Despite its inhospitable appearance and lack of any ... - Udine Cultura
Despite its inhospitable appearance and lack of any ... - Udine Cultura
Despite its inhospitable appearance and lack of any ... - Udine Cultura
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Fauna<br />
FABIO STOCH<br />
<strong>Despite</strong> <strong>its</strong> <strong>inhospitable</strong> <strong>appearance</strong> <strong>and</strong><br />
<strong>lack</strong> <strong>of</strong> <strong>any</strong> sign <strong>of</strong> life at first sight,<br />
groundwater is populated by large<br />
numbers <strong>of</strong> animal species <strong>of</strong> various<br />
taxa. These animals are generally very<br />
small, even tiny (between three-tenths<br />
<strong>of</strong> a millimetre to one centimetre). Only a<br />
few exceed one centimetre, <strong>and</strong> even<br />
fewer are quite big, like the underground<br />
prawns <strong>of</strong> the genus Typhlocaris or the<br />
olm (Proteus anguinus).<br />
Larva <strong>of</strong> stygoxene chironomid<br />
● Stygoxenes. Not all organisms found in groundwater are exclusive to it: in<br />
fact, m<strong>any</strong> <strong>of</strong> them are typical <strong>of</strong> surface environments <strong>and</strong>, through either<br />
active or passive dispersion, accidentally penetrate underground. They are<br />
therefore occasional guests in this habitat, to which they are generally carried<br />
by water percolating from the surface. This situation is very frequent in surface<br />
<strong>and</strong> underground karstic aquifers, with infiltration passages which are very<br />
efficient (sinkholes) or slower (like micro- <strong>and</strong> macro-fissures in limestone).<br />
The accidental guests occurring in groundwater are called stygoxenes. They<br />
do not have adaptations enabling them to survive in the harsh underground<br />
environment, where food supply is more restricted than in their habitat <strong>of</strong><br />
origin. However, in particular conditions - for example if the aquifer is<br />
organically polluted - stygoxenes find optimal conditions for their survival <strong>and</strong><br />
may even reproduce in hypogean (underground) habitats. Their populations<br />
may be quite large <strong>and</strong> compete with local ones, to the point <strong>of</strong> replacing them<br />
completely. They may also play important roles as prey or predators <strong>of</strong><br />
underground species.<br />
● Stygophiles. Stygophiles are organisms that exhibit some adaptation to life<br />
in groundwater environments, <strong>and</strong> may reproduce in both surface <strong>and</strong><br />
underground waters. Stygophiles live within surface water-groundwater<br />
interfaces like springs, humid soil, wood litter <strong>and</strong> moss. These habitats share<br />
several characteristics with the underground environment, in particular<br />
darkness <strong>and</strong> limited living space. This is why stygophiles <strong>of</strong>ten have pre-<br />
Monolistra schottlaenderi (top) <strong>and</strong> Monolistra racovitzai (crustacean isopods, 7x)<br />
41
42<br />
adaptive features to life underground, which enable them to survive in<br />
transitional environments: they are <strong>of</strong>ten partially or totally depigmented <strong>and</strong><br />
have reduced or totally absent visual organs. From the evolutionary viewpoint,<br />
since groundwater is a secondary colonisation environment, the species now<br />
found exclusively here are thought to have been stygophiles in the past. But<br />
the contrary cannot be ruled out - i.e., that all past stygophiles are now<br />
exclusive groundwater dwellers. Evolutionary destiny depends on the<br />
opportunities which single stygophilic species had <strong>of</strong> colonising groundwater,<br />
surviving <strong>and</strong> successfully reproducing.<br />
Stygophiles which regularly frequent the subterranean environment where they<br />
can reproduce, but which do not have marked adaptive characteristics, are<br />
called substygophiles. They include, for instance, some aquatic benthic insects<br />
found in watercourses, where they may spend the early phases <strong>of</strong> their<br />
development in the fluvial hyporheic environment. This is a winning adaptive<br />
strategy as regards avoiding predators, but their life-cycle is always completed<br />
in shallow waters, <strong>and</strong> adults <strong>of</strong>ten inhabit the subaerial habitat. This is true <strong>of</strong><br />
m<strong>any</strong> ephemeropterans, plecopterans <strong>and</strong> dipterans, mainly chironomids.<br />
Conversely, those stygophiles which show not only marked pre-adaptations<br />
but also an elective preference for the subterranean environment, where they<br />
are regular guests, are called eustygophiles. This is the case <strong>of</strong> m<strong>any</strong> molluscs<br />
<strong>and</strong> crustaceans.<br />
Paracyclops imminutus (stygophyle)<br />
● Stygobionts. Animal species closely associated with underground<br />
environments, on which they depend for completing their life-cycle, are called<br />
stygobionts. They <strong>of</strong>ten have marked adaptations to underground life like<br />
depigmentation, anophthalmy (absence <strong>of</strong> eyes), well-developed sensory<br />
organs, <strong>and</strong> a reduced fecundity rate (described in the chapter on the<br />
ecological aspects <strong>of</strong> groundwater). These adaptations are partially shared by<br />
terrestrial troglobionts (cave-dwelling species) <strong>and</strong> by those living in soil<br />
(endogean species). Stygobionts may be ubiquitous <strong>and</strong> live in all types <strong>of</strong><br />
aquifers, <strong>and</strong> sometimes in marginal waters (for instance, under dead leaves in<br />
humid forests), or they may be associated with specific habitats, like<br />
phreatobionts, which live exclusively in saturated alluvial aquifers, <strong>and</strong> karstic<br />
stygobionts, which are limited to aquifers in limestone <strong>and</strong> evaporites.<br />
A clear distinction between these ecological categories is difficult to make,<br />
<strong>and</strong> there are m<strong>any</strong> intermediate levels. In some taxa, <strong>of</strong> which all species<br />
appear to be pre-adapted to life in humid soil <strong>and</strong> groundwater, like<br />
nematodes <strong>and</strong> some families <strong>of</strong> oligochaetes, it is impossible to divide them<br />
according to morphology, <strong>and</strong> their preference for underground habitats is<br />
evident from the frequency with which they are found there.<br />
This chapter on groundwater fauna describes exclusive dwellers, i.e.,<br />
stygobionts. We will discover a fascinating multitude <strong>of</strong> dark-loving organisms,<br />
with sometimes bizarre morphological adaptations.<br />
Niphargus steueri (stygobiont)<br />
43
44 45<br />
Methods for sampling <strong>and</strong> analysing groundwater fauna<br />
Fabio Stoch<br />
Groundwater habitats are difficult to<br />
reach, <strong>and</strong> researchers have had to<br />
come up with ingenious methods for<br />
sampling <strong>and</strong> analysing underground<br />
fauna which, according to the depth <strong>and</strong><br />
accessibility <strong>of</strong> aquifers, are sometimes<br />
expensive <strong>and</strong> so complex that only<br />
specialised research institutes can carry<br />
them out.<br />
In karstic waters, traditional sampling<br />
methods include:<br />
● continuous filtering <strong>of</strong> trickling water<br />
funnelled into containers with filters<br />
which are periodically emptied;<br />
● collection <strong>of</strong> percolating water in<br />
gours <strong>and</strong> micro-gours, by means <strong>of</strong><br />
rubber pumps or syringes;<br />
filtering <strong>of</strong> concretion water with<br />
plankton nets (60-100-µm mesh) which<br />
are emptied with rubber piping;<br />
● direct filtering <strong>of</strong> water from large<br />
pools with plankton nets with h<strong>and</strong>les;<br />
● in streams <strong>and</strong> small watercourses:<br />
after coarse debris has been shaken out,<br />
water is filtered through plankton nets<br />
(with semi-circular openings 20-25 cm in<br />
diameter);<br />
● direct collection <strong>of</strong> large organisms<br />
with aquarium nets <strong>and</strong> tweezers;<br />
● in order to collect large predatory<br />
crustaceans (1), traps containing meat or<br />
tid-b<strong>its</strong> <strong>of</strong> food can be placed in suitable<br />
positions in open cans (to avoid the<br />
death <strong>of</strong> animals trapped inside, if the<br />
trap <strong>its</strong>elf is lost);<br />
● placing artificial substrates (twisted<br />
nylon netting compressed in tubes, or<br />
tubes filled with locally collected washed<br />
sediment) which are periodically emptied<br />
in order to analyse the colonisation <strong>of</strong><br />
various types <strong>of</strong> substrates.<br />
Collecting specimens from wells or<br />
boreholes in alluvial soils may be carried<br />
out with:<br />
● modified plankton nets (Cvetkov nets)<br />
with valves to prevent material from<br />
escaping when the nets are quickly lifted<br />
<strong>and</strong> replaced on the bottom <strong>of</strong> the well<br />
to agitate the sediments (2);<br />
● various types <strong>of</strong> pumps (peristaltic,<br />
rotor, compressed-air), according to<br />
water-table depth (rotor pumps <strong>of</strong><br />
greater power unfortunately easily<br />
destroy material).<br />
Lastly, in flooding watercourses where<br />
collection is concentrated in upwelling or<br />
outwelling stretches (see chapter on<br />
ecology), two methods are used:<br />
● Karaman-Chappuis method: a hole is<br />
dug along the shore <strong>of</strong> a watercourse,<br />
<strong>and</strong> the water permeating from nearby<br />
sediments is collected <strong>and</strong> filtered<br />
through a plankton net;<br />
● Bou-Rouch method: a h<strong>and</strong>-pump (3)<br />
is used to remove interstitial water from<br />
the bed <strong>of</strong> a watercourse, by means <strong>of</strong> a<br />
Filtering trickling water with a plankton net Equipment for sample collection<br />
1<br />
2<br />
perforated tube inserted deeply into the<br />
sediments (for a detailed description <strong>of</strong><br />
this method, see Teaching Suggestions).<br />
Research teams with the most recent<br />
equipment can use drills to place<br />
piezometers at varying depths, from<br />
which groundwater is extracted with<br />
pumps <strong>and</strong> filtered through plankton<br />
nets.<br />
Other, quite expensive methods, like<br />
freeze-coring, use liquid nitrogen to<br />
freeze sediment cores collected from<br />
boreholes <strong>and</strong> subsequently examined<br />
in the laboratory.<br />
More advanced research methods<br />
involve inserting transparent perspex<br />
piezometers with optical-fibre videocameras<br />
into the soil or sediment in the<br />
river bed. In this way, researchers can<br />
analyse large organisms in their natural<br />
environment without disturbing the<br />
underground community.<br />
3
46<br />
■ Poriferans<br />
Among all stygobionts, sponges are certainly the least frequent <strong>and</strong> most<br />
primitive. These essentially marine organisms (there are few freshwater<br />
species belonging to the spongillid family) frequently colonise coastal caves<br />
shrouded in partial darkness. There is, however, at least one exception to this<br />
rule: Higginsia ciccaresei, a sponge which has recently been collected by<br />
scuba divers exploring the Zinzulusa Grotto in the Salento (Apulia). The<br />
species is endemic to the cave, <strong>and</strong> was found at a distance <strong>of</strong> 250 m from <strong>its</strong><br />
entrance, at a depth <strong>of</strong> 12 m, in total darkness. The morphological<br />
characteristics <strong>of</strong> this species, like <strong>its</strong> depigmentation, have led researchers to<br />
consider it a stygobiont.<br />
■ Platyhelminthes<br />
Flatworms are a primitive phylum <strong>of</strong><br />
free-living or parasitic organisms.<br />
Stygobiont planarian worms are<br />
Atrioplanaria morisii<br />
generally depigmented, eyeless, with<br />
slow reproductive cycles <strong>and</strong> high<br />
numbers <strong>of</strong> chromosomes.<br />
In Italy, although very little is known<br />
about these organisms living in<br />
phreatic environments, which are<br />
certainly inhabited by m<strong>any</strong> minute<br />
creatures (micro-turbellarians), some<br />
species living in karstic waters are well<br />
documented. Dendrocoelum collinii lives in pre-Alpine caves <strong>and</strong> in France,<br />
<strong>and</strong> D. italicum in Lombard caves, although the taxonomic position <strong>of</strong> Italian<br />
populations <strong>of</strong> both species requires revision. The genus Atrioplanaria is found<br />
in caves in Sardinia, central-southern Italy (A. racovitzai) <strong>and</strong> southern<br />
Piedmont (A. morisii); Polycelis benazzii lives in Ligurian caves. The taxonomy<br />
<strong>of</strong> these genera is uncertain, due to the fact that it requires examination <strong>of</strong><br />
living specimens <strong>and</strong> the use <strong>of</strong> complex histological <strong>and</strong> karyological<br />
methods. This is why these animals are seldom included in lists <strong>of</strong> fauna.<br />
However, being predators, their trophic role in underground ecosystems may<br />
be <strong>of</strong> local importance.<br />
The taxon <strong>of</strong> temnocephalid flatworms is <strong>of</strong> uncertain position. These<br />
ectoparasitic species sometimes abound on the gills <strong>of</strong> crustaceans like<br />
stygobiont amphipods <strong>and</strong> decapods, whose haemolymph they suck. Very<br />
small (2 mm maximum), these animals have tentacles <strong>and</strong> adhesive discs with<br />
which they attach themselves to their hosts. In Italy, only three genera have<br />
been found so far (Bubalocerus, Scutariella, Troglocaridicola); they are<br />
parasitic on stygobiont shrimps <strong>of</strong> the genus Troglocaris which live in<br />
saturated karstic waters in the Karst areas <strong>of</strong> Trieste <strong>and</strong> Gorizia.<br />
■ Molluscs<br />
All Italian stygobiont molluscs belong<br />
to the gastropod class, in particular to<br />
the hydrobioidean superfamily (spring<br />
snails). Although they are common in<br />
Italian groundwater, with about 70<br />
species described, <strong>and</strong> are found in all<br />
types <strong>of</strong> habitats - except for the<br />
vadose zone <strong>of</strong> karstic aquifers - spring<br />
snails are still little known from the<br />
taxonomic viewpoint. This is because<br />
m<strong>any</strong> species are only known by their Hadziella ephippiostoma<br />
shells, which are found in springs <strong>and</strong><br />
hyporheic water, suggesting that the elective habitat <strong>of</strong> these populations is the<br />
deep, almost inaccessible underground environment. M<strong>any</strong> empty shells are<br />
found in river sediments, <strong>and</strong> therefore their unknown underground habitat<br />
may in fact be very far from where they were actually found. This is why their<br />
genera <strong>and</strong> species described in the past need to be revised.<br />
The shells <strong>of</strong> spring snails have various shapes. They are generally towershaped,<br />
conical <strong>and</strong> cylindrical, <strong>of</strong>ten truncated. Some genera have disc- <strong>and</strong><br />
spiral-shaped shells. Stygobiont species <strong>of</strong> spring snails are usually very small<br />
(for example, the adults <strong>of</strong> the genus Hauffenia have a diameter <strong>of</strong> 2 mm <strong>and</strong><br />
are only 0.7 mm high). The opening <strong>of</strong> the shell is generally large <strong>and</strong> round,<br />
closed with a thin, horny, egg-shaped lid, the operculum, which protects the<br />
s<strong>of</strong>t tissues <strong>of</strong> these animals. They move by means <strong>of</strong> a complex set <strong>of</strong><br />
muscles, the foot, which flattens ventrally <strong>and</strong> adheres to the substrate<br />
allowing the snails to crawl. Stygobiont spring snails feed on micro-particles <strong>of</strong><br />
organic matter, encrusting micro-organisms <strong>and</strong> bacterial bi<strong>of</strong>ilms, which are<br />
scraped <strong>and</strong> ground by their radula, an organ bearing several rows <strong>of</strong> minute<br />
teeth. Except for a few species living in brackish water, most Italian spring<br />
snails live in freshwater <strong>and</strong> are crenobionts (spring-loving) or stygobionts.<br />
47
48<br />
Shells <strong>of</strong> gastropods Iglica vobarnensis, Paladilhiopsis virei <strong>and</strong> Hauffenia subpiscinalis (from top to<br />
bottom, ca. 30x)<br />
Crenobiont species (genera Bythinella <strong>and</strong> Graziana) may enter groundwater<br />
bodies <strong>and</strong> burrow into interstices, probably in search <strong>of</strong> food, <strong>and</strong> therefore<br />
behave as stygophiles. A large number <strong>of</strong> endemic species <strong>of</strong> the genera<br />
Bythiospeum, Iglica, Istriana, Hadziella, Paladilhiopsis <strong>and</strong> Phreatica are<br />
strictly stygobiont, <strong>and</strong> live deep within karstic <strong>and</strong> alluvial underground<br />
networks in northern Italy. Some species, living in Alpine-Dinaric areas, are<br />
