Crenic habitats, hotspots for freshwater biodiversity

Freshwater Science, 2012, 31(2):463–480 ’ 2012 by The Society for Freshwater Science DOI: 10.1899/11-111.1 Published online: 17 April 2012

Crenic habitats, hotspots for freshwater biodiversity conservation: toward an understanding of their ecology Marco Cantonati1,6, Leopold Fu¨reder2,7, Reinhard Gerecke3,8, Ingrid Ju¨ttner4,9, AND Eileen J. Cox5,10 1

Museo delle Scienze, Limnology and Phycology Section, Via Calepina 14, I-38122 Trento, Italy University of Innsbruck, River Ecology and Invertebrate Biology, Institute of Ecology, Austria 3 Department of Comparative Zoology, Institute of Ecology and Evolution, University of Tu¨bingen, Tu¨bingen, Germany 4 National Museum Wales, Department of Biodiversity and Systematic Biology, UK 5 The Natural History Museum, London, UK 2

Abstract. Springs are unique aquatic habitats that contribute significantly to local and regional biodiversity because of their high habitat complexity and the large number of different spring types. Many springs are small, but they are numerous and often of high water quality, and thus, provide habitats for species that are rare elsewhere because of their sensitivity to anthropogenic impacts (least-impaired habitat relicts). Springs are often species-rich and contain a larger number of Red List taxa than other aquatic habitats. Hydrological factors, particularly flow permanence, water chemistry, and temperature are important ecological factors determining species distribution and community composition. Despite their importance for biodiversity and water quality, springs are much less studied than other aquatic ecosystems. They also are insufficiently covered by protective legislation, often resulting in the destruction of their natural habitat. The authors of papers in this special issue describe specific spring biota, including multitaxon studies, and discuss the role of environmental factors, habitat variability at different spatial and temporal scales, and the importance of natural and anthropogenic disturbance in spring habitats. They suggest directions for future research, including defining reference conditions for springs and their role in long-term ecological research, the development of quality-assessment methods, and their more sustainable use as freshwater resources. Key words: springs, freshwater biodiversity, ecology, conservation, species richness, Red List species, flow permanence and variability, least-impaired habitat relicts.

Almost 50 y ago, Illies and Botosaneanu (1963) recognized the unusual characteristics of springs and proposed crenobiology as a special field of limnology. However, springs remained largely underinvestigated for a long time (Table 1). Early studies focused mainly on single groups of typically crenic animals, such as hydrobiid snails (Pezzoli 1969) or water mites (Schwoerbel 1959). From the early 1990s, more comprehensive studies involving several groups of organisms were done in the European Alps (Crema et al. 1996, Cantonati 1998), particularly within the

CRENODAT project (Biodiversity assessment and integrity evaluation of springs of Trentino) in the southeastern Alps (Cantonati et al. 2010a, 2011a). The papers in this special issue include studies on springs in the European Alps, northern and central Germany, Czech Republic, Finland, Spain, New Zealand, and the USA. These papers address a variety of themes, including general patterns of species and community distribution and the role of environmental factors (Glazier 2012, Kubı´kova´ et al. 2012, Lencioni et al. 2012, Rott et al. 2012), the potential of spring biota for use as monitors of long-term environmental change (Kapfer et al. 2012), definition of spring types for benchmarking (Cantonati et al. 2012a, b, Martin and Brunke 2012, Spitale et al. 2012a), downstream longitudinal changes (Guasch et al. 2012, Spitale et al. 2012b), the role of disturbance (Death and

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E-mail addresses: [email protected] [email protected] 8 [email protected] 9 [email protected] 10 [email protected] 7

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TABLE 1. Number of papers published in the Journal of the North American Benthological Society (J-NABS) (column 4) and in ‘‘all freshwater journals’’ (column 5), concerning spring habitats with indication of the main topics. Based on the Institute for Scientific Information (ISI) Web of Knowledge (accessed 30 September 2011): publication period = all years; databases = SCI-EXPANDED, SSCI, A&HCI, CPCI-S, CPCI-SSH; Lemmatization = on. As in 3. AND Topic (= freshwater)

1. Topic

2. J-NABS

3. Topic (=…)

As in 3. AND J-NABS

Spring(s)

98 (Oldest 1989)

Invertebrate Water mite Hydrobiid Chironomid Diversity Endemism Algae Diatom Bryophyte Vertebrate Ecology Conservation Topic (=…) AND Title (=springs) Diversity Benthic Invertebrate Algae Bryophyte

