Review Paper Changing Paradigms in Groundwater Ecology – from

Internat. Rev. Hydrobiol.
93
2008
4–5
565–577
DOI: 10.1002/iroh.200711045
DAN LUCA DANIELOPOL*, 1 and CHRISTIAN GRIEBLER2
1
Commission of the Stratigraphical and Palaeontological Research of Austria,
Austrian Academy of Sciences c/o – Institute of Earth Sciences (Geology and
Palaeontology), University of Graz, Heinrichstraße 26, A-8010 Graz, Austria;
e-mail: [email protected]
2
Helmholtz Center Munich – German Research Center for Environmental
Health (GmbH), Institute of Groundwater Ecology, Ingolstaedter Landstraße 1,
D-85764 Neuherberg, Germany
Review Paper
Changing Paradigms in Groundwater Ecology – from the
‘Living Fossils’ Tradition to the ‘New Groundwater Ecology’
key words: aquatic ecology, biodiversity, groundwater ecosystems, subterranean organisms
Abstract
Groundwater ecology merged during the second part of the 20th century with modern ecological
practice after having adopted the ‘ecosystem concept’. The latter was first applied to karstic systems
and separately for alluvial non-consolidated aquifers along surface running waters. Today groundwater
ecosystems are studied within a multi- and transdisciplinary framework at various spatial and temporal
scales by experts dealing with microbiology, the ecology and systematics of meio- and macro-fauna,
geochemistry, hydrogeology and mathematical modelling. A further paradigmatic change occured with
the recognition that subterranean assemblages of organisms are formed by both hypogean and epigean
taxa. The biological diversity in subterranean ecosystems can be much higher than earlier thought
and may even exceed surface diversity in some taxa. This largely unrecognized biodiversity in many
cases deserves environmental protection. A third phase in the development of groundwater ecology
has occured over the last 15 years with the incorporation of socio-economic research topics within
groundwater ecology (GIBERT et al., 1994a) and in this sense today we have the “New Groundwater
Ecology”.
We should cling to our traditions and do what we can to keep the understanding of the world in
which we live as a resource for all humankind
COLIN S. REYNOLDS, 2001: Limnology in the New Century: 21 Topics for Research. –
Limnology 1, p. 17
1. Introduction
The discipline of groundwater ecology started to develop during the end of the 19th century with natural history observations about organisms living in subsurface habitats accessible to humans. Aquatic animals in European caves impressed deeply men especially after
the discovery of the cave salamander Proteus anguinus LAURENTI 1768 (BELLÉS, 1992). A
first synthesis of scientific information on subterranean organisms and their ecological and
evolutionary problems was published by RACOVITZA (1907). For about 50 years after the
publication of RACOVITZA’S “Essays” subterranean environments were perceived by those
* Corresponding author
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D. L. DANIELOPOL and C. GRIEBLER
who studied it as very stressful biotopes, occupied by highly specialised organisms, especially invertebrate animals. BREHM (1908, p. 448) called this type of research „Forschung
ungewöhnlicher Lebensbezirke“ (Research on anomalous districts of life) and considered
it of huge interest. In the same way, many naturalists during the first part of 20th century
were impressed by the “peculiar” aspects of groundwater environments and its inhabitants:
(i) the extreme oligotrophy of many cave water habitats, (ii) the relative thermal stability of
the subsurface, (iii) the reduced organismic diversity and (iv) for some species their reduced
abundance. Beside this, many species that were described belong to old phylogenetic lineages of which surface living relatives went extinct especially during the Quaternary ice age.
Therefore the subterranean aquatic animals belonging to such lineages were seen as relicts
or “living fossils” of a pre-glacial epigean fauna (cf. THIENEMANN, 1950). During the first
part of the 20th century several generations of naturalists investigated subterranean habitats
in order to sample strictly stygobiotic animals. One could call this period, a pre-ecological
phase of groundwater research where the emphasis was more on cataloguing new species,
their habitats and their biogeographical origin. It was the pioneering work of J. SCHWOERBEL
during the 1960s (e.g., SCHWOERBEL, 1961) on the superficial layers of gravel and sands
along rivers and streams, the so-called hyporheic zone, that allowed to obtain a high number
of subsurface animals and to study their phenology. It is this period, which paved the way
for the emergence of modern groundwater ecology. At the same time, ecological aspects of
cave fauna were first studied under experimental conditions in a special cave laboratory in
Southern France (review in ROUCH, 1986).
It is well accepted today that microbes constitute the major group of organisms in groundwater ecosystems, both in terms of biomass and activity. However, microbiological research
on groundwater and the subterranean underground arose with a considerable delay. Although
first observations of groundwater microbiota date back to ANTONI VAN LEEUWENHOEK in
1677, the systematic investigation started only a few decades ago. The interest in subsurface microbial life was related to technical and hygienic problems in drinking water and oil
production such as the corrosion and clogging of pipes. Nevertheless the effective birth of
subsurface microbiology involved the development of aseptic sampling techniques in the
beginning of the 1980s (e.g., DUNLAP et al., 1977). Since then the ubiquitous presence of
microbes in the subsurface has been demonstrated (e.g., GHIORSE and WILSON, 1988). The
increasing awareness of the importance of microbiota in biogeochemical processes and subsequently for ecosystem functioning and services, including the purification of water and the
degradation of contaminants shaped the subsurface microbiology and made it an ambitious,
innovative and modern scientific discipline. However, the linkage between microbial ecology and the ‘traditional’ groundwater (faunal) ecology is still in its infancy.