exclusive to the eastern Pre-Alps <strong>and</strong> are <strong>of</strong>ten strict endemics (like<br />
Paladilhiopsis robiciana, Phreatica bolei, Hauffenia tellinii <strong>and</strong> Belgr<strong>and</strong>ia<br />
stochi). The area with the fewest species is the Piedmont Alps, with some<br />
endemic species <strong>of</strong> the genera Alzoniella, Iglica <strong>and</strong> Pseudavenionia. The<br />
Apennines host a small number <strong>of</strong> local endemics <strong>of</strong> the genera Pezzolia,<br />
Alzoniella, Pauluccinella, Orientalina, Fissuria <strong>and</strong> Islamia. Exclusive inhabitants<br />
<strong>of</strong> Sardinia are the genera Sardhoratia <strong>and</strong> Sardopaladilhia. Sicily hosts only<br />
one crenobiont species, Islamia cianensis. Thermal waters contain particular<br />
species <strong>of</strong> Bythinella <strong>and</strong> Belgr<strong>and</strong>ia.<br />
■ Polychaetes<br />
Polychaete worms are generally sea animals, <strong>and</strong> only a few species colonise<br />
anchialine coastal waters (l<strong>and</strong>-locked bodies <strong>of</strong> water with a subterranean<br />
connection to the sea), <strong>and</strong> even fewer species are adapted to underground<br />
freshwater. Among them are two stygobiont species <strong>of</strong> great biogeographical<br />
interest.<br />
The nerillid Troglochaetus beranecki is an ancient thalassoid species (that is,<br />
one with marine affinities) originating from members <strong>of</strong> psammon in Tertiary<br />
epicontinental seas, from which it invaded underground freshwater. The<br />
characteristic <strong>of</strong> this species is <strong>its</strong> vast distribution area. In Europe,<br />
Troglochaetus beranecki is found in large rivers (Rhone, Garonne, Rhine,<br />
Weser, Danube, Oder, Elbe), in Finl<strong>and</strong> <strong>and</strong> in Alpine streams. It has also<br />
been found in interstices in river beds <strong>of</strong> Colorado <strong>and</strong> Montana (up to 3050<br />
m), although further molecular analyses are required to establish whether all<br />
these populations are really conspecific. Fewer numbers are found in caves<br />
<strong>of</strong> Switzerl<strong>and</strong>, Germ<strong>any</strong>, Pol<strong>and</strong>, Hungary <strong>and</strong> Romania. In Italy, the species<br />
has recently been found in interstitial environments (Trentino) <strong>and</strong> in caves<br />
(Lessini Hills <strong>and</strong> Carnic Pre-Alps). This distribution is very wide, <strong>and</strong><br />
includes ice-covered areas where underground fauna is minimal if not totally<br />
absent, <strong>and</strong> the rare stygobiont organisms have a remarkable capacity for<br />
adaptation, which enabled them to colonise these areas in post-glacial<br />
periods.<br />
49
50<br />
Alkaline waters in karstic caves in Gorizia <strong>and</strong> Trieste host the second Italian<br />
stygobiont polichaete, Marifugia cavatica. It belongs to the serpulids, which<br />
are marine polychaete worms living in limestone tubules. Marifugia cavatica,<br />
probably a micro-filterer, forms dense colonies that occasionally carpet<br />
extensive areas <strong>of</strong> walls <strong>of</strong> underground streams with tubules up to 1 cm<br />
long. The Marifugia formation is a little-known microhabitat rich in micr<strong>of</strong>auna<br />
(protozoans, gastropods, oligochaetes, copepods, isopods <strong>and</strong><br />
amphipods) that populates, like the colonies <strong>of</strong> marine serpulids, the complex<br />
mosaic <strong>of</strong> spaces between tubules. The species lives in the Dinaric region as<br />
far as Albania, together with other species <strong>of</strong> ancient marine origin, like<br />
isopods <strong>of</strong> the genus Sphaeromides <strong>and</strong> amphipods <strong>of</strong> the genus Hadzia, <strong>of</strong><br />
probable Tertiary origin.<br />
■ Oligochaetes<br />
Oligochaetes are freshwater <strong>and</strong> marine terrestrial annelids whose bodies are<br />
made up <strong>of</strong> segments (metameres) without appendages, with rows <strong>of</strong><br />
transversal, movable bristles (setae). The shape <strong>and</strong> distribution <strong>of</strong> the setae<br />
play an important role in the taxonomy <strong>of</strong> this group. Earthworms are usually<br />
detrivorous <strong>and</strong> microphagous, <strong>and</strong> colonise microhabitats rich in organic<br />
matter. In Italian groundwater, the most common are the lumbriculid <strong>and</strong><br />
Troglochaetus beranecki (ca.50x) Cernosvitoviella sp. (ca. 40x)<br />
tubificid families, together with the aquatic <strong>and</strong> semi-aquatic species <strong>of</strong><br />
enchytraeids.<br />
The identity <strong>and</strong> similarity <strong>of</strong> groundwater oligochaetes have only recently been<br />
partially established, <strong>and</strong> research is beginning. The main problem in defining<br />
an oligochaete as stygobiont lies in the fact that m<strong>any</strong> surface species (living in<br />
sediments <strong>of</strong> surface water <strong>and</strong> sometimes in humid soil) are pre-adapted to<br />
life in hypogean habitats (they are depigmented <strong>and</strong> anophthalmic). It is<br />
common practice to define as stygobiont those species which, as far as is<br />
known today, have exclusively been found in groundwater.<br />
The parvidrilid family is certainly the most interesting among the taxa recently<br />
found in Italy, from the Pre-Alps to Sardinia. So far, all records have been ascribed<br />
to the same species, Parvidrilus spelaeus. They are exclusive inhabitants <strong>of</strong><br />
vadose zones in Italian caves, where they colonise the silty, muddy sediments on<br />
the bottom <strong>of</strong> concretions, pools <strong>of</strong> trickling water <strong>and</strong> interstices <strong>of</strong> hypogean<br />
streams. Presumably, the family has an ancient marine origin.<br />
Among the numerous species <strong>of</strong> tubificids found in Italian groundwater, there<br />
are the genera Haber (H. monfalconensis in springs <strong>of</strong> the Julian Pre-Alps <strong>and</strong><br />
Trieste Karst, <strong>and</strong> H. zavreli in groundwater in Umbria <strong>and</strong> Emilia Romagna),<br />
two endemics <strong>of</strong> the genus Rhyacodrilus, recently described (R. gasparoi in<br />
Pre-Alpine caves <strong>and</strong> R. dolcei in small concretions <strong>of</strong> the Trieste Karst),<br />
Tubifex pescei, in phreatic waters <strong>of</strong> Umbria <strong>and</strong> Marches, Abyssidrilus cuspis,<br />
51
52<br />
collected in phreatic waters in Umbria <strong>and</strong> caves <strong>of</strong> Liguria <strong>and</strong> Friuli Venezia<br />
Giulia, Sketodrilus flabellisetosus in the Trieste Karst, <strong>and</strong> Aktedrilus ruffoi,<br />
recently described on specimens found in interstitial environments <strong>of</strong> the river<br />
Tione (Verona).<br />
Enchytraeids are less well-known, <strong>and</strong> several species <strong>of</strong> Cernosvitoviella, found<br />
in Pre-Alpine caves <strong>and</strong> considered to be stygobionts, are still being examined.<br />
■ Ostracods<br />
Ostracods (from the Greek ostrakon, shell) are a diversified group <strong>of</strong> small<br />
crustaceans, whose body is enclosed by a bivalve carapace made <strong>of</strong> calcite,<br />
their unmistakable characteristic. Their carapace may be egg-, bean- or<br />
trapezoid-shaped, <strong>and</strong> is <strong>of</strong>ten knobbly or dimpled. The number <strong>and</strong> shape <strong>of</strong><br />
their appendages is generally the same.<br />
Freshwater species have eight pairs <strong>of</strong> appendages, four <strong>of</strong> which are<br />
cephalic (antennules, antennae, m<strong>and</strong>ibles, <strong>and</strong> maxillulae), three thoracic,<br />
<strong>and</strong> one caudal (uropod). They are generally small-sized (stygobionts<br />
seldom exceed 1 mm in length), <strong>and</strong> are found in all types <strong>of</strong> surface- <strong>and</strong><br />
groundwater.<br />
<strong>Despite</strong> their large numbers in groundwater, both in caves <strong>and</strong> alluvial<br />
aquifers, stygobiont mussel shrimps are little known in Italy, <strong>and</strong> m<strong>any</strong><br />
Cypria cavernae (ca. 100x) Pseudolimnocythere sp. aff. hypogea (ca. 100x)<br />
species are still being studied. Among the most interesting is Cypria<br />
cavernae, thought to be endemic to alkaline karstic waters in Gorizia, Trieste<br />
<strong>and</strong> Slovenia. Other species are associated with anchialine habitats, like<br />
those in underground lakes <strong>of</strong> coastal caves in the Salento in Apulia<br />
(Trapezic<strong>and</strong>ona stammeri, Pseudolimnocythere hypogea). Specimens <strong>of</strong><br />
the genus Pseudolimnocythere were found in the brackish water <strong>of</strong> the<br />
Poiano springs, which issue from Triassic evaporites in the upper Val<br />
Secchia.<br />
A very interesting genus from the palaeogeographical viewpoint is<br />
Sphaeromicola. It is a commensal species living exclusively on stygobiont<br />
isopod crustaceans <strong>of</strong> the genera Monolistra (Sphaeromicola stammeri, in the<br />
Pre-Alps) <strong>and</strong> Sphaeromides (Sphaeromicola sphaeromidicola, in the Isonzo<br />
Karst). The same genus includes a commensal species on marine amphipod<br />
crustaceans, showing how both these ostracods <strong>and</strong> their hosts had marine<br />
ancestors.<br />
Mussel shrimps are very interesting in palaeogeographical research, because<br />
their shells are easily conserved in sediments, where they fossilise. The large<br />
numbers <strong>of</strong> fossil species, together with the great diversity <strong>of</strong> living ones,<br />
provide detailed information about the evolution <strong>of</strong> the animals <strong>of</strong> this class.<br />
Unfortunately, since stygobiont species are little known, have rarely been<br />
used to analyse the origin <strong>and</strong> evolution <strong>of</strong> stygobiont fauna.<br />
53
54<br />
■ Copepods<br />
Copepods form the largest <strong>and</strong> most diversified group <strong>of</strong> crustaceans, with<br />
13,000 species described, half <strong>of</strong> which are commensal or parasitic on other<br />
organisms. Copepods are divided into ten orders, four <strong>of</strong> which include freeliving<br />
species in groundwater (calanoid, cyclopoid, gelyelloid <strong>and</strong> harpacticoid<br />
copepods). Except for gelyelloid copepods, which live in the Jura mountains<br />
between Switzerl<strong>and</strong> <strong>and</strong> France, the other three orders are found in Italy.<br />
Throughout their long evolution, copepods spread across continents,<br />
successfully colonising <strong>any</strong> aquatic environment. In freshwater, they live in<br />
st<strong>and</strong>ing waters (from lakes to transient pools), in benthic substrates <strong>of</strong> streams,<br />
<strong>and</strong> in all types <strong>of</strong> groundwater. They are also found in moss, forest litter soil <strong>and</strong><br />
in wet meadows. Surface copepods spread easily thanks to their resting stages,<br />
which have been described in previous “Italian Habitats” volumes. These<br />
stages are also thought to exist in stygobiont species, although there is no<br />
evidence. This is why species exclusive to groundwater spread with difficulty,<br />
<strong>and</strong> are generally endemic. This characteristic is particularly evident in karstic<br />
systems, whereas species living in alluvial aquifers generally occupy larger<br />
areas, whose hyporheic habitats may easily be connected.<br />
Stygobiont copepods are very small (0.2-1 mm) <strong>and</strong>, with the sole exception<br />
<strong>of</strong> calanoids, have one main articulation between thoracic somites<br />
Speocyclops sp. aff. infernus (ca. 120x)<br />
(segments) 4 <strong>and</strong> 5, which divide their<br />
bodies into two distinct parts, the<br />
anterior prosome <strong>and</strong> the posterior<br />
urosome. The prosome includes the<br />
cephalothorax <strong>and</strong> four footed<br />
somites. The cephalothorax bears six<br />
pairs <strong>of</strong> cephalic appendages<br />
(antennules, antennae, m<strong>and</strong>ibles,<br />
maxillulae, maxillae <strong>and</strong> maxillipeds),<br />
<strong>and</strong> each thoracic somite has a pair <strong>of</strong><br />
oar-shaped limbs used for swimming<br />
Antennule <strong>of</strong> a male harpacticoid copepod<br />
(ca. 850x)<br />
(hence the name copepod, from the Greek, meaning “oar-shaped foot”). The<br />
urosome includes an anterior somite - bearing the fifth pair <strong>of</strong> thoracic<br />
appendages - <strong>and</strong> four appendage-free abdominal somites, the last <strong>of</strong> which,<br />
called anal somite, bears the two-branched furca, the unmistakable feature <strong>of</strong><br />
copepods.<br />
Reproduction requires the participation <strong>of</strong> both sexes, <strong>and</strong> parthenogenesis is<br />
rare. Males are distinguished from females by one (in calanoids) or both (in<br />
cyclopoids <strong>and</strong> harpacticoids) antennules modified in the shape <strong>of</strong> claspers,<br />
used to hold the female during mating. The fertilised eggs are usually<br />
contained in one or two egg-sacs carried by the females. Groundwater<br />
species produce very few eggs, sometimes only one, large. Some stygobiont<br />
species do not have egg-sacs, <strong>and</strong> release their fertilised eggs directly on to<br />
the substrate. Among crustaceans, copepods exhibit the most complete<br />
metamorphosis. The eggs hatch into larvae called nauplii. There are six<br />
naupliar stages <strong>and</strong>, after the fifth moult, the nauplii turn into copepodids,<br />
which are segmented <strong>and</strong> similar to adults. Five copepodid stages follow, until<br />
the sexually mature adult stage is completed.<br />
Very little is known <strong>of</strong> the feeding requirements <strong>of</strong> stygobiont copepods.<br />
Calanoids, which are part <strong>of</strong> plankton, are filterers; larger cyclopoids<br />
(Acanthocyclops, Megacyclops) are predators <strong>and</strong> feed on other microorganisms.<br />
Most species are omnivorous, <strong>and</strong> the main source <strong>of</strong> food for<br />
small interstitial copepods (almost all harpacticoids <strong>and</strong> cyclopoids <strong>of</strong> the<br />
genera Speocyclops <strong>and</strong> Graeteriella) is particle-sized organic matter <strong>and</strong> <strong>its</strong><br />
associated microbial bi<strong>of</strong>ilm.<br />
● Calanoid copepods. The only Italian stygobiont species, Troglodiaptomus<br />
sketi, lives in caves in the Karst <strong>of</strong> Gorizia <strong>and</strong> Trieste, in Slovenia <strong>and</strong> Croatia.<br />
It is commonly planktonic in underground lakes. Very little is known <strong>of</strong> <strong>its</strong><br />
ecology.<br />
55
56<br />
● Cyclopoid copepods. So far, only about a hundred species are known to<br />
live in Italian freshwater, almost all <strong>of</strong> which belongs to the cyclopids. Few <strong>of</strong><br />
them are planktonic in free waters (some Metacyclops in caves <strong>of</strong> Venezia<br />
Giulia, Apulia <strong>and</strong> Sardinia). Most are epibenthic or interstitial (e.g., genera<br />
Eucyclops, Acanthocyclops, Diacyclops, Graeteriella, <strong>and</strong> several<br />
Metacyclops <strong>and</strong> Speocyclops). Some species are exclusively associated with<br />
the vadose zone <strong>of</strong> karstic habitats, where they inhabit the network <strong>of</strong> micr<strong>of</strong>issures<br />
<strong>and</strong> trickling pools (several species <strong>of</strong> Speocyclops), <strong>and</strong> others (such<br />
as Eucyclops, Acanthocyclops <strong>and</strong> Metacyclops) are exclusive to karstic<br />
phreatic waters. Niche segregation is therefore marked, although their habitat<br />
preferences may vary in different geographical areas. The most common <strong>and</strong><br />
diversified cyclopoids in Italian groundwater belong to the group languidoides<br />
<strong>of</strong> the genus Diacyclops: this group <strong>of</strong> species, m<strong>any</strong> <strong>of</strong> which are still being<br />
described, is found in all Italian regions. Other cyclopoid species live in<br />
restricted areas in the karstic waters <strong>of</strong> north-eastern Italy (Acanthocyclops<br />
troglophilus, A. gordani, Metacyclops gasparoi, M. postojnae, Diacyclops<br />
charon, Speocyclops infernus, to mention only a few), or are widely distributed<br />
(like Eucyclops graeteri along the Alpine chain, <strong>and</strong> Acanthocyclops kieferi,<br />
which colonises Pre-Alpine <strong>and</strong> Apennine areas). Noteworthy is<br />
Acanthocyclops agamus, an exceptional endemic species living in caves <strong>of</strong><br />
the Alburni mountains (Salerno) <strong>and</strong> karstic areas in central Italy. It is an<br />
interesting example <strong>of</strong> progenetic paedomorphosis, a phenomenon described<br />
in the chapter on ecology. From the biogeographical viewpoint, other<br />
interesting species live in anchialine coastal groundwater, like the cyclopinid<br />
Muceddina multispinosa, recently described from caves in Sardinia, <strong>and</strong><br />
m<strong>any</strong> species <strong>of</strong> cyclopids <strong>of</strong> the genus Halicyclops. All groundwater species<br />