34 0 1 6 6 1 10 6 5 0 12 4 3

110 10 7 3 209 9 124 173 7 17 175 107

1 2 1 0 0

36 12 15 2 6

Barquıń 2012, von Fumetti and Nagel 2012), and the potential for recovery (Ilmonen et al. 2012). Here, we will briefly review the current knowledge in fundamental and applied crenobiology, including the often ignored role of spring habitats in the conservation of freshwater biodiversity (Boon and Pringle 2009). Springs, Multiple Ecotones, and Distinct Habitats Biodiversity includes genetic, functional, and habitat diversity (Ward et al. 1999), and springs are important components of riverine landscape biodiversity (Ward and Tockner 2001, Ilmonen et al. 2012). Lamberti et al. (2010) defined ecosystem linkage as any process or attribute that connects different ecosystems in some manner. Based on this definition, springs can be considered multiple 3-way ecotones (Fig. 1) that link terrestrial and aquatic ecosystems, ground and surface waters, and the spring and headwater stream in a 4-dimensional framework (longitudinal, lateral, vertical, and temporal; Ward 1989, Scarsbrook et al. 2007). Illies and Botosaneanu (1963) referred to the spring biocoenosis as the crenon and described the physical habitat as crenal. In all longitudinal models of running waters, springs occupy a separate zone because of their environmental peculiarities. Spring-fed streams are crenal (Ward 1994), flowing springs are rheocrenal (RK), and groundwater-dominated headwater streams are crenal/hypocrenal (KR) (Fu¨reder et al. 2002). The river

continuum concept (RCC) provided a framework for accommodating at least some types of springs in a longitudinal system (Vannote et al. 1980). The differentiation between spring and spring-fed stream varies with spring type. Some springs are isolated systems (Gervasio et al. 2004, Keleher and Rader 2008b). Seepages (helocrenes) and pool springs (limnocrenes) tend to be well defined and easily distinguished from any subsequent rivulets, whereas permanently flowing springs (rheocrenes) and springfed streams are part of a continuum from spring mouth to resulting stream (Cantonati et al. 2010c). As noted by Scarsbrook et al. (2007), the misuse of the term spring when referring to spring-fed streams (Erman and Erman 1995) has led to confusion in the scientific literature. Springs have distinct physical, chemical, and biological characteristics that change downstream (Gerecke et al. 1998), and Gerecke et al. (2007) suggested using empirical evidence to delimit the eucrenal zone. In flowing springs, morphological (e.g., change in slope), or biological (e.g., bryophyte cover and presence of spring-dwelling invertebrates, such as water mites) criteria can be used to delimit the eucrenal from the hypocrenal and epirhithral zones (Cantonati et al. 2006, 2007, Spitale et al. 2012b). Spring biotopes are characterized by marked insularity and disjunct distributions and can be distinguished from the neighboring stream and groundwater habitats by the presence of specific and well differentiated biocoenoses. The presence of species

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SPRINGS: HOTSPOTS FOR BIODIVERSITY CONSERVATION

FIG. 1. The complexity of the spring-habitat, drainagebasin, and aquifer-mediated potential impacts, supplemented by the 3-way ecotone structure (modified from Cantonati et al. 2006 with permission from Springer Science+Business Media B.V.).

with restricted distributions is expected in more isolated freshwater systems because of geographical (e.g., catchment divides) and physicochemical barriers. As a result, in the absence of human disturbance, low gene flow and local radiation can lead to considerable interdrainage variation in biodiversity and to high levels of endemism (Dudgeon et al. 2006). Some species are typically found in springs (Cantonati et al. 2006, 2010c), either inhabiting the spring mouth exclusively (crenobionts) or preferentially colonizing springs and other comparable aquatic habitats (crenophiles; Ilmonen et al. 2012, Martin and Brunke 2012). In Austrian springs, Staudacher and Fu¨reder (2007) identified 22 to 24% crenobiontic, and 8 to 21% crenophilous taxa along a gradient of aggradation (from aquatic to semiterrestrial). Important environmental factors include constant temperature (see Glazier 2012 for the role of temperature in shaping spring invertebrate communities), the existence of a permanently

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unfrozen area of wet soil around seepage springs (Fischer 1996), lower levels of competition caused by shorter food chains, and the rarity of top predators (Lavandier and Dećamps 1984). Representatives of several invertebrate groups, once thought to be crenobionts, recently were found to colonize a wider range of habitats. However, for groups such as Diptera, more research is required to understand whether some species are indeed confined to spring habitats (e.g., Wagner et al. 1998, Stur and Wiedenbrug 2006). In parallel with the decrease in supposed obligate crenobionts, the number of crenophilous species is rising, e.g., caddisflies, vascular plants, bryophytes, diatoms, and cyanobacteria (Zechmeister and Mucina 1994, Cantonati et al. 2006, 2010c and references therein, Ilmonen 2008). The small desmid Oocardium stratum Na¨geli is a typical example of a rheophilic, crenophilous alga, previously and erroneously considered crenobiontic. It builds characteristic carbonate tubes and can be abundant in hard-water spring streams with the typical conditions required for active calcification: depressed pH, CO2 oversaturation, gradual CO2 degassing, and reduction of alkalinity and conductivity (Rott et al. 2012). These conditions lead to algae-mediated biogenic calcification, which can predominate in lower sections of spring streams, where pCO2 equilibrium with the atmosphere has largely been reached (Golubic´ et al. 2008). However, Oocardium also has been recorded from groundwater upwelling areas of larger streams and rivers (e.g., Golubic´ et al. 2008). The highest proportion of well documented spring habitat specialists have been found among water mites, dipterans, hydrobiid snails, bryophytes, and caddisflies (Cantonati et al. 2006). Their distributions must be considered on a regional scale because species with a wide ecological range may become specialists at the margins of their range (regional stenotopy) (e.g., Ilmonen et al. 2012, Martin and Brunke 2012). Reasons for Species Richness: Spatial Heterogeneity at the Habitat Scale Springs are often very small ecosystems, but they are also very numerous. Glazier (2009) estimated that there are .4 springs/km2 (global total .57 3 106 excluding Antarctica) and .105 thermal springs worldwide. Heterogeneity and variability of environmental factors generate high habitat diversity and high total species richness. Spring types have been variously classified based on hydrology, geology, hydrochemistry, water temperature, biological assemblages, and human use (Glazier 2009). Springs whose water temperature approximately equals mean annual air temperature (MAAT) for their