The incorporation of the concept of ecosystem structure and functioning into subsurface
aquatic ecology during the 1970s in Europe represents the first major paradigm change
within the field of groundwater ecology (review in GIBERT et al., 1994b), which we will
refer to as the ‘ecosystem paradigm’. We use the concept of paradigm by KUHN (1970) with
its expanded meaning (cf. COHEN, 1985, p. 26): “a set of shared methods, standards, modes
of explanation, or theories, or a body of shared knowledge”. To groundwater microbiology
the “ecosystem paradigm” was applied in the 1980s (GHIORSE and WILSON, 1988). In the
following pages we provide a brief outline of some of the main aspects and interesting issues
in the development of groundwater ecology.
The development of ecosystem research in groundwater ecology was complemented especially from 1990s onwards, by a new perception that the biological diversity in dynamic
ecosystems is more important than earlier conceived (DANIELOPOL et al., 2000a; GRIEBLER
and LUEDERS, 2008). This novel view on the biodiversity of subterranean aquatic organisms
in relation to ecosystem functioning represents the next important paradigm switch that we
will highlight.
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Changing Paradigms in Groundwater Ecology
Recently, groundwater ecology again entered a new era. Along with the development
and reorganization of European water directives, and especially with the initiation of the
new European Groundwater Directive (DIRECTIVE 2006/118/EC) ecological research on
groundwater received social and political recognition marked by various efforts to incorporate ecological know-how into schemes for environmental planning and policies
(STEUBE et al., 2008). This implies the reinforced linkage of the various disciplines in
groundwater sciences, what will further stimulate and speed up the ecosystem approach.
We consider this trend as one of the promising developments of the “New Groundwater
Ecology” (DANIELOPOL et al., 2007).
2. The Ecosystem Approach as Major Paradigm Change
Traditionally, the investigation of caves accessible to men was the predilection object for
faunistical investigations during the first half of 20th century (BELLÉS, 1992). The positive
perception of the E. ODUM’s book “ Fundamentals of Ecology”, reprinted in many editions
(cf. ODUM, 1971) and subsequent ideas on the ecosystem functioning during the 1960s and
1970s stimulated in Europe a major change in the way karst environments were approached
from an ecological point of view (ROUCH, 1986). In this period a multidisciplinary group
of biologists, hydrogeologists, and geochemists, at the French “Laboratoire Souterrain” in
Moulis, southern France, investigated a complex karst system called Baget. The Baget karst
was approached at a landscape scale with a surface drainage leading to an infiltration basin,
from where the water circulated underground within a structured hydrologic pattern, before
finally reemerging at the surface where it contributes to the epigean stream systems. The main
organising process in the Baget system was found the way water flows through the karst.
Hydrologists (MANGIN, 1975) noticed that the aquatic system in the karst could be divided
in two subsystems, the infiltration sub-system and the flooded (saturated) sub-system. Within
the saturated zone large conduits and fissures through which surface water carrying organic
matter and many surface dwelling meio- and macro-organisms transits rapidly may be distinguished, and an annex system were water is stored for longer periods of time and which
comes in contact with the main draining system only periodically. In this annex system,
generally not directly accessible to men who explore caves, accumulate a high number of
strictly stygobiotic animals. The multi-disciplinary approach was instrumental in identifying
and defining the concept of the ‘karstic ecosystem’, with two components a physical and
a biological one, as a basic functional unit in groundwater ecology (ROUCH, 1977; 1986).
This concept was further validated by the study of another large karst system (the Dorvan)
where the dynamics of meio- and macro-fauna were related to the dynamics of the energetic
resources imported and modulated by the hydrologic regime (GIBERT, 1986). The important
progress achieved through this new way of looking at the subterranean ecology was partly
due to the conceptual approach but also depended on methodological innovation, for example, that of filtering the outflow of karstic systems at springs during long-term hydrologic
events. This approach made clear that cave life provided a very incomplete vision on how
life is organised and evolved in the subsurface of rock systems.
Ecosystem studies in unconsolidated alluvial sediments in and along running waters were
developed especially along the Rhône River by the “Lyon group” (cf. MARMONIER et al.,
2000). The innovation of their approach was that the shallow alluvial aquifer was studied in
close connection with the dynamics of the surface terrestrial and aquatic systems, at the level
of a wetland landscape. This expanded our vision on the way we can monitor and/or protect
not only the aquatic systems but also the groundwater dependent ecosystems.
In the Danube wetlands, near Vienna DANIELOPOL and his colleagues inspired by the karst
ecosystem research of the “Moulis group” developed a slightly different ecosystem approach
combining the holistic view with a reductionistic one (cf. DANIELOPOL et al., 2000b; 2001).
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D. L. DANIELOPOL and C. GRIEBLER
Macro-organisms
Meio-organisms
Micro-organisms
1.000
100
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0
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10
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log Depth [m]
Lake
10
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10.000
Aquitard
Temperature limit
for life
Impermeable rock
100.000
Figure 1. The subterranean domain. Major types of groundwater organisms and its distribution within
the subsurface are highlighted. The water carrying energy and matter through the subsurface passes
through local, intermediate and regional flow-systems characterized by different water residence times
(modified from DANIELOPOL et al., 2003).
They selected a small aquifer unit with finite limits and studied it for more than ten years
through a range of spatial and temporal scales.
