.
Remipedes, like many other animal
groups found in these habitats, are true
living fossils, whose distribution,
enigmatically uneven in several areas
of the world, dates back to the breakup of the ancient Tethys Sea.
In addition to these unique organisms,
there are also other extraordinary
animals, some of which are Italian
endemics with restricted distribution,
like the sponge Higginsia ciccaresei,
the thermosbaenacean Monodella
stygicola, the mysid Stygiomysis
hydruntina, and the decapod
Typhlocaris salentina.
It is worth noting that the copepod
Muceddina multispinosa was recently
discovered in the Grotta Verde (Capo
Caccia, Alghero, Sardinia), a species
with disjunct distribution also found in
anchialine environments on the islands
of Mallorca and Lanzarote (Spain).
Generally speaking, anchialine habitats
host heterogeneous assemblages
which includes strictly marine animals
and, to a lesser degree, freshwater
organisms.
Typically anchialine species are closely
associated with the particular
environment in which they live, and
have never been found in other types of
Diana Maria Paola Galassi
underground habitats. They are also
stygobionts, and have marked
specialised features. Their origin dates
back to various geological times, from
the Tertiary to the more recent
Pleistocene. Some researchers believe
that their ancestors lived in the abysses
of the sea; others trace their origin back
to organisms living in shallow seawater
on the continental shelf.
Sea entrance to the Grotta Zinzulusa (Salento, Apulia)
85
87
86
Simplified sketch of a karstic aquifer
■ Ecology of karstic aquifers
The Fontanon di Goriuda drains the karstic plateau of Mt Canin (Julian Pre-Alps, Friuli)
The network of karstic conduits has two components that offer different living
conditions to fauna: transmissive and capacitive components. The transmissive
component is typical of highly karstified systems with great hydraulic
conductivity and fast currents and, ecologically speaking, has little biodiversity.
What kind of species could possibly survive in such hostile environments? Yet
some actually can, and have even been incredibly successful in adapting to
these harsh habitats. For example, some amphipod crustaceans of the genus
Niphargus have evolved adaptations to exploit the advantages of fast currents
in habitats where interspecies competition is very low.
Research carried out in France reveals that these species, which perhaps live
in fissures adjacent to the transmissive/drainage conduit, lay their eggs
nearby, and exploit the speed of the current to disperse their young. Briefly,
they synchronise their biological cycle to the discharge of the aquifer while
developing growth strategies typical of changeable habitats: thus, they
produce large numbers of fertilised eggs, a few of which will reach the adult
stage, in ways which are typical of surface species rather than underground
ones. Some species of isopod crustaceans of the genus Monolistra also
exploit fast currents by curling up into balls and letting themselves be
transported over great distances.
In capacitive karstic systems, whose development varies according to the
aquifer, water percolates in medium-sized and small fractures in branching
88
anastomoses, often adjacent to the main drainage system. Here, they form
small pools of calm water which are connected to one another and flow into
the main drainage conduit. This lateral network, which is generally more
extensive and has greater volume than the drainage one, is called the
capacitive annex system. Unlike the drainage system, which poses a severe
threat to the survival of species, the situation is completely reversed in the
capacitive system, where water flows slowly and there are large amounts of
organic matter and inorganic sediments, creating habitats for many
underground species. Biodiversity may even increase in capacitive systems
with wide, diversified living environments, like underground lakes. Only in
these habitats do we find plankton (calanoid copepods) together with benthic
and interstitial organisms, large predators, like cirolanid isopods, large
decapod crustaceans, and the olm.
Unsaturated karstic systems also have a diversified network of storage microfractures, where living conditions are favoured by the three-dimensional
complexity of the system. The diversity of substrates in small pools of water
(pools and puddles with silt, clay, sand and organic material percolating from
the surface, or complex calcium microstructures) give rise to diversified fauna,
even if temporary water circulation prompts species to devise adaptations to
withstand adverse conditions in small, locally saturated fractures.
Sketch illustrating connection between transmissive system and capacitive annex subsystem during flood and
drought periods
■ Ecology of alluvial aquifers
The habitats of saturated porous aquifers are not very heterogeneous, and
conditions are determined by the size of sediment grains in unconsolidated
sediments. Food is restricted, because most of the organic matter coming
from the surface is trapped in the subsurface layers of aquifers.