<strong>of</strong> cyclopids known so far probably derive from ancestors that used to inhabit<br />
surface freshwater, <strong>and</strong> the same applies to species living in brackish water,<br />
for which anchialine (<strong>and</strong> marine) environments are secondary habitats.<br />
Instead, cyclopinids probably have marine origins, although none <strong>of</strong> these<br />
species moves far from the coastline.<br />
● Harpacticoid copepods. Except for species living in coastal marine<br />
groundwater, which host interesting biocoenoses, six families <strong>and</strong> 160 species<br />
<strong>of</strong> harpacticoids are known to live in continental Italian freshwater, half <strong>of</strong> which<br />
belong to the canthocamptids. The order includes numerous benthic <strong>and</strong><br />
interstitial species, commonly found in all types <strong>of</strong> underground ecosystems.<br />
Stygobiont harpacticoid species have different origins, <strong>and</strong> include species<br />
with recent <strong>and</strong> ancient marine origin (like ameirids <strong>and</strong> ectinosomatids), as<br />
well as those deriving from surface freshwater ancestors, like most<br />
canthocamptids. There are several endemic species, m<strong>any</strong> <strong>of</strong> which are limited<br />
to specific karstic areas (genera Nitocrella, Elaphoidella, Lessinocamptus,<br />
Moraria, Morariopsis, Paramorariopsis). Several species - only recently<br />
discovered or currently being described - populate micr<strong>of</strong>issures in limestone<br />
or the tiny pools formed by trickling <strong>and</strong> percolating water in the vadose zone <strong>of</strong><br />
caves. The nature <strong>of</strong> these environments <strong>and</strong> the isolation <strong>of</strong> limestone systems<br />
following karstification have presumably favoured speciation by vicariance,<br />
producing large numbers <strong>of</strong> endemics.<br />
Most endemics in karstic waters are known to live in caves in the Pre-Alps<br />
<strong>and</strong> on Sardinia. Recently, species <strong>of</strong> the genus Pseudectinosoma have been<br />
found in deep karstic systems <strong>of</strong> the Gran Sasso Massif, in the Alburni <strong>and</strong><br />
Aurunci mountains. Before this extraordinary discovery, only two species<br />
were known in this genus, one marine species with amphi-Atlantic<br />
distribution <strong>and</strong> the other, stygobiont, known to live in French groundwater.<br />
The discovery <strong>of</strong> members <strong>of</strong> this puzzling genus <strong>of</strong> ectinosomatids in Italian<br />
groundwater has great biogeographical importance, as the genus is not<br />
known to inhabit the Mediterranean area, <strong>and</strong> Italian freshwater stygobionts<br />
may be relict species, the only survivors <strong>of</strong> an ancient fauna which became<br />
extinct in the marine environment during the salinity crisis that affected the<br />
Mediterranean in the Miocene. In addition, the surprising discovery <strong>of</strong><br />
Pseudectinosoma galassiae in Australian groundwater confirms the extremely<br />
Elaphoidella pseudophreatica (ca. 50x)<br />
57
58<br />
SEM photos <strong>of</strong> harpacticoid copepods; from top to bottom: Pseudectinosoma reductum, Nitocrella<br />
pescei <strong>and</strong> Elaphoidella elaphoides (ca. 200x)<br />
ancient origin <strong>of</strong> the genus, which perhaps dates back to a period before the<br />
onset <strong>of</strong> continental drift in the Tertiary.<br />
Groundwater in alluvial aquifers also hosts endemic species like those <strong>of</strong> the<br />
genera Nitocrella, Parapseudoleptomesochra <strong>and</strong> Elaphoidella in much wider<br />
areas than in karstic environments. A particular feature <strong>of</strong> the genus<br />
Parastenocaris is that it fragmented into a myriad <strong>of</strong> species, most <strong>of</strong> which<br />
are known to inhabit only one or a few sites. Italy hosts 35 species - including<br />
those <strong>of</strong> the closely related genus Simplicaris - although m<strong>any</strong> more species<br />
must still be described. Parastenocaris are the tiniest copepods (seldom<br />
longer than 3/10 <strong>of</strong> a mm), with worm-shaped bodies <strong>and</strong> small appendages,<br />
which enable them to wriggle through the minute fissures between s<strong>and</strong> <strong>and</strong><br />
gravel grains in interstitial environments.<br />
■ Bathynellaceans<br />
Bathynellaceans are an order <strong>of</strong> totally<br />
stygobiont syncarid malacostracans <strong>of</strong><br />
extremely ancient origin; some<br />
researchers believe they diversified as<br />
long ago as the Palaeozoic in littoral<br />
coastal waters, lagoons <strong>and</strong> estuaries,<br />
from which they colonised continental<br />
waters before the supercontinent Bathynella skopljensis (ca. 15x)<br />
Pangaea fragmented, causing them to<br />
spread into groundwater. Although only hypothetical, this fascinating scenario<br />
describes bathynellaceans as true living fossils, <strong>and</strong> shows how research on<br />
the taxonomy <strong>of</strong> these stygobionts is closely associated with the great palaeogeographical<br />
events which modelled the Earth’s surface.<br />
About 170 species <strong>of</strong> bathynellaceans are known, all <strong>of</strong> small size (between 0.5<br />
<strong>and</strong> 3.5 mm), anophthalmic <strong>and</strong> diaphanous, with elongated, sometimes<br />
worm-like bodies. They do not have shells or brood pouches like isopods,<br />
amphipods <strong>and</strong> thermosbaenaceans, <strong>and</strong> their last abdominal segment (called<br />
telson) is free; these characteristics clearly identify these malacostracans.<br />
Italian bathynellaceans are still little known <strong>and</strong> studied: the first Italian<br />
representative <strong>of</strong> this group (Anthrobathynella stammeri) was discovered in<br />
1954 in the interstitial environment <strong>of</strong> the river Adige in Verona, <strong>and</strong> since<br />
then only a few species have been described, belonging to the genera<br />
Bathynella, Hexabathynella, Hispanobathynella, Meridiobathynella <strong>and</strong><br />
Sardobathynella. They include exclusively hyporheic interstitial species <strong>and</strong><br />
59
60<br />
those associated with percolating water in caves. They are stenothermal<br />
animals, sometimes living in cold waters, as they have recently been found<br />
at high altitudes in the Alps.<br />
■ Thermosbaenaceans<br />
Thermosbenaceans, like bathynellaceans,<br />
are an order <strong>of</strong> very ancient<br />
malacostracans, with about 30<br />
stygobiont species living in fresh <strong>and</strong><br />
slightly brackish water from the<br />
Caribbean sector to the circum-<br />
Mediterranean area, eastern Africa,<br />
Monodella stygicola (ca. 15x)<br />
Asia, <strong>and</strong> Australia. This group clearly<br />
differs from other malacostracans, due<br />
to the dorsal egg pouch formed by the carapace.<br />
The evolution <strong>of</strong> thermosbaenaceans is probably associated with the retreat <strong>of</strong><br />
the sea following uplift caused by plate tectonics. The species <strong>of</strong>ten live in<br />
isolated locations <strong>and</strong> are <strong>of</strong> great biogeographical interest. Their name is<br />
misleading, as it refers to thermal water: in fact, it derives from the first species<br />
described, which was collected in an African thermal spring.<br />
Italy hosts four species - three <strong>of</strong> which are endemic to the country - living in<br />
saturated aquifers. Limnosbaena finki is found in karstic <strong>and</strong> alluvial water in<br />
north-eastern Italy (it is distributed as far as Bosnia); Monodella stygicola only<br />
lives in karstic habitats, occasionally in alluvial aquifers, in Apulia; Tethysbaena<br />
argentarii is an endemic species <strong>of</strong> anchialine waters in the Grotta di Punta<br />
degli Stretti (Argentario Promontory, Tyrrhenian), <strong>and</strong> Tethysbaena siracusae is<br />
endemic to the karstic area <strong>of</strong> Porto Palo in south-eastern Sicily.<br />
Spelaeomysis bottazzii (ca. 1x)<br />
■ Mysidaceans<br />
Mysidaceans, or opossum shrimps, are<br />
malacostracans generally living in sea<br />
or brackish water. In Italy, there are two<br />
stygobiont genera, Stygiomysis <strong>and</strong><br />
Spelaeomysis, in anchialine <strong>and</strong><br />
freshwater in karstic areas in Apulia.<br />
The Mediterranean area hosts a third<br />
stygobiont species, Troglomysis, in the<br />
Dinaric karst. These detrivorous <strong>and</strong> saprophagous animals are 2-3 cm long -<br />
thus, unusually large compared with other mysids - <strong>and</strong> are found in small<br />
lakes, seldom in flowing water.<br />
A euryhaline <strong>and</strong> eurythermal species, Spelaeomysis bottazzii, usually lives in<br />
anchialine habitats in south-eastern Italy, between the Gargano <strong>and</strong> Salento<br />
(Apulia), even in polluted water. Stygiomysis hydruntina is rare, <strong>and</strong><br />
presumably lives further down, where the water-table recharges; so far, it has<br />
only been collected on the Ionian side <strong>of</strong> the province <strong>of</strong> Lecce. The two<br />
species may locally cohabit. Although electrophoretic analyses suggest that<br />
the species are <strong>of</strong> recent, perhaps Pliocene origin, similar species in Mexico,<br />
the Caribbean <strong>and</strong> eastern Africa imply a more ancient, Tethyan origin.<br />
■ Isopods<br />
Woodlice are a very diversified order<br />
<strong>of</strong> malacostracan crustaceans, with<br />
more than 10,000 known species.<br />
They presumably colonised Italian<br />
groundwater from marine (cirolanids,<br />
microparasellids, microcerberids)<br />
<strong>and</strong> surface freshwater ancestors<br />
(asellotans <strong>and</strong> perhaps sphaeromatids).<br />
Each family is a microcosm in <strong>its</strong>elf,<br />
Proasellus franciscoloi (ca. 6x)<br />
<strong>and</strong> their study reveals very interesting<br />
biogeographical aspects.<br />
Asellids. Almost all stygobiont species <strong>of</strong> this family are Italian endemics.<br />
Asellus cavernicolus lives in the river Timavo (Trieste Karst). Results from<br />
molecular studies reveal that it is a relict species deriving from pre-glacial<br />
colonisation <strong>of</strong> the Trieste Karst by an epigean species, Asellus aquaticus. In<br />
Italy, the genus Proasellus counts several surface as well as cavernicolous<br />
<strong>and</strong> interstitial species.<br />
The genus diversified into m<strong>any</strong> phyletic lines, the taxonomy <strong>of</strong> which<br />
requires clarification: the group deminutus in north-eastern Italy; pavani in the<br />
central-eastern Pre-Alps; cavaticus in France, western Piedmont <strong>and</strong> Liguria,<br />
in karstic environments (P. cavaticus, P. franciscoloi), <strong>and</strong> the group patrizii,<br />
exclusive to Sardinian groundwater. In addition, there are m<strong>any</strong> similar<br />
species: P. ligusticus, found from Liguria to the Apuan Alps, <strong>and</strong> P. acutianus,<br />
in Tusc<strong>any</strong>, Latium <strong>and</strong> the isl<strong>and</strong> <strong>of</strong> Elba are the most widely distributed<br />
61
62<br />
species. Other species are only known to live in restricted areas, like P.<br />
amiterninus, P. dianae, P. adriaticus <strong>and</strong> P. faesolanus.<br />
The similar genus Chthonasellus includes C. bodoni, endemic to karstic <strong>and</strong><br />
interstitial waters in the Cuneo area (Piedmont), which is thought to be<br />
phylogenetically close to the French genus Gallasellus.<br />
Stenasellids. This family comprises exclusively stygobiont species <strong>of</strong> very<br />
ancient origin, found in Tusc<strong>any</strong> (Stenasellus gr. racovitzai) <strong>and</strong> Sardinia, in<br />
both caves <strong>and</strong> interstitial habitats. In Sardinia, techniques <strong>of</strong> molecular<br />
biology have identified m<strong>any</strong> endemics, two <strong>of</strong> which have so far been<br />
attributed to S. racovitzai <strong>and</strong> are similar to French species, <strong>and</strong> two others<br />
(S. nuragicus, S. assorgiai) are similar to species found in eastern Europe.<br />
Two species collected in the area <strong>of</strong> Nuoro (Sardinia) are similar to Spanish<br />
species.<br />
Preliminary dating based on “molecular clocks”, suggests that the separation<br />
<strong>of</strong> the two phyletic lines dates back about 28 million years (Upper Miocene).<br />
This is one <strong>of</strong> the most fascinating biological pieces <strong>of</strong> evidence <strong>of</strong> the<br />
complex Tyrrhenid history.<br />
Microparasellids. This family <strong>of</strong> tiny isopods (a few mm long) deriving<br />
from ancient marine ancestors which colonised interstitial habitats<br />
during the marine regressive phases. Their distribution follows the<br />
ancient coastline <strong>of</strong> Tertiary seas. In Italy, six interstitial species are<br />
known, all belonging to the genus Microcharon (see drawing). Of<br />
these, only M. marinus is associated with transient groundwater<br />
along the Mediterranean coasts, <strong>and</strong> the geographical location <strong>of</strong><br />
other species - e.g. M. novariensis, found in Piedmont springs -<br />
reveals that they are relicts.<br />
Microcerberids. The family comprises mainly marine species, <strong>and</strong> only<br />
the relict Microcerberus ruffoi (see drawing) lives in Italian underground<br />
freshwater (water-table <strong>of</strong> the river Adige).<br />
Cirolanids. This family includes mainly marine species, <strong>and</strong> only<br />
two are Italian stygobionts. Sphaeromides virei inhab<strong>its</strong> alkaline<br />
water in the Gorizia Karst. A voracious predator, it is quite large (more<br />
than 3 cm long). Its typically Balkanic distribution <strong>and</strong> fragmentation<br />
into endemic subspecies suggest that it originally lived in<br />
groundwater in the Dinaric karst. Typhlocirolana aff. moraguesi is<br />
exclusive to the karstic system near Porto Palo (Siracusa, Sicily),<br />
<strong>and</strong> was distinguished from T. moraguesi (isl<strong>and</strong> <strong>of</strong> Majorca) with<br />
molecular biology techniques. Its origin is probably palaeo-<br />
Mediterranean.<br />
Sphaeromatids. M<strong>any</strong> species <strong>of</strong> the genus Monolistra, widely distributed in<br />
the Balkans, also live between the Italian-Slovenian border <strong>and</strong> the area <strong>of</strong><br />
Como (north <strong>of</strong> Milan), in karstic groundwater in Pre-Alpine caves. Their<br />
absence north <strong>of</strong> the line that marked the southern boundary <strong>of</strong> the great<br />
Quaternary glaciers shows that they settled in groundwater during the<br />
Pliocene, perhaps deriving from surface freshwater ancestors which have<br />
become extinct.<br />
Ongoing molecular research will clarify their evolution. Each species <strong>and</strong><br />
subspecies is endemic to a restricted karstic system. Monolistra<br />
schottlaenderi is exclusive to saturated aquifers <strong>of</strong> the Karst in the areas <strong>of</strong><br />
Trieste <strong>and</strong> Isonzo, <strong>and</strong> is the only Italian member <strong>of</strong> the subgenus<br />
Microlistra, which also lives in Slovenia <strong>and</strong> Croatia. The species <strong>of</strong> this<br />
subgenus have knobby dorsal protrusions, <strong>and</strong> sometimes even long, robust<br />
spines that function as efficient defensive structures when the animal curls<br />
into a ball.<br />
Among other species, with smooth teguments, there is Monolistra julia,<br />
endemic to caves in the Julian Pre-Alps, where it lives in small streams <strong>of</strong><br />
trickling water. It has two well-developed caudal appendages (uropods). Other<br />
species do not have uropods, which may be atrophic or barely visible. The<br />
furthest west (Monolistra pavani) is found in the underground stream <strong>of</strong> the<br />
Buco del Piombo (Como).<br />
Monolistra racovitzai (ca. 5x)<br />
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64<br />
Species <strong>of</strong> genus Niphargus; top: N. costozzae; centre: N. longicaudatus; left, bottom: N. pescei (top)<br />
<strong>and</strong> N. transitivus (bottom); right, bottom: N. bajuvaricus gr<strong>and</strong>ii (ca. 3x)<br />
■ Amphipods<br />
This order <strong>of</strong> malacostracans includes<br />
several marine <strong>and</strong> freshwater species,<br />
sometimes sub-terrestrial, which<br />
colonised groundwater either directly<br />
from the sea, or from ancestors that<br />
once inhabited limnic surface water. In<br />
Italy, there are about 100 stygobiont<br />
species, almost all <strong>of</strong> which are<br />
endemic.<br />
Bogidiellids. Italian freshwaters host<br />
seven stygobiont species, most <strong>of</strong> Bogidiella sp. (ca. 10x)<br />
which are interstitial, occasionally<br />
euryhaline. Bogidiella albertimagni (in the Po Plain) <strong>and</strong> Bogidiella aprutina are<br />
the only continental species; the others are Tyrrhenian endemics, found in<br />
Sardinia <strong>and</strong> on the isl<strong>and</strong> <strong>of</strong> Elba.<br />