The biodiversity, distribution and role of mircoorganisms were not a major focus in the
above mentioned ecosystem studies and thus hardly considered. While microbiologists in
the 1980s and 1990s concentrated on selected places of interest, such as individual spectacular caves (e.g., CUNNINGHAM et al., 1995), the hyporheic zone (e.g., ELLIS et al., 1998)
or contaminated areas within aquifers (e.g. HAACK and BEKINS, 2000), modern subsurface
microbial ecology tries to integrate the ecosystem approach. A pioneering study on the
microbial communities of a cave ecosystem was conducted by S. SÂRBU and colleagues,
who could show that microbial chemolithoautotrophy has the potential to energetically fuel
a subsurface ecosystem (SÂRBU, 2000). Recent examples for a more detailed investigation of
microbial biocoenoses are available for individual karstic systems (e.g., SIMON et al., 2001;
FARNLEITNER et al., 2005). The research group of K. PEDERSEN in Sweden has for 15 years
worked to achieve a holistic understanding on the microbial life in deep granitic rock, from
the detection of autochthonous bacteria, its distribution and activities (e.g., PEDERSEN, 1997),
the identification of autotrophic methanogens and acetogens, first microeucaryotes (e.g.,
EKENDAHL et al., 2003), to the measurement of high numbers of bacteriophages in the rock
to a depth of 450 m below land surface (KYLE et al., 2008). Several other working groups
around the world similarly contributed to a better understanding of subsurface microbiology
(see reviews of GHIORSE and WILSON, 1988; MADSEN and GHIORSE, 1993; CHAPELLE, 2001;
GOLDSCHEIDER et al., 2006; GRIEBLER and LUEDERS, 2008). The application of the ecosystem
approach to groundwater microbiology has been significantly impeded because most microorganisms in the subsurface live attached to surfaces and their investigation thus takes an
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Changing Paradigms in Groundwater Ecology
enormous effort, applying drilling and coring, to get a comprehensive view on subsurface
microbial life. It is therefore not surprising to date that only a minute part of the terrestrial
subsurface has been scientifically explored. Despite this, we now have much greater insight
into the subterranean realms and recognise that they are complex, dynamic and diverse largescale ecosystems (cf. Fig. 1).
3. The Present-Day Perception of the Subterranean Biodiversity
As mentioned in the introduction to this review the subterranean domain became famous
during the first period of the groundwater ecology by the documentation of a high number of
relict species perfectly adapted to their living environment. With the incorporation of modern
ecological concepts, such as the (i) relation between spatial and temporal heterogeneity of
the environment and biodiversity, (ii) the role of stability and disturbance for organismic
assemblages and ecosystem functioning and (iii) the importance of longitudinal, lateral and
vertical patterns (summarized in MARMONIER et al., 1993; GIBERT et al., 1994b; GRIEBLER
and MÖSSLACHER, 2003; GRIEBLER and LUEDERS, 2008 among others), it became clear during the last 30 years that when one speaks on subterranean biodiversity whole assemblages, including both transient surface dwelling organisms as well as the peculiar stygobiotic
representatives have to be integrated (ROUCH and DANIELOPOL, 1997). The realisation that
such assemblages have high biological diversity required new explanations of its origin.
Additional to this change in perception new sampling techniques offered serious quantitative data for subterranean organisms. Using the sampling technique of BOU and ROUCH, a
suction pump for animals living in gravel and sandy sediments, and long-term filtration of
exurgencies for karstic systems (review in POSPISIL, 1992) first allowed the documentation
of unexpected abundant and diverse meio-and macro-organismal assemblages (cf. GIBERT
and DEHARVENG, 2002). For instance, in surface running waters such as the Rhône river
system one finds 2 species of amphipods (Crustacea) in the surface water but 11 species in
the interstitial fauna (DOLE-OLIVIER et al., 1994). The karstic Edwards aquifer in the United
States contain 12–13 species of amphipods, the Postojna-Planina cave system and/or the
Baget karst contain more than 20 species of harpacticoids (LONGLEY, 1981; ROUCH and
DANIELOPOL, 1997).
Another trigger which modified our vision on the diversity of subterranean fauna, was the
application of molecular tools which, for example, helped to identify subterranean populations as cryptic species, formerly considered to belong to geographical widely dispersed
taxa (SBORDONI et al., 2000). The trend for recognition of many morphological species
to be genetically different continues and in many cases the use of genetic methods allow
also the reconstruction of the origin and the history of entire phylogentic lineages (e.g.,
ZAKŠEK et al., 2007; TRONTELJ et al., 2008). Today, there is a fair acceptance that subterranean waters are in many cases surprisingly rich in invertebrate species with the meaning
of a KUHNIAN paradigm. Some geographical areas like the Slovenian Karst represent classic
examples of faunal hot-spot diversity centres (SKET, 1999). The view of high subterranean
biodiversity is well presented in the CULVER and WHITE’s (2005) “Encyclopedia of caves”,
where no more than six articles deal with this topic.
Biodiversity is also a main focus within the microbial ecology of groundwater ecosystems.
However, the new microbial ecology does not go for sheer biodiversity collection but looks
for the aim towards enhancing our understanding of the role of biodiversity with respect
to the in situ activity of specific biogeochemical processes and, at its best, to ecosystem
functioning and services (GRIEBLER and LUEDERS, 2008). The major paradigm change in
this context must be seen in the development of cultivation-independent techniques for the
analysis of natural microbial communities in the mid-1990s (AMANN et al., 1995). Despite
the ‘unexpected’ high morphological diversity in unconsolidated aquifers described by P.
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D. L. DANIELOPOL and C. GRIEBLER
HIRSCH and colleagues in the late 1980s and early 1990s (e.g., HIRSCH et al., 1992), today’s
knowledge on microbial diversity in pristine groundwater ecosystems may be summarized as
follows: (i) in comparison to more productive systems such as surface waters and terrestrial
environments microbial diversity is low, (ii) anthropogenic perturbation does in most cases
cause an increase in diversity, and finally (iii) several, mostly uncultured, lineages and phyla
have been detected, which however, can be found also in other environments; so to date
there is no evidence for endemic groundwater microbiota. Two hypotheses may explain these
observations. First, the applied molecular tools are still not sophisticated enough to detect
microbial minorities, respectively low abundant as well as rare species. Second, pristine
groundwater communities are operating at a given minimum diversity, so that any perturbation is more likely to cause a shift in or increase in biodiversity rather than a loss. Yet there
are numerous indications that subsurface microbial communities are distinct from those
found in surface soil and aquatic environments. This distinction does not become apparent
on the level of phyla or genera, but rather by the specific assembly of groundwater microbial
communities and by their special physiological capabilities. A comprehensive review on
the microbial diversity in groundwater ecosystems is found in GRIEBLER and LUEDERS
(2008).