The opposite is observed in surface unconsolidated sediments, generally
unsaturated, where the surface aquatic and terrestrial environments are
continuous or adjacent, giving rise to heterogeneous habitats due to the
ecotonal nature of these environments and the greater availability of organic
matter.
Proximity to wet or dry surfaces produces greater concentrations of organic
matter than in deeper saturated layers, thus contradicting the now out-dated
idea that underground habitats lack niches and habitats.
The hyporheic environment (where groundwater and surface water mix) is
perhaps the most typical example of a subsurface alluvial aquifer and is,
among underground habitats, certainly the best-known from the ecological
viewpoint. It is an ecotone, that is, a transitional area between the surface
habitat of running water (stream or river) and the saturated underground
habitat (groundwater).
Gravel bed of the Tagliamento (Friuli Venezia Giulia)
89
90
Literature defines this environment in myriad ways, each a nuance of the
other, the only differences being the thickness attributed by each expert to
the hyporheic layer. Aquatic ecotones are areas in which large-scale hydraulic
exchanges occur and where biogeochemical activity - more intense than in
adjacent habitats - affects the quality of water flowing through the interface.
Hyporheic environments thus regulate water flow, and temporarily or
permanently store organic, mineral and sometimes polluting matter. The
microbial and animal components in them actively modify the timing and
volume of nutrient and pollutant flows. From the structural viewpoint, the
hyporheic zone is a matrix of permanently dark interstices saturated with
water flowing slowly, with slight daily temperature variations and great
bedrock stability. The hyporheic zone is an aphotic (without light), mechanical
and biogeochemical filter between surface and underground water systems,
ensuring their purification and maintenance.
From this viewpoint, an important contribution came in 1993 from the
American researchers Stanford and Ward with their concept of hyporheic
corridor, which describes the connections and interactions between the
hyporheic zone and the catchment basin. The role played by the hyporheic
corridor in a catchment basin is essential for many ecological processes
associated with nearby water sources: 1) the primary productivity in the
stream above the hyporheic zone is strongly influenced by the distribution
and frequency on the vertical scale of zones of upwelling (where the watertable supplies the stream), outwelling (areas where subsurface water supplies
the stream laterally) and downwelling (areas where surface water supplies the
water-table) of the stream, because the last two are usually richer in algal
nutrients like nitrates and phosphates than surface water; 2) the temporal and
spatial variability of processes of hydric exchange cause biodiversity in the
hyporheic zone to increase more than in the adjacent water-table and surface
habitats.
Although Italian rivers are relatively well-known from the hydrological,
biological and ecological viewpoints, an integrated overview of the Italian
river ecosystem is still missing. Research emphasises a lateral dimension,
i.e., the relationships between stream beds and surrounding floodplain and
river areas in particular; a longitudinal dimension, i.e., the variations occurring
along the length of rivers, from spring to outlet, although little is known about
the vertical dimension, i.e., the relationships of rivers with their underlying
aquifers. And the spatial scale is even less well-known in its temporal
evolution. This three-dimensional spatial view, with the addition of a fourth
temporal dimension, is the so-called four-dimensional nature of a river
ecosystem (as defined by Ward).
Three-dimensional (longitudinal, transversal, vertical) nature of a river system
Spring at the base of a deposit of glacial origin (Pederù, South Tyrol)
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92
The saline springs of Poiano: the importance of biological markers
The Poiano Springs are the largest
karstic springs in Emilia Romagna (mean
discharge exceeding 400 l/s), and the
main drainage system of groundwater
flowing in the Triassic chalk of the Upper
Val Secchia. Unlike other springs in the
area, the Poiano Springs contain salt,
with concentrations of dissolved sodium
chloride between 5 and 7 g/l. Between
autumn 2005 and spring 2007, the Trias
Project (a research project by the
Società Speleologica Italiana for the
Ente Parco Nazionale dell’Appennino
Tosco-Emiliano) was carried out on the
Poiano aquifer, with automatic
collection of the main environmental
parameters (temperature, electric
conductivity, pH, discharge) and
continual collection of fauna by means
of a net placed at the mouth of the
spring. Geological and hydro-chemical
tests showed that the chalk outcrops
from which the springs gush are the top
portion of a still active diapir, i.e., a
chalk mass intruding vertically upwards
because of its low density, bringing with
it rock-salt, which makes the aquifer
salty. Surface water, which infiltrates a
few kilometres upstream through
swallow holes, takes a few days to
reach and mix with this salty water. This
had led geologists to believe there was
Nitocrella psammophila (left, 100 x), Niphargus poianoi (top, right, 6 x) and Pseudolimnocythere sp.
