GROUNDWATER–SURFACE-WATER INTERACTIONS

Groundwater ecosystem services: a review

Christian Griebler1,2 and Maria Avramov1,3

1Helmholtz Zentrum München, German Research Center for Environmental Health, Institute of Groundwater Ecology,Ingolstaedter Landstrasse 1, D-85764 Neuherberg, Germany

Abstract: Our daily life depends on many services delivered by the planet’s ecosystems. Groundwater ecosys-tems deliver services that are of immense societal and economic value, such as: 1) purification of water and itsstorage in good quality for decades and centuries, 2) active biodegradation of anthropogenic contaminants andinactivation and elimination of pathogens, 3) nutrient recycling, and 4) mitigation of floods and droughts. Manyof these services are directly connected to the presence and activity of specific organisms, microorganisms, ormetazoa. Sustainable protection and management of important groundwater ecosystem services will require quan-titative understanding of processes at different spatial and temporal scales and assessment of their resistance andresilience with regard to common anthropogenic impacts. Our review compiles known groundwater ecosystemservices and, where appropriate, highlights important research gaps.Key words: ecosystem services, ground water, biodegradation, pathogens, bioindicators, biodiversity

Ecosystem services are the benefits that people obtainfrom ecosystems for free and are used by humankind toguarantee and increase well-being (Daily 1997, MA 2005).The term ecosystem services emerged in the early 1980s(e.g., Ehrlich and Mooney 1983), but currently >2400 pa-pers related to this topic are listed by the Institute for Sci-entific Information (ISI) Web of Science (Thomson Reu-ters, New York), and they have been cited >30,000 times(Costanza and Kubiszewski 2012). Moreover, both num-bers are increasing exponentially.

The ecosystem-services framework relates ecosystemfunctions and environmental health to human health, se-curity, and the material goods necessary for well-being(Brauman et al. 2007). As a result, ecosystem services isnow an inter- and transdisciplinary field of research(Costanza and Kubiszewski 2012). During the last 3 de-cades, the framework has been evolving from purely con-ceptual toward solution-oriented and ready to supportdecision-making. Its broad acceptance by economists andpoliticians is related to the awareness that individual ser-vices have an enormous monetary value. A recent meta-analysis of 10 important biomes by de Groot et al. (2012)revealed that each year, the ecosystem services poten-tially provided by an average hectare of coral reefs can beworth up to 350,000 int$. (The international dollar [int$],a widely used currency in economics, is a hypothetical unitof currency that has the same purchasing power parity asthe US dollar had in the USA at a given, fixed point intime.) Rivers and lakes ranked at ∼4000 and inland wet-lands at ∼25,000 int$ ha–1y–1. Such large-scale estimates

of ecosystem service monetary value are not yet availablefor groundwater ecosystems, and these ecosystems did notfind consideration in the study by de Groot et al. (2012).Given that ground water is one of the most essential re-sources for the maintenance of human life, this assessmentgap calls for attention. Ground water is a major source ofdrinking water worldwide, serves as a solvent and coolingagent for industrial use, and provides water for irriga-tion in agriculture. On a global scale, 20% of the irriga-tion water and 40% of the water used in industry arederived from ground water (MA 2005). Growing indus-trialization, waste deposition, and the exponentially in-creasing production and use of synthetic chemicals, whichare often released into the environment, put groundwaterresources under growing pressure. Today, groundwaterquality is poor in many areas of the world (Danielopolet al. 2003). Moreover, groundwater resources are facingquantitative problems. Abstraction of ground water frommany large aquifers worldwide significantly exceeds thenatural renewal rate, as recently estimated by the ground-water footprint approach (Gleeson et al. 2012). This deficitposes a threat to the health of aquifers and their organismsand to many other groundwater-dependent ecosystems(GDEs), such as rivers and wetlands. During the recentpast, the perception of ground water by stakeholders andauthorities has been changing slowly from an exclusivefocus on economic aspects to one that includes socialand ecological aspects (Quevauviller 2005). Moreover, con-sensus exists that subsurface ecosystems deliver both im-portant water resources and additional ecosystem ser-

E-mail addresses: 2christian.griebler@helmholtz-muenchen.de; 3maria.avramov@helmholtz-muenchen.de

DOI: 10.1086/679903. Received 15 November 2013; Accepted 8 April 2014; Published online 24 December 2014.Freshwater Science. 2015. 34(1):355–367. © 2015 by The Society for Freshwater Science. 355

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vices and goods that are essential to humankind andGDEs (Danielopol et al. 2004, EU-GWD 2006). These ser-vices and goods range from provision of a natural bio-reactor for the clean-up of water until it reaches drinking-water quality to maintenance of hydraulic conductivity,drought attenuation and flood mitigation, and recreationaland cultural services provided by hot springs (see Fig. 1and specific sections below).