Gammarids. This family comprises exclusively surface species. Among those<br />
which only live in groundwater <strong>and</strong> are Italian endemics, two species <strong>of</strong><br />
Tyrrhenogammarus live in karstic aquifers in south-eastern Sicily<br />
(Tyrrhenogammarus catacumbae) <strong>and</strong> Sardinia (T. sardous). One species <strong>of</strong><br />
Longigammarus (L. planasiae) has recently been collected from a well on the<br />
limestone isl<strong>and</strong> <strong>of</strong> Pianosa (Tuscan archipelago), <strong>and</strong> a specialised species,<br />
Ilvanella inexpectata, is known to inhabit alluvial aquifers on the isl<strong>and</strong> <strong>of</strong> Elba<br />
<strong>and</strong> in Tusc<strong>any</strong>.<br />
Hadziids. The genus Hadzia - presumably a Tethyan relict - has four Italian<br />
species. Hadzia fragilis stochi, an endemic subspecies with delicate, elongated<br />
appendages, has been described in alkaline water in the karstic area <strong>of</strong> Trieste<br />
<strong>and</strong> river Isonzo. Hadzia minuta inhab<strong>its</strong> karstic waters in Salento, <strong>and</strong> H.<br />
adriatica has been collected from pools in Apulia. Another species, which is<br />
still under description, was recently found in southern Sardinia.<br />
Niphargids. The genus Niphargus (more than 250 known species, 70 <strong>of</strong> which<br />
live in Italy; size between 3 <strong>and</strong> 40 mm) have complex, controversial<br />
taxonomy, which is currently being revised by means <strong>of</strong> molecular biology<br />
techniques. Their distribution area includes most <strong>of</strong> Europe (except for the<br />
Iberian Peninsula <strong>and</strong> the upper northern areas) <strong>and</strong> stretches east towards<br />
Iran. This suggests that the genus colonised European surface freshwater<br />
from the basins <strong>of</strong> the Tertiary Paratethys, <strong>and</strong> later moved into groundwater.<br />
However, fossils similar to present species have recently been found in Baltic<br />
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amber, implying a perhaps more ancient origin. Almost all species are endemic<br />
<strong>and</strong> live in the Alps <strong>and</strong> Po Plain, in several distinct, although not welldefined<br />
phyletic lines (the main groups being stygius, kochianus, aquilex <strong>and</strong><br />
bajuvaricus).<br />
The diversity <strong>of</strong> the genus decreases proceeding southwards down the<br />
Apennines, with species belonging to the groups speziae (northern <strong>and</strong><br />
central Apennines), longicaudatus (throughout the Apennines, Sicily,<br />
Sardinia, <strong>and</strong> smaller isl<strong>and</strong>s), <strong>and</strong> orcinus. This last group includes species<br />
similar to Balkan ones (exclusively associated with karstic aquifers), which<br />
colonised Italy from the Julian karst in the north-east <strong>and</strong>, perhaps through<br />
trans-Adriatic pathways, the limestone systems <strong>of</strong> the central-southern<br />
Apennines <strong>and</strong> Apulia. In addition to these groups, there are several species<br />
<strong>of</strong> unknown affinity, like Niphargus stefanellii (found in caves in centralsouthern<br />
Italy), which seems related to Balkan species, <strong>and</strong> colonises even<br />
sulphureous waters.<br />
Niphargus species, which are greatly diversified in structure <strong>and</strong> size,<br />
colonise all types <strong>of</strong> underground habitats. In large alkaline karstic lakes,<br />
species are large (2-4 cm) with elongated antennae <strong>and</strong> other appendages,<br />
<strong>and</strong> large anterior claw-shaped limbs (gnathopods) for seizing prey<br />
(Niphargus steueri, N. tridentinus). Interstitial environments host small<br />
omnivorous species (3-10 mm) with globose (Niphargus pupetta, N.<br />
transitivus) or elongated, worm-like bodies (Niphargus bajuvaricus gr<strong>and</strong>ii,<br />
N. italicus). Other species colonise subsurface, non-karstic aquifers, <strong>and</strong><br />
may even be found in moist soil. They have tapering bodies, like N.<br />
dolenianensis <strong>and</strong> various species <strong>of</strong> the group longicaudatus. Italy also<br />
hosts the only species <strong>of</strong> the related genus Carinurella (C. paradoxa), which<br />
has a globose body with stumpy appendages <strong>and</strong> lives in interstitial waters <strong>of</strong><br />
Friuli Venezia Giulia.<br />
Salentinellids. This is possibly a palaeo-Mediteranean amphipod family that<br />
comprises only stygobionts deriving from marine ancestors, whose identity is<br />
still uncertain.<br />
Salentinella species are still undergoing revision, <strong>and</strong> the most common<br />
species, S. angelieri, is typically interstitial <strong>and</strong> lives in brackish water near the<br />
coastline. It is also found in caves <strong>of</strong> isolated karstic systems <strong>and</strong> in true<br />
continental groundwater, with other species like S. franciscoloi <strong>of</strong> Liguria.<br />
Salentinella gracillima is exclusive to groundwater in Apulia.<br />
Ingolfiellidae. This family includes m<strong>any</strong> stygobionts with elongated bodies<br />
living in marine <strong>and</strong> freshwater interstitial environments. So far, only one<br />
species has been found in Italian fresh groundwaters: Ingolfiella<br />
(Tyrrhenidiella) cottarellii, from a cave on the isl<strong>and</strong> <strong>of</strong> Tavolara (<strong>of</strong>f the northeastern<br />
coast <strong>of</strong> Sardinia).<br />
Metaingolfiellids. The family comprises the single species Metaingolfiella<br />
mirabilis, which is quite large (3 cm). M<strong>any</strong> specimens <strong>of</strong> this species were<br />
collected, on a single occasion, from water pumped out <strong>of</strong> a deep karstic well<br />
in Salento. Described in 1969, it has never been found since. It is perhaps one<br />
<strong>of</strong> the most ancient palaeo-endemics <strong>of</strong> Italian fauna. Its body structure <strong>and</strong><br />
the shape <strong>of</strong> <strong>its</strong> gnathopods suggest that it is a predator.<br />
Pseudoniphargids. This family includes only stygobionts, <strong>and</strong> is particularly<br />
diversified in the Mediterranean area. In Italy, only a few species are known,<br />
living in interstitial environments <strong>and</strong> caves near the coastline, showing their<br />
marine origin. Two species (Pseudoniphargus africanus italicus, P. sodalis) live<br />
in Sicily, <strong>and</strong> one (P. planasiae) in the Tuscan archipelago. Pseudoniphargus<br />
adriaticus has been collected in wells near Bari, <strong>and</strong> is also known to inhabit<br />
the Pelagian Isl<strong>and</strong>s (between Sicily <strong>and</strong> Tunisia), although <strong>its</strong> taxonomic<br />
status is uncertain. Other specimens, collected in Sardinia, are still being<br />
examined.<br />
Metacrangonyctids. This family is distributed around the Atlantic, includes only<br />
stygobionts, <strong>and</strong> is very diversified in the Mediterranean area. Italy hosts only<br />
Metacrangonyx ilvanus, endemic to the isl<strong>and</strong> <strong>of</strong> Elba, where it was recently<br />
found only in one well in alluvial groundwaters.<br />
Salentinella angelieri (ca. 30x)<br />
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■ Decapods<br />
Italian fauna has only two stygobiont<br />
decapod genera living in karstic waters:<br />
Troglocaris (Isonzo <strong>and</strong> Trieste Karst)<br />
<strong>and</strong> Typhlocaris (Apulia). Recent<br />
research has revealed that Italian caves<br />
actually host two species <strong>of</strong> shrimps <strong>of</strong><br />
the genus Troglocaris <strong>of</strong> the<br />
anophthalmus group, morphologically<br />
difficult to distinguish, but easily<br />
Troglocaris anophthalmus<br />
identified by means <strong>of</strong> molecular<br />
biology techniques. They may belong<br />
to T. anophthalmus (Gorizia Karst) <strong>and</strong><br />
T. planinensis (Trieste Karst), although<br />
their taxonomy still requires<br />
Typhlocaris salentina<br />
confirmations. Stygobiont species <strong>of</strong><br />
the genus Troglocaris were thought to<br />
derive from marine ancestors. Very<br />
recent molecular biology analyses<br />
carried out at the University <strong>of</strong> Ljubljana<br />
(Slovenia) have dated the separation <strong>of</strong><br />
the western anophthalmus group from<br />
the Dinaric-Caucasian one at between<br />
6 <strong>and</strong> 11 million years ago, <strong>and</strong> the<br />
beginning <strong>of</strong> speciation within the<br />
anophthalmus group between 3.7 <strong>and</strong><br />
5.3 million years ago. Their marine origin is therefore very ancient, <strong>and</strong><br />
populations colonised groundwater coming from surface freshwater.<br />
The third species <strong>of</strong> Italian stygobiont decapods, Typhlocaris salentina, is<br />
endemic to Apulian caves. It was discovered in the Grotta Zinzulusa at Castro<br />
Marina in 1922, <strong>and</strong> later collected from other caves in Salento, Murge <strong>and</strong><br />
Gargano. This blind, depigmented prawn may reach exceptional sizes (up to<br />
13 cm); a predator, it feeds on mysidaceans <strong>and</strong> stygoxene organisms.<br />
The genus Typhlocaris includes two stygobiont species living in groundwater<br />
in Israel <strong>and</strong> Libya, suggesting that it is an ancient relict <strong>of</strong> an otherwise extinct<br />
palaeo-Mediterranean pre-Pliocene surface fauna associated with a subtropical<br />
climate. Unfortunately, molecular data on this genus are not yet<br />
available.<br />
■ Amphibians<br />
The olm (Proteus anguinus) is the only stygobiont amphibian <strong>of</strong> the Palaearctic<br />
fauna. The pétit dragon <strong>of</strong> the Postojna caves (Slovenia) - discovered by the<br />
Slovenian nobleman Valvasor in 1689 <strong>and</strong> briefly described by Laurenti in<br />
1768 - is the best-known underground animal described so far <strong>and</strong>, in some<br />
ways, the most fascinating. It has a pinkish-white eel-shaped body, with<br />
atrophic eyes concealed under the skin <strong>and</strong> outer red gill plumes which it<br />
retains throughout <strong>its</strong> life. The olm is known for <strong>its</strong> neoteny, i.e., it reaches<br />
precocious reproductive maturity despite <strong>its</strong> larval <strong>appearance</strong>. Olms are<br />
predators feeding on other aquatic, even stygoxene animals; the females lay<br />
between 20 <strong>and</strong> 80 eggs, one at a time for over one month, <strong>and</strong> place them<br />
under rocks <strong>and</strong> stones. The greyish tadpoles have distinct eyes, which they<br />
retain until they are two months old. Until the age <strong>of</strong> three months, olms feed<br />
exclusively on yolk stored in the cells <strong>of</strong> their digestive tracts. In nature,<br />
reproduction seldom occurs before the tenth year <strong>of</strong> age.<br />
The origin <strong>of</strong> olms is debated. Fossils <strong>of</strong> proteids <strong>and</strong> iguanodonts, found at<br />
Bernissart in Belgium, date back to the Lower Cretaceous, when olms lived in<br />
surface water. Their colonisation <strong>of</strong> karstic groundwaters in the Dinaric area<br />
where they now live may have started in the Pliocene, when karstification<br />
began. In 1994, in the Slovenian Karst, a pigmented, eyed subspecies was<br />
Olms also live in the groundwaters <strong>of</strong> the Isonzo Karst<br />
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Olm (Proteus anguinus)<br />
discovered (Proteus anguinus parkelj)<br />
genetically similar to the stygobiont<br />
populations <strong>of</strong> the same area, <strong>and</strong><br />
thus suggesting that groundwater<br />
populations are more recent.<br />
Recent molecular analyses reveal that<br />
there may be more stygobiont olm<br />
species.<br />
In Italy, olms are known to inhabit only<br />
alkaline water in caves <strong>of</strong> the Trieste<br />
<strong>and</strong> Isonzo Karsts. An isolated<br />
population, introduced from Slovenia<br />
in 1850, still lives in Grotta Parolini at<br />
Oliero (Vicenza).<br />
Olms are the only Italian stygobionts<br />
listed as priority species in the Habitats<br />
Directive; they are also included in<br />
Annex IV <strong>and</strong> are therefore under strict<br />
protection.<br />
■ Italian styg<strong>of</strong>aunal provinces<br />
Some olm specimens, coming from Slovenia,<br />
were introduced into the Oliero cave system<br />
(Veneto) in 1850<br />
As analysis <strong>of</strong> previously described taxonomic groups suggests, the present<br />
geographical distribution <strong>of</strong> stygobiont species in Italy is the result <strong>of</strong> a series<br />
<strong>of</strong> events which took place in ancient times (historical factors) <strong>and</strong>, to a lesser<br />
extent, <strong>of</strong> ecological factors, which occour in “real time”. The role played by<br />
both is described in the chapter on ecology.<br />
Since the evolution <strong>of</strong> m<strong>any</strong> Italian taxonomic groups was similar over time,<br />
because they were affected by the same palaeogeographical events, Italy is<br />
divided into areas with similar fauna, particularly endemics. These areas are<br />
called styg<strong>of</strong>aunal provinces. Although these generalisations cannot tell us<br />
directly what the present fauna composition <strong>of</strong> a specific aquifer is, because<br />
this is also influenced by local events, they do describe the present situation<br />
<strong>of</strong> Italian stygobionts <strong>and</strong> explain where the most important endemic<br />
locations are found.<br />
Dinaric province. This area includes only the easternmost portion <strong>of</strong> Italy -<br />
the so-called “classic” Karst - an elliptical area <strong>of</strong> 200 km 2 , whose<br />
stygobionts are similar to those <strong>of</strong> the Karst in Slovenia, Istria <strong>and</strong> Dalmatia.<br />
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Styg<strong>of</strong>aunal provinces in Italy<br />
The area was affected by karstification<br />
in the late Miocene, <strong>and</strong> hosts m<strong>any</strong><br />
palaeo-endemics. Exclusive to the<br />
karstic vadose zone are harpacticoid<br />
copepods <strong>of</strong> the genus Morariopsis,<br />
the bathynellacean Bathynella<br />
skopljensis <strong>and</strong> the amphipod<br />
Niphargus stygius.<br />
Exceptional fauna, whose western<br />
limit <strong>of</strong> distribution is the Karst,<br />
populates large cavities filled with<br />
alkaline karstic water.<br />
Among these, there are polychaetes<br />
(Marifugia cavatica), gastropods<br />
(Belgr<strong>and</strong>ia stochi), ostracods (Cypria<br />
cavernae), calanoids (Troglodiaptomus<br />
sketi), <strong>and</strong> several cyclopoids <strong>and</strong><br />
Sphaeromides virei (ca. 1x)<br />
harpacticoids (like Acanthocyclops<br />
troglophilus <strong>and</strong> Nitocrella stochi). This area hosts the only Italian stygobiont<br />
isopods <strong>of</strong> the genus Asellus, those <strong>of</strong> the subgenus Microlistra, <strong>and</strong> the large<br />
Sphaeromides, as well as amphipods, which are highly diversified, with m<strong>any</strong><br />
endemics (e.g., Niphargus stochi, Hadzia fragilis). Other remarkable<br />
inhabitants are decapods <strong>of</strong> the genus Troglocaris, <strong>and</strong> the most famous<br />
stygobiont species, the olm (Proteus anguinus). Aquifers in marl <strong>and</strong><br />
s<strong>and</strong>stone also host very interesting fauna, with very different species from<br />
those found in adjacent karstic aquifers. Among the main biogeographical<br />
markers, there is the gastropod Istriana mirnae, <strong>and</strong> the large amphipods<br />
Niphargus spinulifemur <strong>and</strong> N. krameri.<br />
Alpine province. The Alpine styg<strong>of</strong>aunal province includes a very complex<br />
area associated with Alpine orogenetic events. It is divided into a northern part<br />
(strictly Alpine), above the southern limit <strong>of</strong> the great Quaternary glaciations,<br />
<strong>and</strong> a southern Pre-Alpine one, below which is the recent alluvial area <strong>of</strong> the<br />
Po Plain. The Alpine area is populated by only a few stygobionts: cold-loving,<br />
stenothermal species which followed the retreat <strong>of</strong> Quaternary glaciers <strong>and</strong><br />
colonised aquifers in carbonate <strong>and</strong> crystalline rocks in the Alps. In particular,<br />
a number <strong>of</strong> amphipods (Niphargus forelii, N. similis, N. strouhali) even live at<br />
high altitudes, above 2000 m, together with a few copepods <strong>and</strong><br />
bathynellaceans.<br />
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In the Pre-Alps, the situation changes completely, as there are large numbers<br />
<strong>of</strong> endemics living in the numerous karstic systems. The main<br />
biogeographical component is <strong>of</strong> eastern origin <strong>and</strong> stretches westwards as<br />
far as the Pre-Alps near Como, with a few genera living on Mount Fenera<br />
(Piedmont) (hydrobioid gastropods <strong>of</strong> the genus Iglica, harpacticoids <strong>of</strong> the<br />
genus Paramorariopsis). Typical genera <strong>of</strong> this area are several hydrobioids<br />