(bottom, right, 100 x)
Fabio Stoch · Mauro Chiesi
a simple conduit system in the chalk
bedrock, a typical feature of evaporites.
The high content of sodium chloride is a
limiting factor for biodiversity in the
Poiano aquifer. Only three species of
stygobiont crustaceans were collected
from the springs: the harpacticoid
Nitocrella psammophila and the ostracod
Pseudolimnocythere sp., both of ancient
marine origin, and the endemic
amphipod Niphargus poianoi. However,
contrary to previous ideas, biological
research revealed that the conduit
system does not carry to the springs the
stygoxenic and stygobiotic organisms
found in the streams flowing into swallow
holes, none of which were collected in
the Poiano Springs. Besides, the
numbers of harpacticoids and ostracods
coming from the springs are larger in
periods of drought than in periods during
which the aquifer is recharging, which
suggested that the conduit system has a
large groundwater basin. The integration
of geological and biological research
methods therefore enabled scientists to
gain a better hydro-dynamic picture of
the aquifer, and also revealed the
unexpected presence of endemic
species which had colonised the
groundwater in the past and which are
therefore now valuable bioindicators.
Trends (measured during analysis) of discharge, precipitation and numbers of drifted stygobionts in
the Poiano springs
93
■ Ecology of springs
94
Springs are like windows opening
on the underground environment Botosaneanu, a Romenian researcher,
defined them as “the gates to the river
Styx”. They are often the only means
of analysing aquifers, because they are
composed of surfacing groundwater
which filters into recharge zones at
different times, and reach spring
points due to gravity. Springs may
Sulphuric spring: the saline waters of Nirano
therefore be studied from the “outside”
(Emilia Romagna)
to
analyse
surface
organisms
colonising the crenal zone (thus, crenobiology), or from the “inside”, to
examine the fauna of the aquifers supplying them - the stygian zone (thus,
stygobiology).
Springs are particular physical environments which have constant temperature
over time and sometimes undergo changes in the chemical composition of their
waters, due to the nature of the aquifers supplying them. These parameters
define extreme natural situations. For instance, according to their thermic
regime, there are thermal springs (like those in the Euganean Hills (Veneto),
which host an endemic species of gastropods of the genus Heleobia) and
glacial ones (such as those in the Adamello-Brenta, between Lombardy and
Trentino, which are colonised by endemic stygophilic harpacticoid copepods).
Brackish springs are saline (like the Poiano springs in Emilia Romagna, whose
exclusive guest is the stygobiotic amphipod crustacean Niphargus poianoi),
and those with particular values of pH and hydrogen sulphide, i.e., sulphuric
springs, which are found throughout Italy and its islands.
■ Groundwater inhabitants
The perennial underground stream of the Pod Lanisce cave (Julian Pre-Alps, Friuli Venezia Giulia)
The “darkness syndrome”. Contrary to ideas in the past, the underground
environment can host great biodiversity. As described in the previous section,
groundwater species may be divided into stygoxenes, stygophiles and
stygobionts, according to their degree of dependency on this habitat for their
survival.
Stygobionts are species which are exclusive to groundwater and have
developed special adaptations to life in this habitat. All their adaptations
95
96
Modified sensory setae on the antennule of a male harpacticoid (top: ca. 2000x; bottom: ca. 4000x,
photo by SEM, scanning electron microscopy)
define the so-called “darkness
syndrome”, a condition made up of a
series of morphological, physiological
and behavioural changes that these
species underwent during their
evolution in the geological past, which
brought their ancestors from surface
waters to the underground ecokingdom. According to how species
Aesthetasc on antennule of a harpacticoid (ca.
react to the underground environment,
8000x, SEM photo)
adaptations are distinguished from
specialisations. Adaptations are strategies developed by species as
responses to what are called the macrodescriptors of the underground
environment, like constant darkness and scarce organic matter. Specialisation
is the reaction to microdescriptors of the various types of habitats found in the
hypogean environment in general.