Within the Millennium Ecosystem Assessment classi-fication scheme (MA 2005), groundwater ecosystem ser-vices and goods partition into all 4 categories: 1) supportingservices, 2) provisioning services, 3) regulating services,and 4) cultural services. The most frequently discussed ser-vices and goods related to these categories are shown inFig. 2, with a special focus on those affiliated to ground-water ecosystems. For example, the presence of groundwater itself is a supporting service because most terres-trial and surface aquatic ecosystems depend on its avail-ability in good quality and sufficient quantity. Groundwater is an important global source for drinking waterand, thus, is a provisioning service. Regulating services in-clude purification of water and, particularly, in situ bio-degradation of contaminants and elimination of pathogenicmicroorganisms and viruses, which in turn, contributes todisease control. Last, cultural services include large waterbodies in caves that constitute tourist attractions and hotsprings that are used for recreation. In many places, groundwater feeds springs that are of high spiritual importance,such as the sacred spring in the Grotto of Massabielle inLourdes, France; the Chalice Well at Glastonbury, UK; sa-cred hot springs in Hierapolis, Turkey; the Ban Ban Springs,

an Aboriginal Cultural Heritage site in Queensland; andsimilar sites in Australia (e.g., McDonald et al. 2005).

The framework of ecosystem services is a powerful toolto raise awareness in human society of the various benefitswe receive and use from ecosystems each day—an im-portant prerequisite for their appreciation. However, theconsequent next step of this awareness, i.e., appropriateprotection and sustainable management of ecosystems, in-cluding their organismic repertoire and diverse set of func-tions, awaits efficient implementation. Moreover, the am-bitious goal of routine implementation of the ecosystemservices concept in water-regulation practice is not yetachieved (Carpenter et al. 2007). This situation also ap-plies to groundwater ecosystem management and exploi-tation, particularly because the concept has become partof the scientific interests in this field only in the last fewyears, and its wide-spread use in current studies is juststarting to develop. The objectives of our article are to re-view the various recognized services and goods providedby groundwater ecosystems and to identify specific, currentknowledge gaps.

GROUND WATER—AN OPEN SYSTEM WITHINTHE HYDROLOGICAL CYCLE

Groundwater systems are an important compartmentof the hydrological cycle. About 30% of all freshwater isterrestrial ground water, whereas the world’s lotic (streamsand rivers) and lentic (lakes) systems contribute only 0.3%(Danielopol et al. 2003). With respect to the available (liq-uid) fresh water, terrestrial ground water contributes 94%.Hydrological recharge of aquifers is geographically very var-

Figure 1. Groundwater ecosystem services. GDEs = groundwater dependent ecosystems.

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iable and strongly dependent on climate, geology, soil type,vegetation, and land use, among other factors (Scanlonet al. 2002). Groundwater recharge via precipitation is com-plemented by naturally infiltrating surface water or by arti-ficial recharge. In the opposite direction, ground waterleaves the subsurface via springs and wetlands (sustaininggroundwater-dependent ecosystems = supporting service,drought attenuation = regulating service), enters surfacewaters (provision of water and nutrient cycling = support-ing services), or is being exploited for different types ofusage, the latter directly contributing to the category of pro-visioning ecosystem services and goods. Moreover, indi-vidual functions may serve different service categories anddifferent ecosystems at the same time.

A key feature of groundwater ecosystems is that theyare open systems that are closely connected to other ter-restrial and aquatic ecosystems, many of which depend onground water in high quality and quantity—the so-calledgroundwater-dependent ecosystems (GDEs; Boulton 2005,Humphreys 2006, Murray et al. 2006). The boundaries andtransition zones (ecotones) of aquifers are particularly im-portant (Gibert et al. 1990) because they play a significantrole in regulating the flux of matter and energy acrosssystems. Ecotones are characterized by steep physicochem-ical and biological gradients, high activities, and high bio-logical diversity (Naiman and Décamps 1997, Ward and

Wiens 2001). From the perspective of ecosystem health,transition zones are significant biobarriers and filters forexternal impacts. Important ecotones are the hyporheiczone of streams and rivers (Gibert et al. 1990, Brunke andGonser 1997, Boulton et al. 2010), the transition betweenthe unsaturated and saturated zone (capillary fringe andgroundwater table) (Madsen and Ghiorse 1993, Lahviset al. 1999), and transitions between geological strata (e.g.,unconsolidated sediments and rock, highly conductive sandlayers and clay lenses; McMahon et al. 1992, Ulrich et al.1998, Krumholz 2000).