(Bythiospeum, Hauffenia, Hadziella, Iglica, Paladilhiopsis), harpacticoids<br />
(Lessinocamptus, Paramorariopsis, <strong>and</strong> several species <strong>of</strong> the genus<br />
Elaphoidella), amphipod crustaceans (Niphargus <strong>of</strong> the stygius group) <strong>and</strong><br />
isopods (Monolistra, Proasellus). The western <strong>and</strong> Ligurian Pre-Alps have<br />
fewer stygobionts, <strong>and</strong> their fauna is more similar to that in France (Proasellus<br />
<strong>of</strong> the cavaticus group) <strong>and</strong> the Apennine province (Alzoniella, Niphargus <strong>of</strong><br />
the longicaudatus group).<br />
Padanian province. The alluvial areas <strong>of</strong> the Po Plain, which stretch into the<br />
Alpine <strong>and</strong> Apennine valleys, have m<strong>any</strong> endemics. Here, as in the nearby<br />
Alpine province, there are m<strong>any</strong> species from the east, such as the isopod<br />
Proasellus intermedius, <strong>and</strong> several endemic amphipods (Niphargus italicus,<br />
N. pupetta, N. transitivus, N. longidactylus, Carinurella paradoxa). Other<br />
species are associated with the fauna <strong>of</strong> the extensive plains <strong>of</strong> centraleastern<br />
Europe, <strong>and</strong> probably migrated towards Italy in more recent times, like<br />
several cyclopoids <strong>of</strong> the groups languidus <strong>and</strong> languidoides <strong>of</strong> the genus<br />
Diacyclops, the bathynellacean Anthrobathynella stammeri, <strong>and</strong> the<br />
amphipods Bogidiella albertimagni <strong>and</strong> Niphargus bajuvaricus gr<strong>and</strong>ii. There<br />
are also more ancient organisms <strong>of</strong> pre-Quaternary marine origin, relict<br />
species survived to Pliocene events, perhaps also to Miocene sea retreat, like<br />
the recently discovered ectinosomatid harpacticoids <strong>and</strong> isopods <strong>of</strong> the<br />
genera Microcerberus <strong>and</strong> Microcharon.<br />
Apennine province. <strong>Despite</strong> <strong>its</strong> extent, from the Colle di Cadibona (Savona) to<br />
the Madonie in Sicily (excluding Apulia), the fauna <strong>of</strong> this area is well<br />
characterised. There are areas rich in endemics (Ligurian Apennines, Alburni<br />
mountains, Gran Sasso Massif) that are widely distributed in the Apennines.<br />
The apparent monotony <strong>of</strong> this fauna may be related to historical events, as<br />
karstification here is a recent event, <strong>and</strong> the fragmented limestone outcrops in<br />
the Apennines were covered by little permeable soil in the interval between the<br />
Pliocene <strong>and</strong> Miocene, <strong>and</strong> were only uncovered in the Quaternary. These<br />
palaeogeographical events are very similar from Latium to Calabria, <strong>and</strong> the<br />
areas are inhabited by endemics which are found along the Apennines <strong>and</strong> do<br />
not have particular habitat preferences (cyclopoid copepods <strong>of</strong> the genus<br />
Diacyclops, harpacticoids like Attheyella paranaphtalica <strong>and</strong> Nitocrella<br />
stammeri, <strong>and</strong> the amphipod Niphargus longicaudatus, which live in recent tufa<br />
Diacyclops gr. languidus, females with egg-sacs (ca. 70x) Harpacticoids <strong>of</strong> the genera Lessinocamptus (left) <strong>and</strong> Paramorariopsis (right) (ca. 100x)<br />
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aquifers in the Sabini mountains <strong>and</strong> in<br />
karstic water in Cilento <strong>and</strong> evaporites<br />
in Calabria as well). These recent<br />
populations settled where palaeoendemics<br />
were already living <strong>and</strong><br />
characterised Apennine areas. Thus,<br />
groundwater percolating in Triassic<br />
evaporites in Emilia hosts Niphargus<br />
poianoi; the karstic systems <strong>of</strong> the<br />
Aurunci, Gran Sasso <strong>and</strong> Alburni<br />
ranges are inhabited by the<br />
extraordinary copepod Acanthocyclops<br />
Stygiomysis hidruntina (ca. 2x)<br />
agamus <strong>and</strong> species <strong>of</strong> the genus<br />
Pseudectinosoma, which are perhaps<br />
Messinian relict. As regards gastropods, the genera Alzoniella, Avenionia <strong>and</strong><br />
Fissuria live in the northern Apennines, <strong>and</strong> Arganiella, Orientalina <strong>and</strong><br />
Pauluccinella in the central Apennines; the genus Islamia is divided into<br />
northern <strong>and</strong> central-southern species.<br />
Apulian province. Apulian groundwater is clearly different from that <strong>of</strong> the<br />
Apennines, <strong>and</strong> is rich in specialised endemics, especially in <strong>of</strong>ten brackish,<br />
saturated, karstic habitats. This is due to the extent <strong>and</strong> ancient origin <strong>of</strong><br />
karstification, as well as to the geological history <strong>of</strong> Apulia, which palaeogeographers<br />
consider as part <strong>of</strong> a different tectonic micro-plate from those<br />
that shaped the Italian peninsula. These waters host exceptional specialised<br />
organisms <strong>of</strong> marine origin, like the sponge Higginsia ciccaresei, the<br />
gastropod Salenthydrobia ferrerii, the ostracods Trapezic<strong>and</strong>ona stammeri<br />
<strong>and</strong> Pseudolimnocythere hypogea, the thermosbaenacean Monodella<br />
stygicola, the extraordinary metaingolfiellid amphipod Metaingolfiella<br />
mirabilis, the hadziid amphipod Hadzia minuta, the salentinellid Salentinella<br />
gracillima, mysids <strong>of</strong> the genera Spelaeomysis <strong>and</strong> Stygiomysis, <strong>and</strong> the large<br />
decapod Typhlocaris salentina.<br />
Tyrrhenian <strong>and</strong> Sardinian provinces. This province includes Sardinia, part <strong>of</strong><br />
the Tuscan archipelago <strong>and</strong> isolated coastal areas in Italy deriving from the<br />
fragmentation <strong>of</strong> the Tyrrhenid, which started in the Oligocene. Palaeo-<br />
Tyrrhenian endemics are phylogenetically similar to evolutionary lines in the<br />
areas <strong>of</strong> Provence, the Pyrenees <strong>and</strong> Corsica. Among the several Sardinian<br />
endemics, the gastropod genera Sardhoratia <strong>and</strong> Sardopaladilhia, m<strong>any</strong><br />
species <strong>of</strong> cyclopoid <strong>and</strong> harpacticoid copepods, the bathynellacean<br />
Sardobathynella, the entire phyletic line <strong>of</strong> isopods related to Proasellus patrizii,<br />
<strong>and</strong> isopods <strong>of</strong> the genus Stenasellus, are also found along the Tuscan coast.<br />
Also presumably <strong>of</strong> palaeo-Tyrrhenian origin are the thermosbenacean<br />
Tethysbaena argentarii <strong>of</strong> Mount Argentario (Tusc<strong>any</strong>) <strong>and</strong> the amphipod<br />
Metacrangonyx ilvanus <strong>of</strong> the isl<strong>and</strong> <strong>of</strong> Elba. Other animals associated with local<br />
anchialine water are m<strong>any</strong> amphipods <strong>of</strong> marine origin <strong>of</strong> the genera Bogidiella<br />
<strong>and</strong> Pseudoniphargus, <strong>and</strong> the subgenus Thyrrenidiella <strong>of</strong> genus Ingolfiella.<br />
More doubtful are the relationships between some gammarid genera, like<br />
Longigammarus, Tyrrhenogammarus, <strong>and</strong> the puzzling Ilvanella.<br />
Iblean province (Sicily). Sicilian stygobionts are biogeographically composite<br />
<strong>and</strong> little known, especially those living in the alluvial plains <strong>and</strong> karstic<br />
aquifers that sometimes develop in chalk. Clearly identified organisms are<br />
found in the Iblean area, especially in the water-table <strong>of</strong> the karstic system<br />
near Porto Palo. Although this small area is jeopardised by man-made<br />
alterations, exceptional, perhaps palaeo-Mediterranean endemics inhabit it,<br />
like the thermosbaenacean Tethysbaena syracusae, the cirolanid isopod<br />
Typhlocirolana aff. moraguesi, <strong>and</strong> the amphipods Tyrrhenogammarus<br />
catacumbae <strong>and</strong> Pseudoniphargus duplus.<br />
Examples <strong>of</strong> distribution <strong>of</strong> endemic stygobiont species; left: gastropods <strong>of</strong> the genus Paladilhiopsis<br />
(Eastern Pre-Alps, red circles) <strong>and</strong> Arganiella (Apennines, green circles); right: crustaceans <strong>of</strong> genera<br />
Stenasellus (Tyrrhenian, red circles), Spelaeomysis (Apulia, blue circles) <strong>and</strong> Tyrrhenogammarus<br />
(T. catacumbae, Iblean Mts, Sicily, green circles)<br />
77
Ecology<br />
DIANA MARIA PAOLA GALASSI<br />
Although Stygobiology - the science<br />
that studies groundwater biology -<br />
dates back to the 18th century, it was<br />
only in 1994 that the ecological<br />
importance <strong>of</strong> this environment was<br />
finally acknowledged <strong>and</strong> exhaustively<br />
described in the monograph<br />
Groundwater Ecology (see select<br />
bibliography). No matter how surprised<br />
we may be to learn that findings in<br />
groundwater ecology are recent, our<br />
surprise turns to shock on hearing<br />
that, although groundwater protection<br />
<strong>and</strong> management are <strong>of</strong> paramount<br />
importance for human survival, current<br />
legislation does not take into account<br />
the ecology <strong>of</strong> this particular<br />
Bottom <strong>of</strong> an old well for drinking-water<br />
environment.<br />
This is probably due to the unique characteristics <strong>of</strong> groundwater: invisible to<br />
most, not perceived as part <strong>of</strong> the territory, a totally dark world populated<br />
almost exclusively by tiny creatures. The biodiversity <strong>of</strong> this environment is<br />
truly “hidden”, as the subtitle <strong>of</strong> this volume suggests. This is perhaps the<br />
reason, albeit not a justifiable one, why man, in both law <strong>and</strong> culture, has<br />
always considered the exploitation <strong>of</strong> groundwater as more important than <strong>its</strong><br />
ecology. It is a narrow-minded view, as we realise when reading the previous<br />
chapter on the complexity, diversity <strong>and</strong> scientific importance <strong>of</strong> styg<strong>of</strong>auna.<br />
It therefore comes as no surprise that, while there are only a few books to<br />
describe the geological <strong>and</strong> speleological aspects <strong>of</strong> these habitats, almost<br />
none has yet been published in Italy on underground ecology. This chapter is<br />
an attempt at overcoming the anthropocentric view <strong>of</strong> groundwater, at<br />
illustrating how the ecosystem works, <strong>and</strong> analysing the ecological factors<br />
that regulate the structure <strong>of</strong> groundwater communities <strong>and</strong> biodiversity.<br />
Waterfall produced by the karstic spring <strong>of</strong> Col del Sole (Friuli Venezia Giulia)<br />
79
80 ■ The ecology <strong>of</strong> aquifers<br />
According to their hydrogeological <strong>and</strong> hydrological characteristics, aquifers<br />
are divided into three groups.<br />
Karstic aquifers are the most intensively studied from the biological<br />
viewpoint, perhaps because caves allow scientists easy access to them.<br />
These aquifers develop in large bedrock cavities, generally limestone,<br />
through a complex network <strong>of</strong> micro-fissures formed by the dissolution <strong>of</strong><br />
carbonates.<br />
This group includes waters that penetrate chalk, <strong>and</strong> that flow into<br />
conglomerate, in which dissolution acts on evaporites <strong>and</strong> the cementing<br />
matrix <strong>of</strong> breccia <strong>and</strong> puddingstone. In the hydrological cycle, karstic<br />
aquifers undergo great variations in flow <strong>and</strong>, therefore, from the ecological<br />
viewpoint, they are less predictable systems.<br />
Unsaturated (vadose) karstic systems, which are more directly influenced by<br />
rainfall, are less stable than saturated ones. However, the stability <strong>and</strong><br />
predictability <strong>of</strong> saturated karstic systems in turn depend on the age <strong>and</strong><br />
depth <strong>of</strong> aquifers. Generally, ancient, deep aquifers are ecologically more<br />
stable than young, shallow ones.<br />
Sketch showing the three main types <strong>of</strong> aquifers: fractured lithoid (A), porous (B), karstic (C) Hypotelminorheic habitat<br />
Porous <strong>and</strong> alluvial aquifers develop in unconsolidated sediments where<br />
interstices between sediment particles vary according to the particle size <strong>of</strong><br />
the sediment <strong>its</strong>elf.<br />
Porous aquifers may be divided into unsaturated or semi-saturated <strong>and</strong><br />
saturated (water-tables). Medium-fine porous aquifers have greater physical<br />
inertia <strong>and</strong>, as water lasts in them for longer than in karstic aquifers, they are<br />
ecologically more stable <strong>and</strong> predictable.<br />
In non-karstic lithoid (stone) aquifers, water circulates in fractures (as in<br />
crystalline rock), between layers (marl-s<strong>and</strong>stone in flysch facies) <strong>and</strong><br />
cavities <strong>of</strong> other origin (e.g., the lava flows <strong>of</strong> Mt. Etna). Water percolates in<br />
fissures whose size depends on the events that created them, <strong>and</strong> on the<br />
solubility <strong>and</strong> erodibility <strong>of</strong> rocks.<br />
Practically unknown from the ecological viewpoint, these aquifers are very<br />
similar to karstic ones if their fractures or cavities (as in lava tubes) are large,<br />
or behave like porous ones in the surface cortex, where soil <strong>and</strong><br />
disintegrated rock host communities typical <strong>of</strong> porous systems.<br />
Lastly, a particular mountain environment is found in leaf litter with trickling<br />
water underneath, the so-called hypotelminorheic habitat. This does not<br />
represent a true aquifer, but is surface water flowing a few centimetres deep.<br />
81
82<br />
Although the ecology <strong>of</strong> this unsaturated habitat is similar to that <strong>of</strong> porous<br />
surface aquifers, it is very unstable <strong>and</strong> unpredictable.<br />
Organisms from adjacent <strong>and</strong> underlying aquifers may migrate to these<br />
habitats to feed.<br />
The same aquifer <strong>of</strong>ten hosts more than one <strong>of</strong> the above categories: for<br />
instance, there are streams in cavities between flysch <strong>and</strong> limestone (in<br />
Friuli Venezia Giulia), between limestone <strong>and</strong> conglomerate (Veneto Pre-<br />
Alps), travertine <strong>and</strong> tuff (Latium), limestone <strong>and</strong> chalk (Grotte di Frasassi),<br />
limestone <strong>and</strong> lava (Lessini mountains), <strong>and</strong> limestone <strong>and</strong> granite<br />
(Sardinia).<br />
In addition, the water <strong>of</strong> karstic aquifers <strong>of</strong>ten drains to alluvial beds in<br />
valleys with complex hydrogeological <strong>and</strong> ecological relationships.<br />
■ Groundwater habitats<br />
The main ecological aspect deriving from the classification described above<br />
is that the various types <strong>of</strong> aquifers provide fauna with a complex availability<br />
<strong>of</strong> living space, with changes in structural complexity, food resources,<br />
stability <strong>of</strong> hydraulic conditions <strong>and</strong> water chemistry. Basically, different<br />
aquifers develop different habitats, <strong>and</strong> may host completely different<br />
animals.<br />
For instance, locally or extensively saturated karstic aquifers <strong>of</strong>ten have<br />
large hydric spaces (underground rivers or lakes), <strong>and</strong> therefore contain<br />
larger organisms which may reach a few centimetres in size, like large<br />
cirolanid isopods, mysids, decapods <strong>and</strong> the olm, the only Italian stygobiont<br />
vertebrate.<br />
Unsaturated karstic environments host smaller animals because the pools in<br />
caves - large pools or lakes <strong>of</strong> trickling water - are only transient habitats for<br />
fauna living in limestone micro-fissures above, adjacent to or underneath the<br />
pools.<br />
Medium-fine porous aquifers provide little living space, <strong>and</strong> only small<br />
animals - less than 1 cm long, <strong>of</strong>ten smaller than 1 mm, according to the<br />
size <strong>of</strong> particles - with particular adaptations have been able to colonise<br />
them.<br />
Fractured aquifers, in line with their nature, may <strong>of</strong>fer different extension <strong>of</strong><br />
living spaces, <strong>and</strong> therefore host relatively large animals (in flysch, amphipods<br />
<strong>of</strong> the genus Niphargus are up to 4 cm long) as well as microscopic organisms<br />
typical <strong>of</strong> porous systems.<br />
Unsaturated karstic habitat (micro-concretions) Porous habitat with (detail) a specimen <strong>of</strong> Niphargus in <strong>its</strong> environment<br />
83
84 85<br />
The discovery <strong>of</strong> a new submerged world: anchialine environments<br />
Diana Maria Paola Galassi<br />
Anchialine environments were first<br />
discovered in 1966, when the Austrian<br />
scientist Rupert Riedl described them<br />
as “marginal caves”. Since then,<br />
experts have debated the correct<br />
definition <strong>of</strong> anchialine systems. Today,<br />
they agree on defining them as caves<br />