4. Groundwater Ecology and Socio-Economic Aspects
Healthy aquifers, without doubt, deliver important ecosystem services to society; e.g., the
purification of incoming surface water and recharge and the storage of high quality (drinking) water over decades and in significant quantities. We are dependent on groundwater
for food production and for domestic, agricultural and/or industrial use. Besides that, the
functioning of many terrestrial and surface aquatic ecosystems directly depends on groundwater and vice versa, Gibert et al., 2008-09-10. Only very recently, legislation started to
consider groundwater not only as a resource but as a living ecosystem, as argued in the
new EU Groundwater Directive (DIRECTIVE 2006/118/EC). In its 5th research frame programme the EU financed an international course on groundwater ecology open to students
from water works, legal authorities and universities and organised by D. L. DANIELOPOL in
Vienna (Austria) in 1999, as a first attempt to improve education in ecological disciplines
(GRIEBLER et al., 2001). Step by step, groundwater and aquifers have been altered in their
‘political’ consideration from an abiotic resource to ecosystems, which can clearly be seen
as a paradigm change. In our opinion, the assessment of ecosystems requires the consideration of ecological criteria (STEUBE et al., 2008). So far, no such criteria are available for
groundwater systems despite ecological status assessment being routine for surface aquatic
ecosystems. It is now with groundwater ecologists to come up with ‘ecological measures’,
such as bioindicators, ecotoxicological thresholds and other bioquality parameters and propose programmes designed to protect whole groundwater systems for both practical and
scientific purposes (GIBERT et al., 2005, 2008). Within these concepts, diverse subterranean
assemblages of organisms have to be integrated in the environmental protection schemes.
Therefore diverse groundwater assemblages are now being more thoroughly mapped, so that
in Europe we could document that the Danube Flood Plain in the Austrian National Park
represents the 4th world hot spot diversity area for groundwater organisms (DANIELOPOL
and POSPISIL, 2001). Another hot spot is found in Western Australia in an area supposed to
become heavily altered in the near future by mining activities (HUMPHREYS, 1999). In the
frame of a German national research project supported by the Federal Environment Agency
(Umweltbundesamt) STEUBE et al., 2008 intend the development of a first concept for the
ecological assessment of groundwater ecosystems considering microorganisms as well as
invertebrates as biological quality units, besides the physical-chemical parameters commonly
monitored.
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5. Discussions and Conclusion
T. S. KUHN (1970) in “The structure of scientific revolutions” proposed the idea of paradigm change as an explanation for the advancement of scientific knowledge within large
conceptual steps (metaphorically called scientific revolutions). We briefly showed that for
the advancement of groundwater ecology, the progress was mainly based on (i) the adaptation of general ecological concepts already known from other ecological domains as well
as (ii) on the inter- and multi-disciplinary cooperation within scientific disciplines. These
approaches need to continue and, without doubt, be further improved. To emphasize the
need for a transdisciplinary research platform, colleagues from different disciplines were
asked to complete two-dimensional Stommel diagrams stating on the spatial and temporal
scale of individual abiotic and biotic parameters and processes (Fig. 2). This exercise shall
demonstrate that the various scientific disciplines in groundwater sciences usually work
on different scales in turns of spatial and temporal resolution. More than this, the scale of
investigation does not necessarily meet the scale of interest, as often it is a matter of the
potential resolution of methods or even traditions (idea: H. EISENMANN). The outcome of
future cooperations will highly depend on speaking a trans-disciplinary scientific language.
Focus must therefore be on the development of new concepts bridging spatial and temporal
scales within individual ecosystems as well as within scientific disciplines. We are convinced
that modern groundwater ecology bringing together micro- and macro ecology and traditional groundwater related disciplines carries the potential to generate new paradigms in the
future. Ecological questions on (i) the structure of groundwater food webs, (ii) the tunnelling
of energy through the underground and recycling of carbon and nutrients (e.g., the role of
microbial chemolithoautotrophy), (iii) the link between biodiversity and ecosystem functioning in relation to different scales, and (iv) the self-purification potential of subsurface
ecosystems and its resistance and resilience towards anthropogenic impacts such as climatic
change, among others, awaits detailed investigation.
It is worth to mention that most of the scientists who contributed to the establishment of
the new paradigms discussed here were zoologists who became converted to the modern
ideas of ecology, e.g., R. ROUCH, who initiated and headed one of the first comprehensive
karst ecosystem projects. Other European specialists, like B. SKET and J. GIBERT, transferred
their wide evolutionary-ecology knowledge into groundwater protection programmes. The
improved mapping of the aquatic subterranean diversity is now used to better protect the
most valuable areas and/or endangered species (GIBERT et al., 2005). Similar activities can
also have been recognized outside Europe. In case of microbial ecology, one must say that
it has developed as a distinct subdiscipline of microbiology and now gradually approaches
the concepts and perspectives of ‘classical’ ecology. The development of comprehensive
paradigms for microbial and faunal ecology will be crucial for understanding groundwater
biodiversity and ecosystem function (GIBERT and DEHARVENG, 2002). The perception that
micro- and macroorganisms share many fundamental aspects of their biology and the recognition of the coupling of trophic interactions and microbial diversity from other aquatic
ecosystems underline the need for future collaboration in that direction.