When snowmelt and heavy precipitation cause floods,aquifers and wetlands act as sponges that receive and re-tard significant amounts of surface water (Postel and Car-penter 1997). Water also is purified (see water clean-upbelow) and is later available for irrigation purposes (provi-sioning service). Conversely, base flow or dry-weather flowin rivers and streams may be fed exclusively by groundwater entering the stream channel (Allan 1995). Withoutthis quantitatively significant contribution, many rivers andstreams would be intermittent or ephemeral (supportingand regulating services). Last, the open corridor betweensurface waters and aquifers enables individual surface spe-cies to find temporary refuge in times of harsh conditions(e.g., floods and droughts, temperature elevations causedby anthropogenic impacts and climate warming; Hose et al.2005, DiStefano et al. 2009).

NATURAL PRODUCTION AND STORAGEOF DRINKING WATER

In Europe, 75% of the drinking water is produced fromground water, and on a global scale, ⅓ of the populationuses ground water as their main source of drinking water(Sampat 2000), a provisioning service that frequently istaken for granted. Covered by active soil and sediment lay-ers, ground water is often much better protected than sur-face water from the negative impacts of human activities. Insome areas, a substantial portion of the drinking water isproduced from bank filtration of surface waters that carrya diverse load of chemicals and pathogens (Tufenkji et al.2002), thus making use of the regulating service of waterpurification.

Water from the tap, when stagnant in in-house distribu-tion pipes or kept open to the atmosphere at room temper-ature, changes in quality within hours or days (Lauten-schlager et al. 2010). In contrast, a healthy aquifer, like anactive biofilter, keeps and further improves water qualityand provides safe water storage for centuries. Drinking-water production uses this service and benefits directlyfrom the integrity of groundwater ecosystems (Tufenkji et al.2002). Moreover, sustainable management of the catch-ment area can be translated directly into economic values.For example, the 4 European cities Berlin, Munich (both

Figure 2. Selected examples of ecosystem services and goodssorted into the 4 categories of services as defined in the Mil-lennium Ecosystem Assessment report (MA 2005). The goodsand services that are directly related to groundwater ecosystemsare highlighted in bold print. GW = groundwater, GDEs =groundwater dependent ecosystems.

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Germany), Vienna (Austria), and Oslo (Norway), each sup-ply their citizens (500,000–3.5 million people) with drink-ing water derived from ground water. The ground wa-ter originates from areas with sustainable management inwhich protective measures range from strict protection(Vienna) to partial conversion of areas from conventionalto organic agriculture (Munich). The drinking water in Vi-enna and Munich is untreated ground water. In Oslo andBerlin, where ground water needs to be treated, the waterworks benefit from the very low contamination levels re-sulting from catchment protection. The annual economicbenefit of natural water purification and provision rangesfrom 17 to 108 million €, which translates into an averagereduction in the water bill by 45 € per capita or 200 € perhousehold and year (ten Brink et al. 2011).

SINK AND SOURCE OF C AND NUTRIENTSAquifers are open systems, so they may be a sink and

source for C and nutrients. Water infiltrating into the sub-surface is continuously depleted in C during the passagethrough soil and sediment (Tufenkji et al. 2002), and as aresult, ground water is typically poor in dissolved organic C(DOC). Nevertheless, in sum, aquifers are fueled continu-ously by considerable amounts of organic C. In pristineaquifers, mineralization of organic C, in terms of respira-tion (O2 consumption) and biomass production (growthrates), is extremely low and at the lower range of sensitiv-ity of the methods routinely used in freshwater microbiol-ogy (Kieft and Phelps 1997). However, facilitated by thehuge volume of aquifers and the comparably long resi-dence times of organic matter in the subsurface, groundwa-ter ecosystems contribute significantly to the turnover of Cand, hence, to the purification of water. At present, whichorganismic guilds are primarily responsible for the C turn-over in aquifers is poorly understood. Nevertheless, evi-dence is increasing that stable, attached microbial commu-nities play a much greater role than dynamic, low-activitysuspended communities (Alfreider et al. 1997, Griebleret al. 2002, Wilhartitz et al. 2009, Flynn et al. 2013). Fur-thermore, seasonal hydrological dynamics are sometimesstrong and may control bacterial activity (heterotrophicproduction), diversity (Zhou et al. 2012), and the distribu-tion of microorganisms between the sediment and waterphases (Griebler et al. 2002) in pristine groundwater eco-systems.