Groundwater organisms are depigmented (white, transparent or translucent),
or sometimes pinkish (haematic pigments are visible through their semitransparent bodies), and their visual organs are generally small
(microphthalmy) or totally absent (anophthalmy). Clearly, in totally dark
environments, there is no advantage in having functioning visual organs or
similarly, exhibiting gaudy colours. But it is more complex to understand what
the disadvantages could be in maintaining these characteristics, since these
same disadvantages often caused them to become extinct over time.
Generally speaking, if an organism has a particular feature that is neither an
advantage nor a disadvantage, a random neutral mutation may occur, causing
that feature to disappear. In addition, if there is also an energy advantage,
because during the ontogeny of these structures available energy can be used
to develop compensatory sensory structures, then the loss of useless organs
also has an adaptive logic. Presumably due to lack of resources, no stygobiont
has developed the complex structures typical of animals living in sea abysses
(like bio-luminescence). Moreover, pre-adaptive dynamics cannot be ruled
out: in surface populations made up of both blind and sighted individuals,
spatial segregation of blind phenotypes in groundwater and survival of sighted
individuals in surface water may have given rise, over time, to two different,
ecologically isolated genotypes. However, the evolutionary dynamics that led
stygobionts to lose their eyes are still being discussed, as even within the
same species eyes may show different evolutionary stages - for example, in
some isopod, amphipod and decapod crustaceans.
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98
The lack of eyes or their functional atrophy is generally accompanied by
hypertrophic (excessively developed) alternative sensory organs for life in a
dark world, where smelling or touching the surrounding space is the only way
of sensing the approach of predators or potential prey, finding a partner, or
making one’s way in three-dimensional space, large or small. The body
surfaces of stygobionts are therefore covered with sensory organs, which have
different shapes according to species. For instance, crustaceans have
aesthetascs, setae with many chemoreceptors sensitive to chemical stimuli,
and thigmoreceptors, end-organs which respond to touch and enable
organisms to find their way around by feeling the lake bed or single sand
particles in interstitial environments. Stygobiont crustaceans living in free
water sometimes have longer antennules than their surface relatives. These
modified cephalic appendages are used to sense at distance: it is better to
know in advance if a predator is coming, before it is too late to escape! In
stygobionts, the compensatory length of sensory appendages is contrasted
by clearly rudimentary locomotory appendages, which are much smaller than
those of their close relatives living on the surface, and generally with fewer
segments, setae and spines. This adaptation is actually a type of
specialisation, as it is typical, or even exclusive, to interstitial species.
The interstitial environment of hyporheic zones of rivers, springs and karstic
springs covered by alluvial sediments has one great disadvantage: living
Body elongation favours movement in the interstitial habitat
spaces are restricted. In these narrow habitats, movement is confined, and
walking species, let alone swimmers, are rare. Most of their time is spent
moving around single sand particles, feeding on the bacterial biofilm covering
the surface. Long legs would only hinder movement. This morphological
adaptation is accompanied by a reduction in body size, as stygobiont species
are generally smaller than their surface relatives. It is no coincidence that
shorter legs and smaller bodies are often associated. The most probable
reason is that these adaptations are the result of developmental heterochrony.
Heterochrony. This is a deviation from
the typical developmental sequence of
formation of organs and parts as a
factor in evolution, both in animals
with discontinuous development (with
larval stages separated by moults)
and those with continuous, gradual
transformations into adults.
Although there are various types of
heterochrony, the most commonly
found in underground environments
are progenetic paedomorphosis (also
known as progenesis) and neoteny.
Why has heterochrony been so
successful in the colonisation of
groundwater?
Progenesis is the process by which
Evolutionary dynamics of stygobiont progenesis
features of the sexually mature animal
develop precociously. The result of this deviation is a reproductively mature
adult which preserves the morphological and/or physiological characteristics
typical of juvenile or larval stages. These small adults often look like larvae
and, if they are metameric (segmented) animals or have segmented body
appendages, they may have fewer metameres and segments than they would
if they had developed normally. But what is the advantage of being small?
Obviously, it enables these animals to creep and wriggle into tiny interstitial
spaces. Although heterochrony is the result of modifications - genome
alterations which are generally disadaptive - it actually provides free admission
to interstitial environments. It may therefore be a pre-adaptation, i.e., nonadaptive, and at times a neutral character or set of characters acquired in their
original habitats (i.e., surface water) which may become useful when
99
organisms find themselves in new
environments.