KUHN subscribed to the idea that the advancement of science proceeds also through a
completely new way to develop research programmes. It is well expressed in the following
sentence: “only a change in the rules of the game could have provided an alternative …”
(KUHN, 1970, p. 40). In our case, the success of the ecosystem approach, at least in Europe,
is also related to a better way to fund and to administrate scientific activities. Starting with
1960, groundwater ecologists succeeded to get large inter- or multi-disciplinary projects
funded through national and international agencies. One nice example is the PASCALIS
project funded in the 5th frame program of the European Community (GIBERT, 2001), which
can be termed huge in comparison to the small projects dealt by single researchers like
J. SCHWOERBEL, T. ORGHIDAN or S. HUSSMANN during 1950. Not surprising, along with the
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Figure 2. Two-dimensional Stommel diagrams highlighting the spatial and temporal scale of various
abiotic and biotic parameters and processes (idea: H. EISENMANN).
improved funding modern techniques for field research and/or for experimental laboratory
work have been developed and working groups expanded.
It is important to mention here also the gradual change in perception of groundwater ecology over time within and among the communities of environmental scientists and those of
the policy – makers. Earlier research completed during 1950 – 1980 was practically ignored
in surveys dealing with the progress of aquatic ecology (cf. MCINTOSCH, 1985). With the
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Cultural patterns & attitudes
Society
Environment
Ecosystem status
Local conditions
Biodiversity,
structure &
funtions of the
ecosystem
Technology
Economics
national
regional
local
Integration
Economics and demography
Policy
Implementation on different levels
International
Social acceptance of political decisions
Site management
Groundwater ecosystem
Use of subsurface/groundwater
Figure 3.
Interacting domains and causal relations with respect to groundwater (modified from
NOTENBOOM, 2001).
rise of concern for groundwater pollution and/or protection of groundwater reserves at the
beginning the 1990s, the U.S. Environmental Protection Agency showed at various occasions
interest for the adoption of its decisions and regulations by more information derived from
ecological research (JOB and SIMONS, 1994) and a similar attitude can be observed in Europe.
At a recent European groundwater conference, at Vienna (2006), an invited presentation on
the importance of the groundwater ecology for EU Water Framework Directive was presented by one of the authors (DANIELOPOL et al., 2006a) and actively discussed. Meanwhile,
two more conferences organized by the International Association of Hydrological Sciences
(IAHS) and the International Association of Hydrogeologists (IAH) on ‘Hydrology and
Ecology’ in Karlovy Vary (Czech Republic) 2006 and on ‘Groundwater and Ecosystems’ in
Lisbon (Portugal) respectively, underline the efforts of bringing the traditional ‘hydrogeo’
and the ‘eco’ together. This is also true for the recognition of groundwater dependent ecosystems (BABA et al., 2006; HUMPHREYS, 2006).
The Swiss Water Protection Ordinance (GSCHV, 1998), is the first authority, which not
only defined water quality through physical-chemical standards for groundwater systems, but
also considered ecological criteria (“the biocenosis should be in a natural state adapted to
the habitat and characteristic of water that is not or only slightly polluted”), an idea which
was recently further supported inter alia by GOLDSCHEIDER et al. (2006), DANIELOPOL et al.
(2007) and STEUBE et al., 2008. At the same time a report on ‘Environmental Performance
Indicators for Groundwater’ prepared by BRIGHT and co-workers (1998) for the New Zealand
Ministry for the Environment already contained a first discussion on the use of groundwater
invertebrates as bioindicators. The development of the new European Groundwater Directive (EU-GWD), a daughter directive of the European Water Framework Directive (DIRECTIVE 2000/60/EC), in the last few years stimulated the discussion about the necessity and
perspectives in using ‘ecological status criteria’ in future groundwater monitoring schemes
(DANIELOPOL et al., 2004; 2006a). Released in December 2006, the EU-GWD now states
the importance of protective measures for groundwater ecosystems in its introductory sec-
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tion and it further quotes: “Research should be conducted in order to provide better criteria
for ensuring groundwater ecosystem quality” (DIRECTIVE 2006/118/EC). In our opinion that
is the official starting point for the definition of reliable ecological criteria, the design of
appropriate indices and the development of applicable assessment schemes, for what DANIELOPOL et al. (2007) called “The New Groundwater Ecology”. Hence we consider that under
the premises that the communication between researchers and policy-makers will positively
develop (cf. DANIELOPOL et al., 2006b), groundwater ecology will be well integrated into the
socio-economic context as represented in Figure 3.
6. Acknowledgements
We acknowledge Professor N. WALZ (Berlin) who invited us to contribute to the present
volume. We shared most of ideas with our colleagues involved in groundwater ecological
projects during the years. D.L.D. is much indebted to his colleagues, R. ROUCH, J. GIBERT,
P. POSPISIL, A. GUNATILAKA, P. MARMONIER, F. MÖSSLACHER, B. SKET, D. C. CULVER,
PH. QUEVAUVILLER, A. MANGIN, M. BAKALOWICZ, J. NOTENBOOM, V. SBORDONI, R. PSENNER,
F. SCHIEMER, the late G. BRETSCHKO and many others. Colleagues from the Institute of
Groundwater Ecology at the Helmholtz Center Munich, namely F. EINSIEDL, H. EISENMANN,
T. LUEDERS, P. MALOSZEWSKI, R. MECKENSTOCK, S. SCHMIDT are acknowledged for completing the 2D-Stommel diagrams. Research activities of D.L.D. in Austria have been supported during many years by the Austrian Academy of Sciences and the Austrian Science
Fund. Research activities of C.G. in Germany have been supported by the Helmholtz Center
Munich (former GSF), the Federal Ministry for Education and Research (B.M.B.F.) and are
currently financed by the German Research Foundation (D.F.G.) and the Federal Environment Agency (U.B.A.). The authors thank W. F. HUMPHREYS and an anonymous reviewer
for valuable comments.
7. References
AMANN, R., W. LUDWIG and K. H. SCHLEIFER, 1995: Phylogenetic identification and in situ detection of
individual microbial cells without cultivation. – FEMS Microbiol. Rev. 59: 143–169.
BABA, A., K. W. F. HOWARD and O. GUNDUZ, 2006: Groundwater and Ecosystems, Springer Verlag,
Dordrecht.