Subsurface metazoa also are involved in groundwaterC cycling. However, their quantitative role is unclear.Only a few investigators have examined the indirect par-ticipation of groundwater invertebrates in natural attenu-ation through grazing on microbial biofilms (see naturalattenuation below). Stimulation of C turnover via grazingby meio- and macrofauna on microorganisms, ingestionof microbially colonized sand, and bioturbation has been

demonstrated repeatedly in surface aquatic systems andin sediment-column experiments (Mermillod-Blondin 2011,Griebler et al. 2014a).

Groundwater exfiltrating into surface waters and atsprings generally is supersaturated with CO2 because ofmetabolic processes in the subsurface waters. However, insome cases, groundwater ecosystems can act as a source ofC. Little attention has been paid to the concept of CO2

fixation and chemolithoautotrophic primary production inground water. CO2 fixation (linked to photosynthesis) isone of the most important processes on the Earth’s sur-face (Berg 2011), but our current understanding of its oc-currence and importance in groundwater ecosystems (i.e.,without the participation of light) is poor (Kinkle and Kane2000). Recently, a huge diversity and distribution of auto-trophic bacteria and functional genes involved in CO2

fixation have been reported from pristine and contami-nated aquifers (Alfreider et al. 2003, 2009, Kellermannet al. 2012). Microbial CO2-fixation potential may be of in-terest with respect to C sequestration and climate change,a putative regulating service.

Depending on the redox conditions and the availabilityof organic C, nutrients (such as N and P) may be effec-tively converted, retarded, or immobilized in ground water(e.g., Billen et al. 1991, Lewandowski and Nützmann 2010,Bouwman et al. 2013). This regulating service is used inartificial groundwater-recharge (Schmidt et al. 2012) orstormwater wetlands and infiltration ponds (Datry et al.2004, Moore and Hunt 2012). However, ground watersometimes can be little more than a transport medium fornutrients, e.g., NO2

–, which is diluted but not transformedin oxic conditions and in the absence of organic matter.Ground water also can act as a source of P and Si for thesurface. Surface vegetation in contact with ground watermay directly benefit from the provision of nutrients, butan excessive supply to surface waters and wetlands cancause undesirable eutrophication with massive develop-ment of primary producers, e.g., in the form of algal blooms(Freeze and Cherry 1979, Hurley et al. 1985).

NATURAL ATTENUATION OF CONTAMINANTSAND PATHOGEN ELIMINATION

Groundwater ecosystems provide biologically mediatedtransformation and degradation of contaminants (Tufenkjiet al. 2002). To date, >75 million chemicals are registered(CAS Registry 2013), and several hundred thousands ofthese are traded daily on the world market. Accordingly,ground water is severely contaminated at millions of sites(EEA 2007). The list of priority contaminants includes chlo-rinated solvents, petroleum hydrocarbons, heavy metals,pesticides, and is complemented by chemicals of emerg-ing concern, such as human and veterinary pharmaceu-ticals, personal care products, and food ingredients (e.g.,

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artificial sweeteners) (Richardson and Ternes 2011). For-tunately, groundwater ecosystems have immense potentialto naturally attenuate and aerobically, anaerobically, andsyntrophically degrade a huge diversity of pollutants re-leased into the underground (Díaz et al. 2013, Jeon andMadsen 2013, Gieg et al. 2014). Furthermore, microbes candevelop new metabolic pathways and, thus, the potentialto degrade emerging contaminants (van der Meer 2006,Kolvenbach et al. 2014). In many cases, natural attenuationprocesses in the subsurface are sufficient to prevent con-tinuous distribution of contaminants over large areas (animportant regulating service). Therefore, a steadily growingnumber of contaminated sites are being managed via moni-tored and enhanced natural attenuation, a direct economicuse of this ecosystem service (Herman et al. 2001).