or other underground aquatic habitats<br />
near the coastline <strong>of</strong> isl<strong>and</strong>s <strong>and</strong><br />
continents, supplied by continental<br />
freshwater <strong>and</strong> with underground<br />
connections to the sea. Consequently,<br />
the water <strong>of</strong> anchialine pools is<br />
brackish, <strong>and</strong> light-weight freshwater<br />
generally floats on top <strong>of</strong> heavier<br />
seawater.<br />
The most typical feature <strong>of</strong> anchialine<br />
environments is the absence <strong>of</strong> a<br />
surface connection with the sea, which<br />
manages to reach far inl<strong>and</strong> through<br />
deep infiltration passages in limestone<br />
<strong>and</strong> volcanic rocks.<br />
The most fascinating, extraordinary<br />
examples are the well-known Mexican<br />
cenotes, small bodies <strong>of</strong> crystalline<br />
brackish water, like blue eyes glittering<br />
in the tropical forests <strong>of</strong> Mexico <strong>and</strong><br />
Belize, not far from the coast. In Italy,<br />
typical anchialine pools are found in<br />
the Grotta Zinzulusa, Abisso <strong>and</strong> Buco<br />
dei Diavoli (Salento), together with<br />
other water-tables in Apulia,<br />
groundwater in Porto Palo (Sicily), the<br />
Grotta Verde, Grotta di Nettuno <strong>and</strong><br />
Grotta del Bue Marino (Sardinia) <strong>and</strong><br />
the Grotta di Punta degli Stretti<br />
(Argentario, Tusc<strong>any</strong>).<br />
Anchialine pools are marked by few<br />
food resources, total darkness, <strong>and</strong><br />
vertical gradients <strong>of</strong> salinity <strong>and</strong><br />
oxygen concentrations. Although in the<br />
past anchialine ecosystems were<br />
believed to support themselves on<br />
allochthonous organic matter (deriving<br />
from the rock above <strong>and</strong> from<br />
seawater), today we know that part <strong>of</strong><br />
the organic matter is locally<br />
synthesised by chemo-autotrophs.<br />
The most fascinating aspect that<br />
makes these environments true treasure<br />
troves <strong>of</strong> biodiversity is their exclusive<br />
fauna. Examples are remipedes, the<br />
most primitive class <strong>of</strong> living<br />
crustaceans, which have been found in<br />
anchialine caves on the Bahamas, in<br />
lava tubes on the isl<strong>and</strong> <strong>of</strong> Lanzarote<br />
<strong>and</strong>, more recently, in Australia.<br />
Remipedes, like m<strong>any</strong> other animal<br />
groups found in these habitats, are true<br />
living fossils, whose distribution,<br />
enigmatically uneven in several areas<br />
<strong>of</strong> the world, dates back to the breakup<br />
<strong>of</strong> the ancient Tethys Sea.<br />
In addition to these unique organisms,<br />
there are also other extraordinary<br />
animals, some <strong>of</strong> which are Italian<br />
endemics with restricted distribution,<br />
like the sponge Higginsia ciccaresei,<br />
the thermosbaenacean Monodella<br />
stygicola, the mysid Stygiomysis<br />
hydruntina, <strong>and</strong> the decapod<br />
Typhlocaris salentina.<br />
It is worth noting that the copepod<br />
Muceddina multispinosa was recently<br />
discovered in the Grotta Verde (Capo<br />
Caccia, Alghero, Sardinia), a species<br />
with disjunct distribution also found in<br />
anchialine environments on the isl<strong>and</strong>s<br />
<strong>of</strong> Mallorca <strong>and</strong> Lanzarote (Spain).<br />
Generally speaking, anchialine habitats<br />
host heterogeneous assemblages<br />
which includes strictly marine animals<br />
<strong>and</strong>, to a lesser degree, freshwater<br />
organisms.<br />
Typically anchialine species are closely<br />
associated with the particular<br />
environment in which they live, <strong>and</strong><br />
have never been found in other types <strong>of</strong><br />
underground habitats. They are also<br />
stygobionts, <strong>and</strong> have marked<br />
specialised features. Their origin dates<br />
back to various geological times, from<br />
the Tertiary to the more recent<br />
Sea entrance to the Grotta Zinzulusa (Salento, Apulia)<br />
Pleistocene. Some researchers believe<br />
that their ancestors lived in the abysses<br />
<strong>of</strong> the sea; others trace their origin back<br />
to organisms living in shallow seawater<br />
on the continental shelf.
86<br />
The Fontanon di Goriuda drains the karstic plateau <strong>of</strong> Mt Canin (Julian Pre-Alps, Friuli)<br />
Simplified sketch <strong>of</strong> a karstic aquifer<br />
■ Ecology <strong>of</strong> karstic aquifers<br />
The network <strong>of</strong> karstic condu<strong>its</strong> has two components that <strong>of</strong>fer different living<br />
conditions to fauna: transmissive <strong>and</strong> capacitive components. The transmissive<br />
component is typical <strong>of</strong> highly karstified systems with great hydraulic<br />
conductivity <strong>and</strong> fast currents <strong>and</strong>, ecologically speaking, has little biodiversity.<br />
What kind <strong>of</strong> species could possibly survive in such hostile environments? Yet<br />
some actually can, <strong>and</strong> have even been incredibly successful in adapting to<br />
these harsh habitats. For example, some amphipod crustaceans <strong>of</strong> the genus<br />
Niphargus have evolved adaptations to exploit the advantages <strong>of</strong> fast currents<br />
in habitats where interspecies competition is very low.<br />
Research carried out in France reveals that these species, which perhaps live<br />
in fissures adjacent to the transmissive/drainage conduit, lay their eggs<br />
nearby, <strong>and</strong> exploit the speed <strong>of</strong> the current to disperse their young. Briefly,<br />
they synchronise their biological cycle to the discharge <strong>of</strong> the aquifer while<br />
developing growth strategies typical <strong>of</strong> changeable habitats: thus, they<br />
produce large numbers <strong>of</strong> fertilised eggs, a few <strong>of</strong> which will reach the adult<br />
stage, in ways which are typical <strong>of</strong> surface species rather than underground<br />
ones. Some species <strong>of</strong> isopod crustaceans <strong>of</strong> the genus Monolistra also<br />
exploit fast currents by curling up into balls <strong>and</strong> letting themselves be<br />
transported over great distances.<br />
In capacitive karstic systems, whose development varies according to the<br />
aquifer, water percolates in medium-sized <strong>and</strong> small fractures in branching<br />
87
88<br />
anastomoses, <strong>of</strong>ten adjacent to the main drainage system. Here, they form<br />
small pools <strong>of</strong> calm water which are connected to one another <strong>and</strong> flow into<br />
the main drainage conduit. This lateral network, which is generally more<br />
extensive <strong>and</strong> has greater volume than the drainage one, is called the<br />
capacitive annex system. Unlike the drainage system, which poses a severe<br />
threat to the survival <strong>of</strong> species, the situation is completely reversed in the<br />
capacitive system, where water flows slowly <strong>and</strong> there are large amounts <strong>of</strong><br />
organic matter <strong>and</strong> inorganic sediments, creating habitats for m<strong>any</strong><br />
underground species. Biodiversity may even increase in capacitive systems<br />
with wide, diversified living environments, like underground lakes. Only in<br />
these habitats do we find plankton (calanoid copepods) together with benthic<br />
<strong>and</strong> interstitial organisms, large predators, like cirolanid isopods, large<br />
decapod crustaceans, <strong>and</strong> the olm.<br />
Unsaturated karstic systems also have a diversified network <strong>of</strong> storage micr<strong>of</strong>ractures,<br />
where living conditions are favoured by the three-dimensional<br />
complexity <strong>of</strong> the system. The diversity <strong>of</strong> substrates in small pools <strong>of</strong> water<br />
(pools <strong>and</strong> puddles with silt, clay, s<strong>and</strong> <strong>and</strong> organic material percolating from<br />
the surface, or complex calcium microstructures) give rise to diversified fauna,<br />
even if temporary water circulation prompts species to devise adaptations to<br />
withst<strong>and</strong> adverse conditions in small, locally saturated fractures.<br />
■ Ecology <strong>of</strong> alluvial aquifers<br />
Sketch illustrating connection between transmissive system <strong>and</strong> capacitive annex subsystem during flood <strong>and</strong><br />
drought periods Gravel bed <strong>of</strong> the Tagliamento (Friuli Venezia Giulia)<br />
The habitats <strong>of</strong> saturated porous aquifers are not very heterogeneous, <strong>and</strong><br />
conditions are determined by the size <strong>of</strong> sediment grains in unconsolidated<br />
sediments. Food is restricted, because most <strong>of</strong> the organic matter coming<br />
from the surface is trapped in the subsurface layers <strong>of</strong> aquifers.<br />
The opposite is observed in surface unconsolidated sediments, generally<br />
unsaturated, where the surface aquatic <strong>and</strong> terrestrial environments are<br />
continuous or adjacent, giving rise to heterogeneous habitats due to the<br />
ecotonal nature <strong>of</strong> these environments <strong>and</strong> the greater availability <strong>of</strong> organic<br />
matter.<br />
Proximity to wet or dry surfaces produces greater concentrations <strong>of</strong> organic<br />
matter than in deeper saturated layers, thus contradicting the now out-dated<br />
idea that underground habitats <strong>lack</strong> niches <strong>and</strong> habitats.<br />
The hyporheic environment (where groundwater <strong>and</strong> surface water mix) is<br />
perhaps the most typical example <strong>of</strong> a subsurface alluvial aquifer <strong>and</strong> is,<br />
among underground habitats, certainly the best-known from the ecological<br />
viewpoint. It is an ecotone, that is, a transitional area between the surface<br />
habitat <strong>of</strong> running water (stream or river) <strong>and</strong> the saturated underground<br />
habitat (groundwater).<br />
89
90<br />
Literature defines this environment in myriad ways, each a nuance <strong>of</strong> the<br />
other, the only differences being the thickness attributed by each expert to<br />
the hyporheic layer. Aquatic ecotones are areas in which large-scale hydraulic<br />
exchanges occur <strong>and</strong> where biogeochemical activity - more intense than in<br />
adjacent habitats - affects the quality <strong>of</strong> water flowing through the interface.<br />
Hyporheic environments thus regulate water flow, <strong>and</strong> temporarily or<br />
permanently store organic, mineral <strong>and</strong> sometimes polluting matter. The<br />
microbial <strong>and</strong> animal components in them actively modify the timing <strong>and</strong><br />
volume <strong>of</strong> nutrient <strong>and</strong> pollutant flows. From the structural viewpoint, the<br />
hyporheic zone is a matrix <strong>of</strong> permanently dark interstices saturated with<br />
water flowing slowly, with slight daily temperature variations <strong>and</strong> great<br />
bedrock stability. The hyporheic zone is an aphotic (without light), mechanical<br />
<strong>and</strong> biogeochemical filter between surface <strong>and</strong> underground water systems,<br />
ensuring their purification <strong>and</strong> maintenance.<br />
From this viewpoint, an important contribution came in 1993 from the<br />
American researchers Stanford <strong>and</strong> Ward with their concept <strong>of</strong> hyporheic<br />
corridor, which describes the connections <strong>and</strong> interactions between the<br />
hyporheic zone <strong>and</strong> the catchment basin. The role played by the hyporheic<br />
corridor in a catchment basin is essential for m<strong>any</strong> ecological processes<br />
associated with nearby water sources: 1) the primary productivity in the<br />
Three-dimensional (longitudinal, transversal, vertical) nature <strong>of</strong> a river system<br />
stream above the hyporheic zone is strongly influenced by the distribution<br />
<strong>and</strong> frequency on the vertical scale <strong>of</strong> zones <strong>of</strong> upwelling (where the watertable<br />
supplies the stream), outwelling (areas where subsurface water supplies<br />
the stream laterally) <strong>and</strong> downwelling (areas where surface water supplies the<br />
water-table) <strong>of</strong> the stream, because the last two are usually richer in algal<br />
nutrients like nitrates <strong>and</strong> phosphates than surface water; 2) the temporal <strong>and</strong><br />
spatial variability <strong>of</strong> processes <strong>of</strong> hydric exchange cause biodiversity in the<br />
hyporheic zone to increase more than in the adjacent water-table <strong>and</strong> surface<br />
habitats.<br />
Although Italian rivers are relatively well-known from the hydrological,<br />
biological <strong>and</strong> ecological viewpoints, an integrated overview <strong>of</strong> the Italian<br />
river ecosystem is still missing. Research emphasises a lateral dimension,<br />
i.e., the relationships between stream beds <strong>and</strong> surrounding floodplain <strong>and</strong><br />
river areas in particular; a longitudinal dimension, i.e., the variations occurring<br />
along the length <strong>of</strong> rivers, from spring to outlet, although little is known about<br />
the vertical dimension, i.e., the relationships <strong>of</strong> rivers with their underlying<br />
aquifers. And the spatial scale is even less well-known in <strong>its</strong> temporal<br />
evolution. This three-dimensional spatial view, with the addition <strong>of</strong> a fourth<br />
temporal dimension, is the so-called four-dimensional nature <strong>of</strong> a river<br />
ecosystem (as defined by Ward).<br />
Spring at the base <strong>of</strong> a deposit <strong>of</strong> glacial origin (Pederù, South Tyrol)<br />
91
92 93<br />
The saline springs <strong>of</strong> Poiano: the importance <strong>of</strong> biological markers<br />
Fabio Stoch · Mauro Chiesi<br />
The Poiano Springs are the largest<br />
karstic springs in Emilia Romagna (mean<br />
discharge exceeding 400 l/s), <strong>and</strong> the<br />
main drainage system <strong>of</strong> groundwater<br />
flowing in the Triassic chalk <strong>of</strong> the Upper<br />
Val Secchia. Unlike other springs in the<br />
area, the Poiano Springs contain salt,<br />
with concentrations <strong>of</strong> dissolved sodium<br />
chloride between 5 <strong>and</strong> 7 g/l. Between<br />
autumn 2005 <strong>and</strong> spring 2007, the Trias<br />
Project (a research project by the<br />
Società Speleologica Italiana for the<br />
Ente Parco Nazionale dell’Appennino<br />
Tosco-Emiliano) was carried out on the<br />
Poiano aquifer, with automatic<br />
collection <strong>of</strong> the main environmental<br />
parameters (temperature, electric<br />
conductivity, pH, discharge) <strong>and</strong><br />
continual collection <strong>of</strong> fauna by means<br />
<strong>of</strong> a net placed at the mouth <strong>of</strong> the<br />
spring. Geological <strong>and</strong> hydro-chemical<br />
tests showed that the chalk outcrops<br />
from which the springs gush are the top<br />
portion <strong>of</strong> a still active diapir, i.e., a<br />
chalk mass intruding vertically upwards<br />
because <strong>of</strong> <strong>its</strong> low density, bringing with<br />
it rock-salt, which makes the aquifer<br />
salty. Surface water, which infiltrates a<br />
few kilometres upstream through<br />
swallow holes, takes a few days to<br />
reach <strong>and</strong> mix with this salty water. This<br />
had led geologists to believe there was<br />
Nitocrella psammophila (left, 100 x), Niphargus poianoi (top, right, 6 x) <strong>and</strong> Pseudolimnocythere sp.<br />
(bottom, right, 100 x)<br />
a simple conduit system in the chalk<br />
bedrock, a typical feature <strong>of</strong> evaporites.<br />
The high content <strong>of</strong> sodium chloride is a<br />
limiting factor for biodiversity in the<br />
Poiano aquifer. Only three species <strong>of</strong><br />
stygobiont crustaceans were collected<br />
from the springs: the harpacticoid<br />
Nitocrella psammophila <strong>and</strong> the ostracod<br />
Pseudolimnocythere sp., both <strong>of</strong> ancient<br />
marine origin, <strong>and</strong> the endemic<br />
amphipod Niphargus poianoi. However,<br />
contrary to previous ideas, biological<br />
research revealed that the conduit<br />
system does not carry to the springs the<br />
stygoxenic <strong>and</strong> stygobiotic organisms<br />
found in the streams flowing into swallow<br />
holes, none <strong>of</strong> which were collected in<br />
the Poiano Springs. Besides, the<br />
numbers <strong>of</strong> harpacticoids <strong>and</strong> ostracods<br />
coming from the springs are larger in<br />
periods <strong>of</strong> drought than in periods during<br />
which the aquifer is recharging, which<br />
suggested that the conduit system has a<br />
large groundwater basin. The integration<br />
<strong>of</strong> geological <strong>and</strong> biological research<br />
methods therefore enabled scientists to<br />
gain a better hydro-dynamic picture <strong>of</strong><br />
the aquifer, <strong>and</strong> also revealed the<br />
unexpected presence <strong>of</strong> endemic<br />