BELLÉS, X., 1992: From dragons to allozymes. A brief account on the history of biospeleology. – In:
CAMACHO, A. I. (ed.), The natural history of biospeleology, Museo Nacional Ciencias Naturales,
CSIC, Madrid, pp. 3–24.
BREHM, V., 1908: Die geographische Verbreitung der Copepoden und ihre Beziehungen zur Eiszeit. –
Internat. Rev. ges. Hydrobiol. Hydrogr. 1: 447–462.
BRIGHT, J., V. BIDWELL, C. ROBB, and J. WARD, 1998: Environmental performance indicator for groundwater. – Technical Paper No. 38 Freshwater, Ministry for the Environment, Wellington, New Zealand,
29 pp.
CHAPELLE, F. H., 2001: Groundwater microbiology and geochemistry. John Wiley and Sons, New
York.
COHEN, J. B., 1985: Revolution in science. – Harvard Univ. Press, Cambridge, MA., 711 pp.
CULVER, D. C. and W. B. WHITE, 2005: Encyclopedia of caves. – Elsevier Academic Press, San Diego,
CA, 654 pp.
CUNNINGHAM, K. I., D. E. NORTHUP, R. M. POLLASTRO, W. G. WRIGHT and E. J. LAROCK, 1995: Bacteria,
fungi and biokarst in Lechuguilla Cave, Carlsbad Cavers National Park, New Mexico. – Environ.
Geol. 25: 2–8.
DANIELOPOL, D. L., P. POSPISIL and R. ROUCH, 2000a: Biodiversity in groundwater: a large-scale view. –
Trends Ecol. Evol. 15: 223–224.
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.revhydro.com
Changing Paradigms in Groundwater Ecology
575
DANIELOPOL, D. L., P. POSPISIL, J. DREHER, F. MÖSSLACHER, P. TORREITER, M. GEIGER-KEISER, A. GUNATILAKA, 2000 b: A groundwater ecosystem in the Danube wetlands at Wien (Austria). – In: WILKENS,
H., CULVER, D.C. and HUMPHREYS, W. F. (eds.), Subterranean ecosystems, Ecosystems of the world,
30, Elsevier, Amsterdam, pp. 481–511.
DANIELOPOL, D. L. and P. POSPISIL, 2001: Hidden biodiversity in the groundwater of the Danube Flood
Plain National Park (Austria). – Biodiv. Conserv. 10: 1711–1721.
DANIELOPOL, D. L., P. POSPISIL, J. DREHER, 2001: Structure and functioning of groundwater ecosystems
in a Danube wetland at Vienna. – In: GRIEBLER, C., DANIELOPOL, D. L., GIBERT, J., NACHTNEBEL, H. P.
and NOTENBOOM (eds.), Groundwater ecology, a tool for management of water resources. – Office for
Official Publications of the European Publications, Luxenbourg, pp. 121–142.
DANIELOPOL, D. L., C. GRIEBLER, A. GUNATILAKA and J. NOTENBOOM, 2003: Present state and future
prospects for groundwater ecosystems. – Env. Conserv. 30: 104–130.
DANIELOPOL, D. L., J. GIBERT, C. GRIEBLER, A. GUNATILAKA, H. J. HAHN, G. MESSANA, J. NOTENBOOM,
and B. SKET, 2004: Incorporating ecological perspectives in European groundwater management
policy. – Env. Conserv. 31: 185–189.
DANIELOPOL, D. L., A. GUNATILAKA, J. NOTENBOOM, C. GRIEBLER, J. GIBERT, B. SKET, H. J. HAHN,
G. MESSANA, T. LÜDERS, J. GRIFFIOEN, J. LIEBICH and H.-J. ALBRECHTSEN, 2006a: Groundwater ecology as a necessary link to the EU Water Framework Directive. – In: Umweltbundesamt GmbH (ed.),
European Groundwater Conference 2006, Proceedings, Vienna, pp. 94–99.
DANIELOPOL, D. L., J. GIBERT and C. GRIEBLER, 2006b: Efforts of the European Commission to improve
communication between environmental scientists and policy-makers. – Environ. Sci. Pollut. Res. 13:
138–139.
DANIELOPOL, D. L., C. GRIEBLER, A. GUNATILAKA, H. J. HAHN, J. GIBERT, F. MERMILLOD-BLONDIN,
G. MESSANA, J. NOTENBOOM and B. SKET, 2007: Incorporation of groundwater ecology in environmental policy. – In: QUEVAUVILLER, PH. (ed.), Groundwater science and policy, Royal Soc. Chemistry,
London, pp. 671–689.
DIRECTIVE 2006/118/ECEU GWD, of the European Parliament and of the Council of 12 December
2006 – Official Journal of the European Communities L372: (19).
DOLE-OLIVIER, M.-J., P. MARMONIER, CREUZÉ des CHÂTELLIERS and D. MARTIN, 1994: Interstitial fauna
associated with the alluvial floodplains of the Rhône River (France). – In: GIBERT, J., D. L. DANIELOPOL. and J. A. STANFORD (eds.), Groundwater ecology. – Academic Press, San Diego, pp. 313–346.
DUNLAP, W. J., J. F. MCNABB, M. R. SCALF, and R. L. COSBY, 1977: Sampling for organic chemicals and
microorganisms in the subsurface. – In: U.S. Environment Protection Agency Report, pp. 77–176.
EKENDAHL, S., A. H. O’NEILL, E. THOMSSON and K. PEDERSEN, 2003: Characterization of yeasts isolated
from deep igneous rock aquifers of the Fennoscandian shield. – Microb. Ecol. 46: 416–428.
ELLIS, B. K., J. STANFORD, and J. V. WARD, 1998: Microbial assemblages and production in alluvial
aquifers of the Flathead River, Montana, USA. – J. N. Am. Benthol. Soc. 17: 382–402.