Pathogenic microorganisms and viruses compose an-other important class of contaminants. Pathogens regu-larly enter soils and aquifers via infiltration of surfacewaters that have received waste water or via seepage ofprecipitation water from areas where manure has been ap-plied (e.g. Tufenkji et al. 2002, Lucena et al. 2006, Kraussand Griebler 2011, Sinreich et al. 2011). As is the casewith organic contaminants, the subsurface systems beara great potential for effective retardation, inactivation,and elimination of pathogens. Global change is likely toincrease the pressure on terrestrial and aquatic environ-ments, and therefore, water carrying pathogenic viruses(e.g., from sewage treatment discharge) probably will bespread into regions used for drinking-water productionmore often, e.g., by an increasing frequency of large floods(Alley 2001, Green et al. 2011). Therefore, the ecosystemservice of pathogen elimination can be expected to gainimportance in the future. However, our understanding ofthe mechanisms behind natural pathogen control and ofits limits is still incomplete. Recurring epidemics caused bycontaminated surface, ground, and drinking water (Kraussand Griebler 2011) underline the importance of shed-ding light on the ecology and fate of pathogens in aquaticecosystems.

Efficient decay of pathogenic viruses takes place in theform of physical, chemical, and biological retardation andthrough inactivation and destruction. Environmental fac-tors, such as sorption, irradiation (not relevant for ground-water systems), temperature, and ionic strength are cur-rently regarded as the main factors affecting the survivaland migration of pathogens in water (Krauss and Griebler2011). Groundwater microorganisms also can contribute topathogen elimination. Hirsch and Rades-Rohkohl (1983)showed that >20% of 217 pure bacterial strains isolatedfrom ground water inhibited the growth of Escherichia colistrain K 12. Individual pathogenic bacteria, i.e., E. coli andVibrio cholerae, which can proliferate in natural waters inthe presence of sufficient DOC, did not grow well or weresuppressed in the presence of ambient microbial communi-

ties (Vital et al. 2007, 2008). Bacteria can inactivate anddestroy viruses via exoenzymes (proteases, nucleases) andmake use of them as growth substrates after lysis (Cliverand Herrmann 1972, Gerba 1983, Lipson and Stotzky 1985,Nasser et al. 2002). Strong evidence exists that grazing bynanoflagellates may contribute to viral decay (Manage et al.2002, Bettarel et al. 2005, Deng et al. 2013).

Studies of the potential role of groundwater metazoa incontaminant and pathogen removal are limited. Sinton(1984) demonstrated an essential contribution of inverte-brates in C turnover in a sewage-polluted aquifer. The pres-ence of E. coli and coliform bacteria in the guts of isopodsprovided strong evidence that the isopods had consumedorganic material that originated directly or indirectly fromthe sewage discharge and that the isopods had eliminated aconsiderable number of pathogens via their feeding activ-ity. Based on the invertebrate standing crop, Sinton (1984)suggested that isopods assimilated 20% of the discharged C(given as calorific equivalents), and based on invertebratedensity, total ingestion by invertebrates was estimated as100 to 200 tonnes of C/y for the contaminated aquifer. ThisC was converted to animal biomass and CO2 (Fenwick1998). Thus, in some cases, groundwater invertebrates mayplay an important role in removing organic contaminantsfrom aquifers. Unfortunately, similar data sets from othersites are missing. In contrast, a high organic load to thesubsurface is typically accompanied by a fast depletion ofO2 and a switch to anoxic conditions, which would preventactive contribution and survival of invertebrates (Malardand Hervant 1999).

MAINTENANCE OF HYDRAULIC CONDUCTIVITYIN AQUIFERS

Another ecosystem service attributed to groundwatermetazoa, especially invertebrates, is maintenance of hydrau-lic conductivity in porous sediments through their feedingon microbial biofilms and bioturbation (Eder 1982, Daniel-opol 1989, Nogaro et al. 2006, Song et al. 2007, Mermillod-Blondin 2011). In the authors’ personal opinion, this ser-vice is restricted to energetically favorable and denselycolonized areas, such as the hyporheic zone of streams andrivers, shores of lakes, and bottom sediments in artificialgroundwater-recharge ponds.Here, the influx of organicmat-ter in dissolved and particulate form sustains the formation ofpronounced biofilms and large populations of invertebrates.Burrowing fauna positively affect sediment permeability insediment-column experiments (Eder 1982, Nogaro et al.2006) and in gravel and sand filters used in artificial ground-water recharge (Rumm 1993, see also Mermillod-Blondin2011). Even low invertebrate densities may significantly en-hance the permeability of fine sand by creating burrows thatconstitute preferential flow paths (C. Stumpp [HelmholtzZentrum München] and G. C. Hose [Macquarie Univer-sity], personal communication). Ward et al. (1998) used the

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term ecosystem engineers (Jones et al. 1994) when describ-ing the ecological function of invertebrates in aquifers. How-ever, given the generally low densities of invertebrates inmost pristine groundwater systems, this role awaits furtherevaluation.