Many
of
the
evolutionary lines in stygobiotic
crustaceans (copepods, ostracods,
bathynellaceans, thermosbenaceans,
asellid isopods, ingolfiellid and
bogidiellid amphipods) originated in
this way.
Another type of heterochrony is
neoteny. The final result is the same:
sexually mature adults that look like
larvae. In this case, the dynamics are
different, because larval development
is so slow that individuals reach
sexual maturity without having
completed their larval development. In
this case, animals may grow to the
Elongation of the first antenna in the amphipod
Hadzia fragilis stochi (ca. 8x)
same size or larger than their nonheterochronic relatives. The classic
example of neoteny in underground environments is provided by the olm.
Stygobiont animals also have physiological adaptations to life underground,
like low metabolic rates and slow body growth, longevity, reduced fecundity,
larger eggs richer in yolk (enabling embryos to survive for longer periods), and
less frequent reproduction, often independent of the season and occurring
throughout the year.
However, like all generalisations, this too has its exceptions. For instance, in
open karstic environments, some Niphargus species depend on the seasons.
In particular, in spring, when aquifers increase their discharge due to
snowmelt, and surface water carries larger amounts of organic matter, the
biological cycle of these animals is timed in order to produce their juvenile
stages which exploit the greater amount of food in order to develop.
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Theoretical evolutionary sequence which, starting from a large surface-living ancestor (1), through
evolutionary steps (2-4), may have led to a progenetic interstitial species (5)
Other adaptive strategies. Another characteristic of all interstitial organisms
is body elongation, which makes even phylogenetically distant taxa acquire a
common worm-like shape (turbellarians, annelids, crustaceans and mites).
The advantage is that their bodies are capable of wriggling into tiny interstices.
Only a few ethological strategies for survival in particular underground
environments are known. In hyporheic habitats, mainly in the upper layers of
river sediments, where current velocity may be considerable, animals without
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adhesive organs to cling to the
sediments may curl around single
particles, to prevent being carried
away by the current. This is the case of
oligochaetes, harpacticoid copepods
and amphipods with elongated
bodies. Others may become globose
(some isopods and amphipods), and
drift with the current to colonise new
habitats.
Another
strategy
adopted
by
crustaceans is gender segregation in
spatial niches, to avoid intraspecific
competition. When sampling a
particular underground environment,
scientists often collect larger numbers
of males or, vice versa, of females. In
Harpacticoid female of Morariopsis aff.
scotenophila with only one egg per sac
addition to the sex ratio, which in
(ca. 100x)
nature is notably in favour of females,
in interstitial environments, males and females may occupy microhabitats at
different depths. Although little is known of the ethology of underground
species, some male copepods occasionally re-clasp (mate with the same
female) to ensure their paternity.
Reproductive strategies. Until recently, the underground ecosystem was
thought to be simple, stable and predictable. In fact, scientific research has
proven this axiom invalid, at least for some habitats.
Generally speaking, in physically predictable but ecologically unfavourable
environments, species adopt a demographic strategy called A-selection
(Adversity Selection), based on slow development and low fecundity in stressful
environments with few resources and predictable changes. However, when
habitats are still physically predictable and food resources are more abundant,
species may turn to K-selection strategy, whereby populations grow to the
carrying capacity of the environment. In this condition, intraspecies competition
and predation may also become important for population dynamics. When
environments are physically unpredictable but provide great food resources,
there may be exponential population growth followed by plummeting figures
when resources are no longer available: this is known as r-selection. Clearly, a
single model cannot be applied to all underground species.
■ The food-chain
A classic description of underground environments is generally made by
comparing its physical and biological organisations with those of surface
environments. For example, groundwater is permanently dark and has no
nyctemeral (day-night) cycle, whereas surface water is illuminated by the sun,
and therefore does have a day-night cycle. This condition influences the
biological and, equally importantly, the energy characteristics of the
ecosystem. Lack of light results in detritus food-chains because there are no
photosynthetic organisms (green plants) and very few chemo-autotrophic
organisms (ones feeding on oxidised inorganic chemical compounds). These
are bacteria that exploit chemical energy instead of light energy, and
synthesise organic compounds from carbon dioxide. One of the typical
locations is the Movile Cave (Romania), where these organisms are primary
producers and the entire food-chain relies on them. There are also examples in
Italian groundwater, an underground stream in the Grotte di Frasassi (Marches)
and sulphuric basins in the Grotta del Fiume Sotterraneo in the Lepini
mountains (Latium), which are still being studied.