FARNLEITNER, A. H., I. WILHARTITZ, G. RYZINSKA, A. K. T. KIRSCHNER, H. STADLER and M. M. BURTSCHER, 2005: Bacterial dynamics in spring water of alpine karst aquifers indicates the presence of
stable autochthonous microbial endokarst communities. – Env. Microbiol. 7: 1248–1259.
GHIORSE, W. C., and J. T. WILSON, 1988: Microbial ecology of the terrestrial subsurface. – Adv. Appl.
Microbiol. 33: 107–172.
GIBERT, J., 1986: Ecologie d’un système karstique jurassien. Hydrogéologie, dérive animale, transit de
matières, dynamique de la population de Niphargus (Crustacé Amphipode). – Mém. Biospéol. 13:
1–379.
GIBERT, J., D. L. DANIELOPOL and J. A. STANFORD, 1994a (eds.): Groundwater ecology, Academic Press,
San Diego, 571 pp.
GIBERT, J., J. A. STANFORD, M-J. DOLE-OLIVIER and J. V. WARD, 1994b: Basic attributes of groundwater
ecosystems and prospects for research. – In: GIBERT, J., DANIELOPOL, D. L. and STANFORD, J. A. (eds.),
Groundwater ecology, Academic Press, San Diego: pp. 8–40.
GIBERT, J., 2001: Protocols for the assessment and conservation of aquatic life in the subsurface
(PASCALIS): a European project. – In: CULVER, D. C., DEHARVENG, L., GIBERT, J. and SASOWSKY,
I. D. (eds.), Mapping Subterranean Biodiversity, Proceedings, Karst Water Institute, Special Publication 6, Charles Town, WV, pp. 19–21.
GIBERT, J. and L. DEHARVENG, 2002: Subterranean ecosystems: a truncated function biodiversity. – Bioscience 52: 473–481.
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.revhydro.com
576
D. L. DANIELOPOL and C. GRIEBLER
GIBERT, J., A. BRANCELJ, A. CAMACHO, F. CASTELLARINI, C. DE BROYER, L. DEHARVENG, M.-J. DOLEOLIVIER, C. DOUADY, D. M. P. GALASSI, F. MALARD, P. MARTIN, G. MICHEL, F. STOCH, P. TRONTELJ
and A. G. VALDECASAS, 2005: Protocols for the assessment and conservation of aquatic life in the
subsurface (PASCALIS): overview and main results. – In: GIBERT, J. (ed.), Symposium on world
subterranean biodiversity, Proceedings, Univ. Claude Bernard, Lyon 1, Villeurbanne: pp. 39–52.
GIBERT, J., D. C. CULVER, D. L. DANIELOPOL, C. GRIEBLER, A. GUNATILAKA, J. NOTENBOOM and B. SKET,
2008: Groundwater ecosystems: human impacts and future management. – In: POLUNIN, N. V. C.
(ed.), Aquatic ecosystems, trends and global prospect. Cambridge University Press, Cambridge,
pp. 30–34.
GOLDSCHEIDER, N., D. HUNKELER and P. ROSSI, 2006: Review: Microbial biocenosis in pristine aquifers
and an assessment of investigation methods. – Hydrogeol. J. 14: 926–941.
GRIEBLER, C., D. L. DANIELOPOL, J. GIBERT, H. P. NACHTNEBEL, NOTENBOOM (eds.), 2001: Groundwater
ecology, a tool for management of water resources. – Office for Official Publications of the European
Publications, LuxenbourgLuxembourg: pp. 1–413.
GRIEBLER, C. and F. MÖSSLACHER (eds.), 2003: Grundwasser-Ökologie – UTB-Facultas, Vienna:
pp. 1–495.
GRIEBLER, C. and T. LUEDERS, 2008: Towards a conceptual understanding of microbial biodiversity in
groundwater ecosystems. – Freshw. Biol. online DOI: 101111/j.1365-2427.2008.02013x.
GSCHV, 1998: Gewässerschutzverordnung (Swiss Water Ordinance) 814.201. – Der Schweizer Bundesrat, 58 pp.
HAACK, S. K. and BEKINS, B. A., 2000: Microbial populations in contaminant plumes. Hydrogeol. J. 8:
63–76.
HIRSCH, P., E. RADES-ROHKOHL, J. KÖLBEL-BOELKE and A. NEHRKORN, 1992: Morphological and taxonomic diversity of ground water microorganisms. – In: MATTHESS, G., FRIMMEL, F., HIRSCH, P.,
SCHULZ, H. D., and USDOWSKI, E. (eds.), Progress in Hydrogeochemistry. Berlin-Heidelberg: Springer
Verlag, pp. 311–325.
HUMPHREYS, W., 1999: Relict stygofaunas living in sea salt, karst and calcrete habitats in arid northwestern Australia contain many ancient lineages. – In: PONDER, W. and LUNNEY, D. (eds.), Trans. Roy.
Zool. Soc. New South Wales, Mosman, pp. 219–227.
HUMPHREYS, W. F., 2006: Aquifers: the ultimate groundwater-dependent ecosystems. – Austral. J. Bot. 54:
115–132.
JOB, C. A. and J. J. SIMONS,1994: Ecological basis for management of groundwater in the United
States: Statutes, regulations, and a strategic plan. – In: GIBERT, J., DANIELOPOL, D. L. and STANFORD,
J. A. (eds.), Groundwater ecology, Academic Press, San Diego, pp. 523–540.
KUHN, T. S., 1970: The structure of scientific revolutions (2nd Edition, enlarged). – Chicago Univ. Press,
Chicago, 210 pp.
KYLE, J. E., H. S. C. EYDAL, F. G. FERRIS and K. PEDERSEN, 2008: Viruses in granitic groundwater from
69 to 450 m depth of the ASPÖ hardrock laboratory, Sweden. – ISMEJ. 2: 571–574.