Boulton et al. (2008) carried out an initial study inwhich they emphasized the ecological role of groundwaterfauna at well characterized alluvial aquifers in Australiaand New Zealand. They categorized important ecosystemservice providers (ESPs) among the invertebrates found inriverbed sediments and alluvial aquifers and proposed aconceptual model of the contribution of individual groupsof invertebrates to 2 ecosystem services (biogeochemicalfiltration and particulate organic matter [POM] break-down). In this conceptual model, Boulton et al. (2008) as-signed a significant role in C turnover to stygobitic inverte-brates, particularly amphipods and isopods. However, theyalso pointed out several gaps in understanding of the func-tional importance of most stygofauna and highlighted theneed for further research in this area.

BIOINDICATION AND BIOMONITORINGGroundwater organisms live in an energy-limited habi-

tat with comparably predictable environmental conditions.Thus, they may be very sensitive to anthropogenic impactsand environmental changes. This sensitivity would makethem potential candidates as bioindicators that could pro-vide decision makers and groundwater managers with use-ful information on ecosystem status (Griebler et al. 2010),an important cultural ecosystem service (Fig. 2). The signif-icant economic and environmental value of aquifers andground water makes detailed understanding and monitor-ing of the behavior and status of these ecosystems crucial.However, to date, ground water and aquifers have beenperceived mainly from a resource-oriented, economic per-spective (Danielopol et al. 2004). In Europe, this attitudestarted to change with the December 2006 release of theEuropean Groundwater Directive (EU-GWD), which man-dates at a political level that ground water is more than justa resource and aquifers are more than just drinking-waterreservoirs, and that both are also unique habitats. Ecologi-cal assessment of ecosystem status is done routinely forsurface waters. Metazoa (invertebrates and fishes), macro-phytes, phytoplankton, and diatoms are used frequentlyas bioindicators. Groundwater ecosystems lack algae andhigher plants, but native invertebrate communities harborsensitive sentinels available for an ecologically oriented as-sessment (Notenboom et al. 1995, Malard et al. 1996,Mösslacher 1998, 2000, Dumas et al. 2001, Hahn 2006,Schmidt et al. 2007, Bork et al. 2009, Brielmann et al. 2009,Stein et al. 2010) and biomonitoring (Moesslacher et al.2001, Marmonier et al. 2013). However, invertebrate densi-ties are low and many ground waters are naturally anoxic,so ubiquitous microorganisms and microbially related vari-

ables, such as total cell number, ATP concentration, andspecific activities, may be promising bioindicators and eco-logical criteria (Claret 1998, Feris et al. 2009, Pronk et al.2009, Griebler et al. 2010, Stein et al. 2010). Several at-tempts are in progress to develop an assessment schemefor groundwater systems comparable to the ones routinelyused for surface-water ecosystems (Steube et al. 2009, Kor-bel and Hose 2011, Griebler et al. 2014b).

BIODIVERSITYGround water and aquifers are habitats for diverse mi-

crobial communities (Ghiorse and Wilson 1988, Hirschet al. 1992, Madsen and Ghiorse 1993, Novarino et al. 1997,Goldscheider et al. 2006, Griebler and Lueders 2009) andmetazoan fauna (Marmonier et al. 1993, Danielopol andPospisil 2000, Culver and Pipan 2009, Deharveng et al.2009). The diversity and activity of groundwater organismsis linked directly to the provision of individual ecosystemservices. Therefore, groundwater quality depends on bio-logical activity and ecosystem health. Moreover, the uniqueorganisms found only in ground water (see below) havehigh existence and bequest value. Bequest value, in eco-nomics, is defined as ‘the willingness to pay for the satis-faction derived from endowing future generations with anatural environment’ (Greenley et al. 1981), i.e., the valuepeople may place on knowing that a resource exists even ifthey never use it directly and the value derived from pre-serving the option to use a service in future (that may notbe used at present) by others or by future generations (MA2005).

Groundwater metazoa (stygofauna) have been investi-gated for >100 y. Groundwater ecosystems harbor a vastdiversity of living fossils and endemic species (Marmonieret al. 1993, Danielopol and Pospisil 2000, Ferreira et al.2007, Humphreys 2008, Gibert and Culver 2009, Malardet al. 2009). Moreover, as indicated by the cumulative rich-ness curves of stygobitic species that have been reported invarious studies (e.g. Deharveng et al. 2009), a major part ofgroundwater metazoan diversity still awaits discovery.