Therefore, with very few exceptions, the entire groundwater ecosystem is
not self-sufficient, but depends on inputs of organic matter from terrestrial
Sulphur spring in the cave of Cala Fetente (Capo Palinuro, Campania)
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Sketch showing degrading phases of particulate organic matter (POM) and its entry into the hyporheic
environment (see text for abbrevations)
and aquatic surface environments - defined by the French researcher Rouch
as “epigean manna”. Due to the often total absence of primary producers,
the aquatic underground environment is oligotrophic, i.e., deficient in
nutrients and, as such, incapable of supporting long food-chains. There are
only a few examples of dystrophic underground environments, which are
periodically or occasionally filled with dissolved humic matter coming from
the surface.
Eutrophic conditions are associated with sudden increases in organic matter
due to pollution. This happens in some saturated karstic habitats in periods of
intense rainfall. Rain and surface organic matter percolate into aquifers
through effective infiltration pathways, giving rise to large-scale although
short-lived increases in organic matter available to biota. Similar events occur
in unsaturated karstic environments, such as concretions and pools of
trickling water in springs or hyporheic habitats, where the quantity of organic
matter depends on the season. Clearly, the type of aquifer greatly affects the
amounts of food available to underground communities, and may produce
distinct community organisations.
Most underground organisms are therefore detrivorous and feed on particles of
organic matter produced by the decomposition of dead animal and plant
organisms. This ingested matter is divided into two categories: Coarse
Particulate Organic Matter (CPOM), with particles >1 mm, and Fine Particulate
Organic Matter (FPOM), with particles <1 mm and >0.5 µm. Occasionally, some
small organisms may feed on Dissolved Organic Matter (DOM) with particle
sizes <0.5 µm, composed of proteins, aminoacids and simple sugars. Most
interstitial organisms feed on bacterial biofilm made up of bacteria and fungi
that provide proteins, fats and sugars, vitamins and oligo-elements. Bacterial
biofilms develop on the surface of single sediment particles, exploiting the
dissolved organic matter coming from the exterior; most bacteria are also
heterotrophs (consumers). Several crustaceans and oligochaetes are
limnivorous, because the inert matrix of silt - the finest soil fraction - traps the
bacteria and organic matter on which these animals feed.
Interstitial and karstic environments share the same predators, like copepods,
cirolanid isopods, many amphipods, decapods, and olms. Cannibalism is not
rare, and adults prey on their young - a process which may be used to keep
demographic growth under control. In the surface water/groundwater ecotone
and in underground environments rich in stygoxenes, there may be many
hydrozoans, larvae of tanypodine chironomids and other insects that prey on
copepods and amphipods, and microturbellarians, whose flat, diaphanous,
transparent bodies show the prey (generally small copepods) that they have
swallowed whole.
Pools in Grotta dell’Acqua (Trieste Karst, Friuli Venezia Giulia)
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Functional redundancy is a rare
phenomenon in groundwater ecosystems, i.e., each trophic role is
generally played by one or a few
species, and there is little competition
at each link of the food-chain.
For the same reason, the ecosystem is
certainly extremely vulnerable, as
communities have low inertia (capacity
for withstanding human disturbance
unaltered). In fact, the extinction of one
species of the community may bring
the entire food-chain to a halt, with
irreversible consequences for the
whole ecosystem. Many underground
species are therefore “key species”, as
conservationist biologists call them.
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Groundwater in a Tuscan cave
■ Stygodiversity: groundwater biodiversity
Hierarchical approach to the study of underground ecosystems: from large regional to small microhabitat scales
Several factors contribute towards the spatial and temporal distributions of
the so-called stygodiversity, and they may be both historical (palaeoclimatic,
palaeogeographical and palaeoecological events) and ecological. The
structure and functioning of underground aquatic ecosystems are the result of
complex processes that may act in different ways at different spatial - and
temporal - levels. These factors are therefore studied at continental or regional
scale (mega- or macro-scale), aquifer (meso-scale) and microhabitat level
(micro- or fine-scale). These scales are a series of spatial configurations fitting
one into the other, and each level integrates the processes occurring at lower
levels and is associated with others at the same level. This hierarchical
subdivision into continental, regional, and sometimes aquifer levels allows us
to focus on the palaeogeographical and palaeoclimatic events that influenced
the origin of biodiversity in groundwater.