species which had colonised the<br />
groundwater in the past <strong>and</strong> which are<br />
therefore now valuable bioindicators.<br />
Trends (measured during analysis) <strong>of</strong> discharge, precipitation <strong>and</strong> numbers <strong>of</strong> drifted stygobionts in<br />
the Poiano springs
94 ■ Ecology <strong>of</strong> springs<br />
95<br />
The perennial underground stream <strong>of</strong> the Pod Lanisce cave (Julian Pre-Alps, Friuli Venezia Giulia)<br />
Springs are like windows opening<br />
on the underground environment -<br />
Botosaneanu, a Romenian researcher,<br />
defined them as “the gates to the river<br />
Styx”. They are <strong>of</strong>ten the only means<br />
<strong>of</strong> analysing aquifers, because they are<br />
composed <strong>of</strong> surfacing groundwater<br />
which filters into recharge zones at<br />
different times, <strong>and</strong> reach spring<br />
points due to gravity. Springs may<br />
therefore be studied from the “outside”<br />
to analyse surface organisms<br />
colonising the crenal zone (thus, crenobiology), or from the “inside”, to<br />
examine the fauna <strong>of</strong> the aquifers supplying them - the stygian zone (thus,<br />
stygobiology).<br />
Springs are particular physical environments which have constant temperature<br />
over time <strong>and</strong> sometimes undergo changes in the chemical composition <strong>of</strong> their<br />
waters, due to the nature <strong>of</strong> the aquifers supplying them. These parameters<br />
define extreme natural situations. For instance, according to their thermic<br />
regime, there are thermal springs (like those in the Euganean Hills (Veneto),<br />
which host an endemic species <strong>of</strong> gastropods <strong>of</strong> the genus Heleobia) <strong>and</strong><br />
glacial ones (such as those in the Adamello-Brenta, between Lombardy <strong>and</strong><br />
Trentino, which are colonised by endemic stygophilic harpacticoid copepods).<br />
Brackish springs are saline (like the Poiano springs in Emilia Romagna, whose<br />
exclusive guest is the stygobiotic amphipod crustacean Niphargus poianoi),<br />
<strong>and</strong> those with particular values <strong>of</strong> pH <strong>and</strong> hydrogen sulphide, i.e., sulphuric<br />
springs, which are found throughout Italy <strong>and</strong> <strong>its</strong> isl<strong>and</strong>s.<br />
■ Groundwater inhabitants<br />
Sulphuric spring: the saline waters <strong>of</strong> Nirano<br />
(Emilia Romagna)<br />
The “darkness syndrome”. Contrary to ideas in the past, the underground<br />
environment can host great biodiversity. As described in the previous section,<br />
groundwater species may be divided into stygoxenes, stygophiles <strong>and</strong><br />
stygobionts, according to their degree <strong>of</strong> dependency on this habitat for their<br />
survival.<br />
Stygobionts are species which are exclusive to groundwater <strong>and</strong> have<br />
developed special adaptations to life in this habitat. All their adaptations
96<br />
Modified sensory setae on the antennule <strong>of</strong> a male harpacticoid (top: ca. 2000x; bottom: ca. 4000x,<br />
photo by SEM, scanning electron microscopy)<br />
define the so-called “darkness<br />
syndrome”, a condition made up <strong>of</strong> a<br />
series <strong>of</strong> morphological, physiological<br />
<strong>and</strong> behavioural changes that these<br />
species underwent during their<br />
evolution in the geological past, which<br />
brought their ancestors from surface<br />
waters to the underground ecokingdom.<br />
According to how species<br />
react to the underground environment,<br />
adaptations are distinguished from<br />
Aesthetasc on antennule <strong>of</strong> a harpacticoid (ca.<br />
8000x, SEM photo)<br />
specialisations. Adaptations are strategies developed by species as<br />
responses to what are called the macrodescriptors <strong>of</strong> the underground<br />
environment, like constant darkness <strong>and</strong> scarce organic matter. Specialisation<br />
is the reaction to microdescriptors <strong>of</strong> the various types <strong>of</strong> habitats found in the<br />
hypogean environment in general.<br />
Groundwater organisms are depigmented (white, transparent or translucent),<br />
or sometimes pinkish (haematic pigments are visible through their semitransparent<br />
bodies), <strong>and</strong> their visual organs are generally small<br />
(microphthalmy) or totally absent (anophthalmy). Clearly, in totally dark<br />
environments, there is no advantage in having functioning visual organs or<br />
similarly, exhibiting gaudy colours. But it is more complex to underst<strong>and</strong> what<br />
the disadvantages could be in maintaining these characteristics, since these<br />
same disadvantages <strong>of</strong>ten caused them to become extinct over time.<br />
Generally speaking, if an organism has a particular feature that is neither an<br />
advantage nor a disadvantage, a r<strong>and</strong>om neutral mutation may occur, causing<br />
that feature to disappear. In addition, if there is also an energy advantage,<br />
because during the ontogeny <strong>of</strong> these structures available energy can be used<br />
to develop compensatory sensory structures, then the loss <strong>of</strong> useless organs<br />
also has an adaptive logic. Presumably due to <strong>lack</strong> <strong>of</strong> resources, no stygobiont<br />
has developed the complex structures typical <strong>of</strong> animals living in sea abysses<br />
(like bio-luminescence). Moreover, pre-adaptive dynamics cannot be ruled<br />
out: in surface populations made up <strong>of</strong> both blind <strong>and</strong> sighted individuals,<br />
spatial segregation <strong>of</strong> blind phenotypes in groundwater <strong>and</strong> survival <strong>of</strong> sighted<br />
individuals in surface water may have given rise, over time, to two different,<br />
ecologically isolated genotypes. However, the evolutionary dynamics that led<br />
stygobionts to lose their eyes are still being discussed, as even within the<br />
same species eyes may show different evolutionary stages - for example, in<br />
some isopod, amphipod <strong>and</strong> decapod crustaceans.<br />
97
98<br />
The <strong>lack</strong> <strong>of</strong> eyes or their functional atrophy is generally accompanied by<br />
hypertrophic (excessively developed) alternative sensory organs for life in a<br />
dark world, where smelling or touching the surrounding space is the only way<br />
<strong>of</strong> sensing the approach <strong>of</strong> predators or potential prey, finding a partner, or<br />
making one’s way in three-dimensional space, large or small. The body<br />
surfaces <strong>of</strong> stygobionts are therefore covered with sensory organs, which have<br />
different shapes according to species. For instance, crustaceans have<br />
aesthetascs, setae with m<strong>any</strong> chemoreceptors sensitive to chemical stimuli,<br />
<strong>and</strong> thigmoreceptors, end-organs which respond to touch <strong>and</strong> enable<br />
organisms to find their way around by feeling the lake bed or single s<strong>and</strong><br />
particles in interstitial environments. Stygobiont crustaceans living in free<br />
water sometimes have longer antennules than their surface relatives. These<br />
modified cephalic appendages are used to sense at distance: it is better to<br />
know in advance if a predator is coming, before it is too late to escape! In<br />
stygobionts, the compensatory length <strong>of</strong> sensory appendages is contrasted<br />
by clearly rudimentary locomotory appendages, which are much smaller than<br />
those <strong>of</strong> their close relatives living on the surface, <strong>and</strong> generally with fewer<br />
segments, setae <strong>and</strong> spines. This adaptation is actually a type <strong>of</strong><br />
specialisation, as it is typical, or even exclusive, to interstitial species.<br />
The interstitial environment <strong>of</strong> hyporheic zones <strong>of</strong> rivers, springs <strong>and</strong> karstic<br />
springs covered by alluvial sediments has one great disadvantage: living<br />
Body elongation favours movement in the interstitial habitat<br />
spaces are restricted. In these narrow habitats, movement is confined, <strong>and</strong><br />
walking species, let alone swimmers, are rare. Most <strong>of</strong> their time is spent<br />
moving around single s<strong>and</strong> particles, feeding on the bacterial bi<strong>of</strong>ilm covering<br />
the surface. Long legs would only hinder movement. This morphological<br />
adaptation is accompanied by a reduction in body size, as stygobiont species<br />
are generally smaller than their surface relatives. It is no coincidence that<br />
shorter legs <strong>and</strong> smaller bodies are <strong>of</strong>ten associated. The most probable<br />
reason is that these adaptations are the result <strong>of</strong> developmental heterochrony.<br />
Heterochrony. This is a deviation from<br />
the typical developmental sequence <strong>of</strong><br />
formation <strong>of</strong> organs <strong>and</strong> parts as a<br />
factor in evolution, both in animals<br />
with discontinuous development (with<br />
larval stages separated by moults)<br />
<strong>and</strong> those with continuous, gradual<br />
transformations into adults.<br />
Although there are various types <strong>of</strong><br />
heterochrony, the most commonly<br />
found in underground environments<br />
are progenetic paedomorphosis (also<br />
known as progenesis) <strong>and</strong> neoteny.<br />
Why has heterochrony been so<br />
successful in the colonisation <strong>of</strong><br />
groundwater?<br />
Progenesis is the process by which<br />
Evolutionary dynamics <strong>of</strong> stygobiont progenesis<br />
features <strong>of</strong> the sexually mature animal<br />
develop precociously. The result <strong>of</strong> this deviation is a reproductively mature<br />
adult which preserves the morphological <strong>and</strong>/or physiological characteristics<br />
typical <strong>of</strong> juvenile or larval stages. These small adults <strong>of</strong>ten look like larvae<br />
<strong>and</strong>, if they are metameric (segmented) animals or have segmented body<br />
appendages, they may have fewer metameres <strong>and</strong> segments than they would<br />
if they had developed normally. But what is the advantage <strong>of</strong> being small?<br />
Obviously, it enables these animals to creep <strong>and</strong> wriggle into tiny interstitial<br />
spaces. Although heterochrony is the result <strong>of</strong> modifications - genome<br />
alterations which are generally disadaptive - it actually provides free admission<br />
to interstitial environments. It may therefore be a pre-adaptation, i.e., nonadaptive,<br />
<strong>and</strong> at times a neutral character or set <strong>of</strong> characters acquired in their<br />
original habitats (i.e., surface water) which may become useful when<br />
99
100<br />
Theoretical evolutionary sequence which, starting from a large surface-living ancestor (1), through<br />
evolutionary steps (2-4), may have led to a progenetic interstitial species (5)<br />
organisms find themselves in new<br />
environments. M<strong>any</strong> <strong>of</strong> the<br />
evolutionary lines in stygobiotic<br />
crustaceans (copepods, ostracods,<br />
bathynellaceans, thermosbenaceans,<br />
asellid isopods, ingolfiellid <strong>and</strong><br />
bogidiellid amphipods) originated in<br />
this way.<br />
Another type <strong>of</strong> heterochrony is<br />
neoteny. The final result is the same:<br />
sexually mature adults that look like<br />
larvae. In this case, the dynamics are<br />
different, because larval development<br />
is so slow that individuals reach<br />
sexual maturity without having<br />
completed their larval development. In<br />
this case, animals may grow to the<br />
same size or larger than their nonheterochronic<br />
relatives. The classic<br />
Elongation <strong>of</strong> the first antenna in the amphipod<br />
Hadzia fragilis stochi (ca. 8x)<br />
example <strong>of</strong> neoteny in underground environments is provided by the olm.<br />
Stygobiont animals also have physiological adaptations to life underground,<br />
like low metabolic rates <strong>and</strong> slow body growth, longevity, reduced fecundity,<br />
larger eggs richer in yolk (enabling embryos to survive for longer periods), <strong>and</strong><br />
less frequent reproduction, <strong>of</strong>ten independent <strong>of</strong> the season <strong>and</strong> occurring<br />
throughout the year.<br />
However, like all generalisations, this too has <strong>its</strong> exceptions. For instance, in<br />
open karstic environments, some Niphargus species depend on the seasons.<br />
In particular, in spring, when aquifers increase their discharge due to<br />
snowmelt, <strong>and</strong> surface water carries larger amounts <strong>of</strong> organic matter, the<br />
biological cycle <strong>of</strong> these animals is timed in order to produce their juvenile<br />
stages which exploit the greater amount <strong>of</strong> food in order to develop.<br />
Other adaptive strategies. Another characteristic <strong>of</strong> all interstitial organisms<br />
is body elongation, which makes even phylogenetically distant taxa acquire a<br />
common worm-like shape (turbellarians, annelids, crustaceans <strong>and</strong> mites).<br />
The advantage is that their bodies are capable <strong>of</strong> wriggling into tiny interstices.<br />
Only a few ethological strategies for survival in particular underground<br />
environments are known. In hyporheic habitats, mainly in the upper layers <strong>of</strong><br />
river sediments, where current velocity may be considerable, animals without<br />
101
102<br />
Harpacticoid female <strong>of</strong> Morariopsis aff.<br />
scotenophila with only one egg per sac<br />
(ca. 100x)<br />
adhesive organs to cling to the<br />
sediments may curl around single<br />
particles, to prevent being carried<br />
away by the current. This is the case <strong>of</strong><br />
oligochaetes, harpacticoid copepods<br />
<strong>and</strong> amphipods with elongated<br />
bodies. Others may become globose<br />
(some isopods <strong>and</strong> amphipods), <strong>and</strong><br />
drift with the current to colonise new<br />
habitats.<br />
Another strategy adopted by<br />
crustaceans is gender segregation in<br />
spatial niches, to avoid intraspecific<br />
competition. When sampling a<br />
particular underground environment,<br />
scientists <strong>of</strong>ten collect larger numbers<br />
<strong>of</strong> males or, vice versa, <strong>of</strong> females. In<br />
addition to the sex ratio, which in<br />
nature is notably in favour <strong>of</strong> females,<br />
in interstitial environments, males <strong>and</strong> females may occupy microhabitats at<br />
different depths. Although little is known <strong>of</strong> the ethology <strong>of</strong> underground<br />
species, some male copepods occasionally re-clasp (mate with the same<br />
female) to ensure their paternity.<br />
Reproductive strategies. Until recently, the underground ecosystem was<br />
thought to be simple, stable <strong>and</strong> predictable. In fact, scientific research has<br />
proven this axiom invalid, at least for some habitats.<br />
Generally speaking, in physically predictable but ecologically unfavourable<br />
environments, species adopt a demographic strategy called A-selection<br />
(Adversity Selection), based on slow development <strong>and</strong> low fecundity in stressful<br />
environments with few resources <strong>and</strong> predictable changes. However, when<br />
habitats are still physically predictable <strong>and</strong> food resources are more abundant,<br />
species may turn to K-selection strategy, whereby populations grow to the<br />
carrying capacity <strong>of</strong> the environment. In this condition, intraspecies competition<br />
<strong>and</strong> predation may also become important for population dynamics. When<br />
environments are physically unpredictable but provide great food resources,<br />
there may be exponential population growth followed by plummeting figures<br />
when resources are no longer available: this is known as r-selection. Clearly, a<br />
single model cannot be applied to all underground species.<br />
■ The food-chain<br />
A classic description <strong>of</strong> underground environments is generally made by<br />
comparing <strong>its</strong> physical <strong>and</strong> biological organisations with those <strong>of</strong> surface<br />
environments. For example, groundwater is permanently dark <strong>and</strong> has no<br />
nyctemeral (day-night) cycle, whereas surface water is illuminated by the sun,<br />
<strong>and</strong> therefore does have a day-night cycle. This condition influences the<br />
biological <strong>and</strong>, equally importantly, the energy characteristics <strong>of</strong> the<br />
ecosystem. Lack <strong>of</strong> light results in detritus food-chains because there are no<br />
photosynthetic organisms (green plants) <strong>and</strong> very few chemo-autotrophic<br />
organisms (ones feeding on oxidised inorganic chemical compounds). These<br />
are bacteria that exploit chemical energy instead <strong>of</strong> light energy, <strong>and</strong><br />
synthesise organic compounds from carbon dioxide. One <strong>of</strong> the typical<br />
locations is the Movile Cave (Romania), where these organisms are primary<br />