In contrast, groundwater microbiology and microbialecology have much shorter histories. These disciplines havetheir early roots in the middle of the 20th century. Thisresearch was triggered by industrial activities and hygienicaspects of the extraction of oil and water (e.g., Leenheeret al. 1976, Godsy and Ehrlich 1978). From today’s stand-point, it is not surprising that diverse microbial communi-ties were found. Recent studies show that microbes arepresent even hundreds and thousands of meters below ourfeet (Ghiorse 1997, Griebler and Lueders 2009).

With respect to ecosystem services, biological diversitycan be seen from 2 perspectives. First, it stands for a cer-tain repertoire of functions (provisioning service). Second,it represents the richness of species (supporting service),some of which may be rare and in need of protection (cul-

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tural service). Processes in individual habitats or ecosystemsare a direct result of the functional-trait diversity withinbiotic communities (Griebler and Lueders 2009). There-fore, changes in diversity may lead to changes in ecosystemprocesses (Humbert and Dorigo 2005). Moreover, highbiodiversity (although not in every case) is linked to func-tional stability and flexibility of ecosystems or habitats and,hence, stands for functional resilience (e.g., Girvan et al.2005, Eisenhauer et al. 2012; reviewed by Loreau 2000,McCann 2000, Schwartz et al. 2000, Cottingham et al.2001). The occurrence of microbes with a similar func-tional repertoire but slightly different niches (with respectto temperature or other biophysical and chemical condi-tions, substrate affinity, uptake and storage of nutrients, Cdegradation kinetics, growth rates) secures system func-tioning in the face of environmental dynamics and distur-bances (e.g., the “insurance hypothesis”; Botton et al. 2006).Microbial species in aquifers may display functional redun-dancies, but like in other environments, each species alsomay possess very specialized catalytic abilities. One promi-nent example for the direct benefit of microbial diversityin aquifers is the enormous intrinsic potential for degrada-tion of a variety of contaminants (Aamand et al. 1989,Haack and Bekins 2000, Röling and van Verseveld 2002,Griebler and Lueders 2009). Moreover, the subsurface mayhave in store an almost untapped reservoir of processesand biological compounds (e.g., enzymes, antibiotics) use-ful for novel biochemical and biotechnological applications(Pedersen 2000, Griebler et al. 2014a).

GEOTHERMAL ENERGY USAGESubsurface heat and cold are increasingly important as

sources of sustainable energy that has a comparably lowimpact in terms of CO2 emissions (Lund et al. 2011). Geo-thermal energy is abiotic and arises from the geophysicalproperties of the planet rather than as a result of biologicalactivity. Therefore, this service should be considered morea system service than an ecosystem service per se. Never-theless, the provision of geothermal energy is mentionedhere because it depends on the availability of ground waterand, as such, on the provisioning service of groundwaterecosystems. Furthermore, use of geothermal energy can di-rectly affect groundwater biodiversity and other ecosystemservices.

Depending on the depth below surface, the use of geo-thermal energy differs. Deep subsurface installations aimexclusively at extraction of heat, which is then convertedto electricity in geothermal power plants or is used directlyfor heating purposes. In contrast, geothermal energy usefrom the shallow subsurface (<400 m depth) encompasses3 strategies: 1) open-loop systems, 2) closed-loop systems,and 3) aquifer storage systems (Malin and Wilson 2000).Closed-loop systems influence aquifer ecosystems by sea-sonally decreasing and increasing average groundwater

temperatures by only a few °K (Rybach and Sanner 2000,Sanner et al. 2003), but open-loop systems may produceextensive heat plumes several hundred meters in length,thus resulting in absolute increases in temperature ≥20°C(Brielmann et al. 2009). Furthermore, aquifer heat-storagesystems may even exhibit temperatures of 30–90°C (San-ner 2004). These temperature alterations act on an ecosys-tem that would be (below a depth of 10–20 m) unaffectedby seasonal temperature fluctuations under natural condi-tions and would maintain constant temperature conditions(Matthess 1994), e.g., between 8 and 14°C in Central Eu-rope. Thus, apart from the clear benefits of using geother-mal energy sources, altering the local thermal regime ofaquifers and introducing seasonal temperature fluctuationscould affect aquifer biogeochemical processes and conse-quently, water quality (Bonte et al. 2011, 2013a, b). Tem-perature is a key regulator of (micro-) biological activitiesand often is more important than other limiting factors,such as the availability of substrates or nutrients (Peterset al. 1987). Changes in temperature cause changes in aqui-fer hydro- and geochemistry and, thus, influence the ther-modynamics of biogeochemical processes (Bonte et al.2013a). Thus, increasing use of the subsurface as storagecapacity for heat and cold is a putative danger because it isnot clear how groundwater ecosystems are affected struc-turally and biologically by regularly induced temperaturechanges (Guimarães et al. 2010, Brielmann et al. 2011).