The origin of stygobionts in fresh groundwater is double. Some of them evolved
from ancestors living in continental surface freshwater (lakes and rivers) - most
hydrobiid gastropods, cyclopoid copepods and many canthocamptid
harpacticoids, asellid isopods, niphargid amphipods and olms - and are called
limnicoid stygobionts. Others - polychaetes, parvidrilid oligochaetes,
amphipods of the genera Hadzia and Salentinella, microcerberid,
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Stygodiversity in the Presciano springs: a pilot experiment
The Presciano springs make up one of
the three great sources giving rise to the
river Tirino in Abruzzi, at the foot of the
greatest karstic aquifer in the
Apennines. They have proved to be
excellent natural laboratories for
scientific research on the environmental
factors affecting the spatial distribution
of groundwater species (the spring area
does not exceed 2000 m2).
This spring system is structurally
complex, as a heterogeneous alluvial
layer lies on strongly karstified bedrock,
covering the underlying karstic aquifer.
This situation has enabled researchers
to examine how the different types of
sediments affect the composition of
underground communities.
Detailed samplings have revealed that
stygoxenic, stygophilic and stygobiont
species are not at all homogenously
distributed in the small spring area
Presciano springs (Abruzzi)
As depth increases, the relative
importance of stygobionts increases to
the detriment of other ecological
categories, while stygophiles are
generally found at intermediate depths
(at 30 and 70 cm below the spring bed).
This vertical distribution is a direct
consequence of the ecological
characteristics of stygobionts, which are
morphologically and physiologically
adapted to life in deep habitats, and of
stygophiles, a transitional category that
clearly prefers ecotonal areas.
Stygoxenes are scattered, especially in
subsurface sites, perhaps restricted by
the low temperatures and oligotrophic
conditions of the spring environment.
Further analysis, carried out by
dividing fauna living in karstic sites from
that of alluvial sites, shows that
stygophiles are almost exclusively
found in the latter habitat.
Diana Maria Paola Galassi · Barbara Fiasca
In addition, alluvial sites characterized
by heterogeneous grain-size
composition, with clearly alternating
temporal upwelling and downwelling
phases, host greater biodiversity, as
they provide more ecological niches
than karstic sites, and contain greater
quantities of organic matter, which is
trapped in interstices.
Copepod taxocoenoses, the most
important group in the analysed springs,
are found in alluvial sites, with 15 out of
the 17 species collected in the entire
spring system. Instead, karstic sites
host more monotonous karstic fauna,
with one harpacticoid copepod
(Nitocrella pescei) making up 90% of
the entire assemblage. However, it is
precisely in karstic sites that we find the
most biogeographically interesting
species, Pseudectinosoma reductum, a
relict of ancient marine origin.
Nitocrella pescei
Distribution of ecological categories (number of
specimens) at various depths (in cm)
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microparasellid and cirolanid isopods, ameirid and ectinosomatid harpacticoids
and mysids - are related to taxa that are still living in marine environments and
are called thalassoid stygobionts. The current distribution of stygobiont species
is the result of an ever-changing mosaic of communities which have evolved on
a geological time-scale and whose composition is still evolving.
A particularly interesting aspect of the development of stygodiversity, which
has long been debated by scientists, is the large number of relict species in
underground communities. Some underground systems conserve species and
even entire taxonomic groups related to now extinct ancient surface fauna (in
one of his books, the French biologist René Jeannel spoke of cave-dwelling
“living fossils”). Events like the Pleistocene glaciations, sea regressions and
transgressions, and the salinity crisis of the Mediterranean have long been the
focus of scientific debates on the origin of underground fauna.
Some scientists believe stygobionts to be the “survivors” of surface
populations which had taken refuge underground to escape harsh surface
conditions (this “refugium” hypothesis goes back to the ideas of Charles
Darwin). Others view colonisation as a continuous, ongoing process (the
“active colonisation” hypothesis).