producers <strong>and</strong> the entire food-chain relies on them. There are also examples in<br />
Italian groundwater, an underground stream in the Grotte di Frasassi (Marches)<br />
<strong>and</strong> sulphuric basins in the Grotta del Fiume Sotterraneo in the Lepini<br />
mountains (Latium), which are still being studied.<br />
Therefore, with very few exceptions, the entire groundwater ecosystem is<br />
not self-sufficient, but depends on inputs <strong>of</strong> organic matter from terrestrial<br />
Sulphur spring in the cave <strong>of</strong> Cala Fetente (Capo Palinuro, Campania)<br />
103
104<br />
Sketch showing degrading phases <strong>of</strong> particulate organic matter (POM) <strong>and</strong> <strong>its</strong> entry into the hyporheic<br />
environment (see text for abbrevations)<br />
<strong>and</strong> aquatic surface environments - defined by the French researcher Rouch<br />
as “epigean manna”. Due to the <strong>of</strong>ten total absence <strong>of</strong> primary producers,<br />
the aquatic underground environment is oligotrophic, i.e., deficient in<br />
nutrients <strong>and</strong>, as such, incapable <strong>of</strong> supporting long food-chains. There are<br />
only a few examples <strong>of</strong> dystrophic underground environments, which are<br />
periodically or occasionally filled with dissolved humic matter coming from<br />
the surface.<br />
Eutrophic conditions are associated with sudden increases in organic matter<br />
due to pollution. This happens in some saturated karstic habitats in periods <strong>of</strong><br />
intense rainfall. Rain <strong>and</strong> surface organic matter percolate into aquifers<br />
through effective infiltration pathways, giving rise to large-scale although<br />
short-lived increases in organic matter available to biota. Similar events occur<br />
in unsaturated karstic environments, such as concretions <strong>and</strong> pools <strong>of</strong><br />
trickling water in springs or hyporheic habitats, where the quantity <strong>of</strong> organic<br />
matter depends on the season. Clearly, the type <strong>of</strong> aquifer greatly affects the<br />
amounts <strong>of</strong> food available to underground communities, <strong>and</strong> may produce<br />
distinct community organisations.<br />
Most underground organisms are therefore detrivorous <strong>and</strong> feed on particles <strong>of</strong><br />
organic matter produced by the decomposition <strong>of</strong> dead animal <strong>and</strong> plant<br />
organisms. This ingested matter is divided into two categories: Coarse<br />
Particulate Organic Matter (CPOM), with particles >1 mm, <strong>and</strong> Fine Particulate<br />
Organic Matter (FPOM), with particles 0.5 µm. Occasionally, some<br />
small organisms may feed on Dissolved Organic Matter (DOM) with particle<br />
sizes
106<br />
Hierarchical approach to the study <strong>of</strong> underground ecosystems: from large regional to small microhabitat<br />
scales<br />
Functional redundancy is a rare<br />
phenomenon in groundwater ecosystems,<br />
i.e., each trophic role is<br />
generally played by one or a few<br />
species, <strong>and</strong> there is little competition<br />
at each link <strong>of</strong> the food-chain.<br />
For the same reason, the ecosystem is<br />
certainly extremely vulnerable, as<br />
communities have low inertia (capacity<br />
for withst<strong>and</strong>ing human disturbance<br />
unaltered). In fact, the extinction <strong>of</strong> one<br />
species <strong>of</strong> the community may bring<br />
the entire food-chain to a halt, with<br />
irreversible consequences for the<br />
whole ecosystem. M<strong>any</strong> underground<br />
species are therefore “key species”, as<br />
conservationist biologists call them.<br />
■ Stygodiversity: groundwater biodiversity<br />
Groundwater in a Tuscan cave<br />
Several factors contribute towards the spatial <strong>and</strong> temporal distributions <strong>of</strong><br />
the so-called stygodiversity, <strong>and</strong> they may be both historical (palaeoclimatic,<br />
palaeogeographical <strong>and</strong> palaeoecological events) <strong>and</strong> ecological. The<br />
structure <strong>and</strong> functioning <strong>of</strong> underground aquatic ecosystems are the result <strong>of</strong><br />
complex processes that may act in different ways at different spatial - <strong>and</strong><br />
temporal - levels. These factors are therefore studied at continental or regional<br />
scale (mega- or macro-scale), aquifer (meso-scale) <strong>and</strong> microhabitat level<br />
(micro- or fine-scale). These scales are a series <strong>of</strong> spatial configurations fitting<br />
one into the other, <strong>and</strong> each level integrates the processes occurring at lower<br />
levels <strong>and</strong> is associated with others at the same level. This hierarchical<br />
subdivision into continental, regional, <strong>and</strong> sometimes aquifer levels allows us<br />
to focus on the palaeogeographical <strong>and</strong> palaeoclimatic events that influenced<br />
the origin <strong>of</strong> biodiversity in groundwater.<br />
The origin <strong>of</strong> stygobionts in fresh groundwater is double. Some <strong>of</strong> them evolved<br />
from ancestors living in continental surface freshwater (lakes <strong>and</strong> rivers) - most<br />
hydrobiid gastropods, cyclopoid copepods <strong>and</strong> m<strong>any</strong> canthocamptid<br />
harpacticoids, asellid isopods, niphargid amphipods <strong>and</strong> olms - <strong>and</strong> are called<br />
limnicoid stygobionts. Others - polychaetes, parvidrilid oligochaetes,<br />
amphipods <strong>of</strong> the genera Hadzia <strong>and</strong> Salentinella, microcerberid,<br />
107
108 109<br />
Stygodiversity in the Presciano springs: a pilot experiment<br />
Diana Maria Paola Galassi · Barbara Fiasca<br />
The Presciano springs make up one <strong>of</strong><br />
the three great sources giving rise to the<br />
river Tirino in Abruzzi, at the foot <strong>of</strong> the<br />
greatest karstic aquifer in the<br />
Apennines. They have proved to be<br />
excellent natural laboratories for<br />
scientific research on the environmental<br />
factors affecting the spatial distribution<br />
<strong>of</strong> groundwater species (the spring area<br />
does not exceed 2000 m 2).<br />
This spring system is structurally<br />
complex, as a heterogeneous alluvial<br />
layer lies on strongly karstified bedrock,<br />
covering the underlying karstic aquifer.<br />
This situation has enabled researchers<br />
to examine how the different types <strong>of</strong><br />
sediments affect the composition <strong>of</strong><br />
underground communities.<br />
Detailed samplings have revealed that<br />
stygoxenic, stygophilic <strong>and</strong> stygobiont<br />
species are not at all homogenously<br />
distributed in the small spring area<br />
Presciano springs (Abruzzi)<br />
As depth increases, the relative<br />
importance <strong>of</strong> stygobionts increases to<br />
the detriment <strong>of</strong> other ecological<br />
categories, while stygophiles are<br />
generally found at intermediate depths<br />
(at 30 <strong>and</strong> 70 cm below the spring bed).<br />
This vertical distribution is a direct<br />
consequence <strong>of</strong> the ecological<br />
characteristics <strong>of</strong> stygobionts, which are<br />
morphologically <strong>and</strong> physiologically<br />
adapted to life in deep habitats, <strong>and</strong> <strong>of</strong><br />
stygophiles, a transitional category that<br />
clearly prefers ecotonal areas.<br />
Stygoxenes are scattered, especially in<br />
subsurface sites, perhaps restricted by<br />
the low temperatures <strong>and</strong> oligotrophic<br />
conditions <strong>of</strong> the spring environment.<br />
Further analysis, carried out by<br />
dividing fauna living in karstic sites from<br />
that <strong>of</strong> alluvial sites, shows that<br />
stygophiles are almost exclusively<br />
found in the latter habitat.<br />
In addition, alluvial sites characterized<br />
by heterogeneous grain-size<br />
composition, with clearly alternating<br />
temporal upwelling <strong>and</strong> downwelling<br />
phases, host greater biodiversity, as<br />
they provide more ecological niches<br />
than karstic sites, <strong>and</strong> contain greater<br />
quantities <strong>of</strong> organic matter, which is<br />
trapped in interstices.<br />
Copepod taxocoenoses, the most<br />
important group in the analysed springs,<br />
are found in alluvial sites, with 15 out <strong>of</strong><br />
the 17 species collected in the entire<br />
spring system. Instead, karstic sites<br />
host more monotonous karstic fauna,<br />
with one harpacticoid copepod<br />
(Nitocrella pescei) making up 90% <strong>of</strong><br />
the entire assemblage. However, it is<br />
precisely in karstic sites that we find the<br />
most biogeographically interesting<br />
species, Pseudectinosoma reductum, a<br />
relict <strong>of</strong> ancient marine origin.<br />
Nitocrella pescei<br />
Distribution <strong>of</strong> ecological categories (number <strong>of</strong><br />
specimens) at various depths (in cm)
110<br />
microparasellid <strong>and</strong> cirolanid isopods, ameirid <strong>and</strong> ectinosomatid harpacticoids<br />
<strong>and</strong> mysids - are related to taxa that are still living in marine environments <strong>and</strong><br />
are called thalassoid stygobionts. The current distribution <strong>of</strong> stygobiont species<br />
is the result <strong>of</strong> an ever-changing mosaic <strong>of</strong> communities which have evolved on<br />
a geological time-scale <strong>and</strong> whose composition is still evolving.<br />
A particularly interesting aspect <strong>of</strong> the development <strong>of</strong> stygodiversity, which<br />
has long been debated by scientists, is the large number <strong>of</strong> relict species in<br />
underground communities. Some underground systems conserve species <strong>and</strong><br />
even entire taxonomic groups related to now extinct ancient surface fauna (in<br />
one <strong>of</strong> his books, the French biologist René Jeannel spoke <strong>of</strong> cave-dwelling<br />
“living fossils”). Events like the Pleistocene glaciations, sea regressions <strong>and</strong><br />
transgressions, <strong>and</strong> the salinity crisis <strong>of</strong> the Mediterranean have long been the<br />
focus <strong>of</strong> scientific debates on the origin <strong>of</strong> underground fauna.<br />
Some scientists believe stygobionts to be the “survivors” <strong>of</strong> surface<br />
populations which had taken refuge underground to escape harsh surface<br />
conditions (this “refugium” hypothesis goes back to the ideas <strong>of</strong> Charles<br />
Darwin). Others view colonisation as a continuous, ongoing process (the<br />
“active colonisation” hypothesis).<br />
Karstic spring (Friuli Venezia Giulia)<br />
According to the “refugium” theory,<br />
tropical regions, which were not<br />
affected by catastrophic events, would<br />
have scarce underground fauna; most<br />
importantly, surface populations, the<br />
ancestors <strong>of</strong> stygobionts, would<br />
generally have become extinct in<br />
geographical areas which underwent<br />
drastic climatic changes.<br />
Further knowledge has proved that<br />
both these theories were partly wrong,<br />
<strong>and</strong> suggested a new evolutionary<br />
scenario, according to which the<br />
present structure <strong>of</strong> stygodiversity has<br />
several causes. First, the extinction <strong>of</strong><br />
surface populations is not a m<strong>and</strong>atory<br />
prerequisite for speciation in<br />
The endemic gastropod Bythiospeum calepii<br />
underground habitats. We already<br />
mentioned this when describing the coexistence <strong>of</strong> pigmented, eyed species<br />
<strong>of</strong> crustaceans with depigmented, anophthalmic or totally blind ones - m<strong>any</strong><br />
cases are known in Italy, especially for crustaceans <strong>of</strong> the genera Proasellus,<br />
Synurella <strong>and</strong> Gammarus. These are examples <strong>of</strong> ongoing active colonisation<br />
<strong>of</strong> groundwater not associated with dramatic changes in the surface<br />
environment. Stygobionts have also been found in all kinds <strong>of</strong> habitats in<br />
tropical areas - lava tubes on volcanic isl<strong>and</strong>s, cenotes in Mexico, caves in<br />
Somalia, anchialine systems in Australian deserts <strong>and</strong> in the caves <strong>of</strong> small<br />
isl<strong>and</strong>s in the Caribbean, <strong>and</strong> in Brazilian caves, inhabited by multitudes <strong>of</strong><br />
blind fish - thus definitively contradicting the “refugium” hypothesis as the only<br />
explanation for the origin <strong>of</strong> underground communities.<br />
Although groundwater colonisation may occur independently <strong>of</strong> unfavourable<br />
conditions in the environments lying above, dramatic climatic <strong>and</strong> geological<br />
changes in surface habitats may in fact suddenly interrupt the genetic flow<br />
between hypogean <strong>and</strong> epigean populations. This explains the origin <strong>of</strong><br />
“relicts”, both eco-geographical (separated from their closest surface relatives -<br />
still living <strong>and</strong> sometimes well diversified) <strong>and</strong> phyletic (the last survivors <strong>of</strong> a<br />
now extinct surface evolutionary line).<br />
Phyletic relicts are very interesting from the scientific viewpoint. Entire<br />
taxonomic groups (like bathynellaceans <strong>and</strong> thermosbaenaceans) belong to<br />
this category, <strong>and</strong> their closest relatives can no longer be found among the<br />
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animal groups still living on the surface. However, since the chronology <strong>of</strong><br />
colonisation <strong>and</strong> speciation is hard to establish, a solution has been found in<br />
the so-called “molecular clocks”, which synchronise DNA mutations in living<br />
organisms with palaeogeographical <strong>and</strong> palaeoclimatic events. An example is<br />
afforded by the examination <strong>of</strong> Sardinian, Provençal <strong>and</strong> Tuscan species <strong>of</strong><br />
stenasellid isopods, living evidence <strong>of</strong> the ancient tectonic fragmentation <strong>of</strong><br />
the Tyrrhenian plate <strong>and</strong> drifting <strong>of</strong> the Sardinian-Corsican continental plate<br />
<strong>and</strong> <strong>its</strong> fragments from what is now Provence towards present-day Italy.<br />
Although necessary for speciation, vicariance (i.e., the splitting <strong>of</strong> the area <strong>of</strong><br />
the old species into two parts separated by boundaries) is not only associated<br />
with these ancient, wide-ranging events, <strong>and</strong> may occur on <strong>any</strong> scale, from<br />
small, isolated fractures in karstic systems, to continents. Vicariant events may<br />
be geoclimatic <strong>and</strong> ecological: obviously, the efficiency <strong>of</strong> these “boundaries”<br />
is closely related to the ecology <strong>of</strong> the species, especially their aptitude for<br />
dispersal. M<strong>any</strong> stygobiont species are not prone to dispersal, <strong>and</strong> show<br />
Affinities between Provençal, Sardinian-Corsican <strong>and</strong> coastal Tyrrhenian fauna are explained by their<br />
common palaeogeographic history<br />
Niphargus similis, found in relict sites in glacialised areas <strong>of</strong> the Alpine chain<br />
limited geographic distribution (they are strict endemics). Furthermore, the low<br />
fecundity, benthic larval development <strong>and</strong> low dispersal potential <strong>of</strong> m<strong>any</strong><br />
interstitial crustaceans suggest that continuous <strong>and</strong> jump dispersal are quite<br />
rare in these groups. This is why stygobionts can be used as excellent<br />
historical (palaeogeographical) indicators, their descriptive capacity being<br />
similar to that <strong>of</strong> true fossils.<br />
Among the events that modelled present-day Italian styg<strong>of</strong>auna, the best<br />
known are certainly glaciations <strong>and</strong> sea regressions. The Quaternary<br />
glaciations depleted underground fauna in large areas <strong>of</strong> Italy, thus leading to<br />
the total absence <strong>of</strong> entire stygobiont genera <strong>of</strong> gastropods, copepods,<br />
isopods <strong>and</strong> amphipods north <strong>of</strong> the boundary <strong>of</strong> the Würmian glaciation. Sea<br />
regression, associated with glacial eustatism, trapped several taxa in coastal<br />
sediments, giving rise to stygobization. Very ancient regressive events led<br />
fauna <strong>of</strong> marine origin to become relicts, enigmatically confined <strong>and</strong> unevenly<br />
distributed in continental groundwater far from coastlines (amphi-Atlantic,<br />
Caribbean-Mediterranean, Caribbean-Mediterranean-Australian). In this case,<br />
the gr<strong>and</strong>iose movements <strong>of</strong> plate tectonics were the main cause <strong>of</strong><br />
relictualisation <strong>and</strong>, in the Mediterranean area, gave rise to the so-called<br />
Tethyan relicts, which date back to the dis<strong>appearance</strong> <strong>of</strong> the ancient Tethys<br />
Sea in the Oligocene.<br />
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