MINERAL WATER AND HOT SPRINGSDeep subsurface ground water delivers mineral water to

human society which is then either bottled for daily con-sumption, applied in medical therapy, or enjoyed in naturalhot springs and centers for recreation (spas). The idea thatwater has magical properties to heal and confer vitality hasdeep historical roots in sacred springs and wells that wereseen as sources of spiritual knowledge and wisdom (Strang2004). Research of this mainly cultural service is found inthe social and economic science disciplines and is not fur-ther discussed here.

DISCUSSION AND CONCLUSIONSGroundwater ecology has become a modern subdisci-

pline of ecology and limnology, and has undergone severalparadigm changes from the ‘living fossils’ tradition to amore holistic ecosystem research field that includes manysocioeconomic aspects and that is slowly catching up withgeneral aquatic and terrestrial ecology (Danielopol andGriebler 2008). However, compared to other disciplines,hypothesis-driven research is obviously lacking. Such re-search is needed to provide mechanistic explanations thatmay allow the predictions that are necessary for the protec-tion and sustainable management of ecosystem integrityand services (Larned 2012, Griebler et al. 2014a). Much ofthe scientific work on groundwater systems in the past has

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been purely descriptive. The concept of ecosystem servicessupports the recent trend to move beyond describing ob-served structures, e.g., community composition of commu-nities, to focus on the functions and individual processesthat are connected to them. Unraveling the ecological prin-ciples will allow prediction of ecosystem functions and ser-vices in the face of short- and long-term disturbances, suchas contaminant spills and global change, respectively. Suchpredictive tools are urgently needed by practitioners andpolicy makers to develop appropriate instruments for riskassessment and resource protection (Griebler et al. 2014a).

As a prerequisite, ecologists must conduct inter- andtransdisciplinary work while studying groundwater ecosys-tems to fill still-open research gaps. Detailed information islacking for important groundwater ecosystem properties,such as structural heterogeneity; ecosystem size, borders,and connectivity to neighboring systems; inflow and out-flow of matter; and the spatial and temporal distribution ofsubstrates (organic C and nutrients) (Larned 2012). Properevaluation of these patterns will improve our qualitativeand quantitative understanding of groundwater ecosystemservices. However, filling these gaps will require the inti-mate involvement of expertise in the fields of geohydrology,geophysics, and geochemistry.

A currently almost untouched topic is groundwater–foodweb interactions, especially between micro- and mac-roorganisms, and their links to processes (C and nutrientcycling) and services (attenuation of contaminants; re-viewed by Marmonier et al. 2012 for the hyporheic zone).Even in low numbers, invertebrates may significantly in-fluence sediment permeability via burrowing activity and,thereby, affect the transport and distribution of matter,which is later transformed by microbes. Stygofauna maybe a vector for the distribution of key microbes and func-tions. Within the microbial food web, the roles of grazersand viruses in shaping of communities and underlyingprocesses, such as the turnover of C, still await evaluation.The general prediction that ongoing loss of biodiversityfeeds back on ecosystem responses (Hooper et al. 2012) islikely to apply to groundwater ecosystems. Thus, futureresearchers will have to address interdependencies amongincreasing pressures (e.g., pollution, overexploitation, useof ground water for heating) and the loss of biodiversity,ecosystem reactions, and potential loss of ecosystem ser-vices. Without doubt, the ecosystem services scheme is auseful tool for raising awareness of the importance ofgroundwater ecosystems. Monetary values of ecosystem ser-vices, where these can be assessed in a meaningful way, canprovide convincing arguments in public discourse, politics,and legislation.

ACKNOWLEDGEMENTSThe authors thank Colette Whitfield for language editing,

Guest Editor Kathleen Rugel, and 2 anonymous referees for theirvaluable comments and suggestions, as well as editor Pamela Sil-

ver for the final editing of the manuscript. Colleagues in the fieldof groundwater ecology are acknowledged for ongoing criticaland fruitful discussions. Financial support to Maria Avramov wasgranted by the German Federal Environmental Foundation interms of a PhD scholarship and is also highly appreciated (DBU,grant 20009/005, 2009–2012).

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