Karstic spring (Friuli Venezia Giulia)
According to the “refugium” theory,
tropical regions, which were not
affected by catastrophic events, would
have scarce underground fauna; most
importantly, surface populations, the
ancestors of stygobionts, would
generally have become extinct in
geographical areas which underwent
drastic climatic changes.
Further knowledge has proved that
both these theories were partly wrong,
and suggested a new evolutionary
scenario, according to which the
present structure of stygodiversity has
several causes. First, the extinction of
surface populations is not a mandatory
prerequisite
for
speciation
in
The endemic gastropod Bythiospeum calepii
underground habitats. We already
mentioned this when describing the coexistence of pigmented, eyed species
of crustaceans with depigmented, anophthalmic or totally blind ones - many
cases are known in Italy, especially for crustaceans of the genera Proasellus,
Synurella and Gammarus. These are examples of ongoing active colonisation
of groundwater not associated with dramatic changes in the surface
environment. Stygobionts have also been found in all kinds of habitats in
tropical areas - lava tubes on volcanic islands, cenotes in Mexico, caves in
Somalia, anchialine systems in Australian deserts and in the caves of small
islands in the Caribbean, and in Brazilian caves, inhabited by multitudes of
blind fish - thus definitively contradicting the “refugium” hypothesis as the only
explanation for the origin of underground communities.
Although groundwater colonisation may occur independently of unfavourable
conditions in the environments lying above, dramatic climatic and geological
changes in surface habitats may in fact suddenly interrupt the genetic flow
between hypogean and epigean populations. This explains the origin of
“relicts”, both eco-geographical (separated from their closest surface relatives still living and sometimes well diversified) and phyletic (the last survivors of a
now extinct surface evolutionary line).
Phyletic relicts are very interesting from the scientific viewpoint. Entire
taxonomic groups (like bathynellaceans and thermosbaenaceans) belong to
this category, and their closest relatives can no longer be found among the
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animal groups still living on the surface. However, since the chronology of
colonisation and speciation is hard to establish, a solution has been found in
the so-called “molecular clocks”, which synchronise DNA mutations in living
organisms with palaeogeographical and palaeoclimatic events. An example is
afforded by the examination of Sardinian, Provençal and Tuscan species of
stenasellid isopods, living evidence of the ancient tectonic fragmentation of
the Tyrrhenian plate and drifting of the Sardinian-Corsican continental plate
and its fragments from what is now Provence towards present-day Italy.
Although necessary for speciation, vicariance (i.e., the splitting of the area of
the old species into two parts separated by boundaries) is not only associated
with these ancient, wide-ranging events, and may occur on any scale, from
small, isolated fractures in karstic systems, to continents. Vicariant events may
be geoclimatic and ecological: obviously, the efficiency of these “boundaries”
is closely related to the ecology of the species, especially their aptitude for
dispersal. Many stygobiont species are not prone to dispersal, and show
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Niphargus similis, found in relict sites in glacialised areas of the Alpine chain
Affinities between Provençal, Sardinian-Corsican and coastal Tyrrhenian fauna are explained by their
common palaeogeographic history
limited geographic distribution (they are strict endemics). Furthermore, the low
fecundity, benthic larval development and low dispersal potential of many
interstitial crustaceans suggest that continuous and jump dispersal are quite
rare in these groups. This is why stygobionts can be used as excellent
historical (palaeogeographical) indicators, their descriptive capacity being
similar to that of true fossils.
Among the events that modelled present-day Italian stygofauna, the best
known are certainly glaciations and sea regressions. The Quaternary
glaciations depleted underground fauna in large areas of Italy, thus leading to
the total absence of entire stygobiont genera of gastropods, copepods,
isopods and amphipods north of the boundary of the Würmian glaciation. Sea
regression, associated with glacial eustatism, trapped several taxa in coastal
sediments, giving rise to stygobization. Very ancient regressive events led
fauna of marine origin to become relicts, enigmatically confined and unevenly
distributed in continental groundwater far from coastlines (amphi-Atlantic,
Caribbean-Mediterranean, Caribbean-Mediterranean-Australian). In this case,
the grandiose movements of plate tectonics were the main cause of
relictualisation and, in the Mediterranean area, gave rise to the so-called
Tethyan relicts, which date back to the disappearance of the ancient Tethys
Sea in the Oligocene.