LONGLEY, G., 1981: The Edwards aquifer: earth’s most diverse groundwater ecosystem? – Int. J. Speleol. 11: 105–122.
MADSEN, E. L. and W. C GHIORSE, 1993: Groundwater microbiology: subsurface ecosystem processes. –
In: FORD, T. E. (ed.), Aquatic microbiology – an ecological approach. Blackwell Scientific Publication, pp. 167–213.
MANGIN, A., 1975: Contribution à l’étude hydrodynamique des aquifères karstiques. – Annls. Spéléol.,
30: 21–124.
MARMONIER, P., P. VERVIER, J. GIBERT and M. J. DOLE-OLIVIER, 1993: Biodiversity in ground waters: a
research field in progress. – Trends Ecol. Evol. 8: 392–395.
MARMONIER, P., M. CREUZÉ DES CHÂTELLIERS, M. J. DOLE-OLIVIER, S. PLÉNET and J. GIBERT, 2000:
Rhône groundwater systems.). – In: WILKENS, H., CULVER, D. C. and HUMPHREYS, W. F. (eds.), Subterranean ecosystems, Ecosystems of the world, 30, Elsevier, Amsterdam, pp. 513–531.
MCINTOSCH, R. P., 1985: The background of ecology; concept and theory. – Cambridge Univ. Press,
Cambridge, 383 pp.
NOTENBOOM, J., 2001: Managing ecological risks of groundwater pollution. – In: GRIEBLER, C.,
DANIELOPOL, D. L., GIBERT, J., NACHTNEBEL, H. P. and NOTENBOOM (eds.), Groundwater ecology, a
tool for management of water resources. – Office for Official Publications of the European Publications, Luxenbourg, pp. 121–142.
ODUM, E. P., 1971. Fundamentals of ecology. – W.B. Saunders, Philadelphia: 574 pp.
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.revhydro.com
Changing Paradigms in Groundwater Ecology
577
PEDERSEN, K., 1997: Microbial life in deep granitic rock. – FEMS Microbiol. Rev. 20: 399–414.
POSPISIL, P., 1992: Sampling methods for groundwater animals of unconsolidated sediments. – In:
CAMACHO, A. I. (ed.),The natural history of biospeleology, Museo Nacional Ciencias Naturales, CSIC,
Madrid, pp. 107–134.
RACOVITZA, E. G., 1907: Essai sur les problèmes biospéologiques. – Biospéologica 1. Arch. Zool. Exp.
Gén. 4: 371–488.
ROUCH, R., 1977: Considerations sur l’écosystème karstique. C. R. Acad. Sc. Paris, Série D 284:
1101–1103.
ROUCH, R., 1986: Sur l’écologie des eaux souterraines dans le karst. – Stygologia 2: 352–398.
ROUCH, R. and D. L. DANIELOPOL, 1997: Species richness of microcrustacea in subterranean freshwater
habitats. Comparative analysis and approximate evaluation. – Internat. Rev. ges. Hydrobiol., 82:
121–145.
SÂRBU, S. M., 2000: Movile cave: a chemoautotrophically based groundwater ecosystem. – In: WILKENS,
H., CULVER, D. C., and HUMPHREYS, W. F. (eds), Ecosystems of the world: Subterranean Ecosystems
Elsevier, Amsterdam, 30, pp. 319–343.
SBORDONI, V., G. ALLEGRUCCI and D. CESARONI , 2000: Population genetic structure, speciation
and evolutionary rates in cave-dwelling organisms. – In: WILKENS, H., CULVER, D. C. and HUMPHREYS, W. F. (eds.), Subterranean ecosystems, Ecosystems of the world, 30, Elsevier, Amsterdam,
pp. 453–477.
SCHWOERBEL, J., 1961: Subterrane Wassermilben (Acari: Hydrachnellidae, Porohalacaridae und Stygothrombiidae), ihre Ökologie und Bedeutung für die Abgrenzung eines aquatischen Lebensraumes
zwischen Oberfläche und Grundwasser. – Arch. Hydrobiol., Suppl. 25: 242–306.
SIMON, K. S., J. GIBERT, P. PETITOT and R. LAURENT, 2001: Spatial and temporal patterns of bacterial
density and metabolic activity in a karst aquifer. – Arch. Hydrobiol. 151: 67–82.
SKET, B., 1999: High biodiversity in hypogean waters and its endangerment – The situation in Slovenia,
the Dynaric Karst and Europe. – Crustaceana 72: 767–780.
STEUBE, C., S. RICHTER and C. GRIEBLER, 2008: First attempts towards an integrative concept for
the ecological assessment of groundwater ecosystems. – Hydrogeol. J., early online, DOI: 10.1007/
s10040-008-0346-6.
THIENEMANN, A., 1950: Verbreitungsgeschichte der Süsswassertierwelt Europas. – Die Binnengewässer
18: pp. 1–809. Schweizerbart, Stuttgart.
TRONTELJ, P., C. J. DOUADY, C. FISER, J. GIBERT, S. GORICKI, T. LEFÉBURE, B. SKET and V. ZAKŠEK,
2008: A molecular test for cryptic diversity in groundwater: how large are the ranges of macrostygobionts? Freshw. Biol., DOI: 10.1111/j1365-2427.2007.01877.x.
VAN LEEUWENHOEK, A. 1677: About little animals observed in rain, well, sea, and snow water, as also in
water wherein pepper had lain infused. – Philosophical Transactions of the Royal Society of London
12: 821–831.
ZAKŠEK, V., B. SKET and P. TRONTELJ, 2007: Phylogeny of the cave shrimp Troglocaris: evidence of
a young connection between Balkans and Caucasus. – Molecular Phylogeny and Evolution 42:
223–235.
Manuscript received December 3rd, 2007; revised January 18th, 2008; accepted February 27th, 2008
© 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
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