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catchment should be called ambient springs (Glazier 2009) or nonthermal springs (or cool springs; Sanders et al. 2010). The term cold springs should be reserved for springs with temperatures below MAAT, whereas temperatures in thermal springs are significantly above MAAT. Several categories of thermal springs exist, e.g., hot springs are above human body temperature (Glazier 2009). The hydrochemistry of most springs reflects the lithology of the aquifer. Mineral springs are characterized by high concentrations of §1 ions. Most hot springs are also mineral springs (Castenholz 1969). Iron springs are intensely colonized by iron bacteria, particularly the genus Leptothrix, but have poor algal communities (Cantonati et al. 2006, 2012a, b). Guasch et al. (2012) found that an iron spring was characterized by a low-productivity, stress-tolerant community of low algal biomass, absence of cyanobacteria, and dominance of the diatom Navicula cincta (Ehrenberg) Ralfs. Teratological forms of Achnanthidium minutissimum (Ku¨tzing) Czarnecki dominated diatom assemblages in metal-rich (Cu, Cd, Zn) springs (Cantonati 1998, MC, unpublished data). Hard-water springs have high concentrations of Ca2+ and HCO32 and, because of supersaturation, some degas CO2 and precipitate carbonate deposits (spring-associated limestones [SAL]; Sanders et al. 2010) where they emerge. This process may be enhanced by CO2 removal by photoautotrophs, such as calcifying cyanobacteria (e.g., Rivularia and Scytonema), the desmid Oocardium stratum (Rott et al. 2012), bryophytes like Eucladium verticillatum (Brid.) Bruch et Schimp. in B.S.G. and Palustriella commutata (Hedw.) Ochyra, the xanthophyte Vaucheria, or thick diatom biofilms (Sanders et al. 2010). The traditional biological classification of springs by Steinmann (1915) and Thienemann (1924) was mainly based on current velocity at the spring mouth. Limnocrenes or pool springs occur in water-filled depressions and lack noticeable currents. Helocrenes or seepage springs are characterized by the diffuse emergence of slow-flowing water and the development of a swampy zone. Rheocrenes or flowing springs have stream-like flow velocities (Cantonati et al. 2006). This classification is still widely used in crenobiological research, but most springs are of intermediate types (e.g., Schwoerbel 1959, Martin and Brunke 2012). The most important environmental factors for the 2 most common spring types in the European Alps, rheocrenes and helocrenes, are current velocity and moisture gradient with the presence of semiaquatic habitats, respectively. In helocrenes, strong changes in faunal composition can occur if nearby sites represent a gradient from aquatic to semiterrestrial moist areas (Staudacher and

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Fu¨reder 2007, Gerecke et al. 2011). In forest springs that are particularly rich in litter, permanently moist leaves form an important habitat for spring-specific animals (Nielsen 1950). Tomaselli et al. (2011) presented a phytosociological classification based on the study of 81 springs in the Italian Alps. Two vegetation types, PlatyhypnidioFontinalietea antipyreticae and Montio-Cardaminetea (nonsubmerged plant communities with variable mixtures of bryophytes and vascular plants) make up most of what is regarded as crenic vegetation. Most spring communities belong to the Cratoneurion commutati alliance, represented by 6 different vegetation types. In general, spring types can be characterized by specific assemblages of algae (Cantonati et al. 2012a, b) and zoobenthos (Hahn 2000, Zollho¨fer et al. 2000, Schindler 2005, Kubı´kova´ et al. 2012, Martin and Brunke 2012). In North America, Glazier (1991) found that nonemerging taxa, such as crustaceans, mollusks, and triclads, dominated communities in relatively old (in geological terms) hard-water limestone springs, but emerging insects dominated the fauna of acidic, soft-water springs. The interpretation that a relatively high diversity of emerging insects reflects a relatively low long-term habitat stability, and vice versa, is supported by observations by Gerecke et al. (2009a). In fact, zoobenthos community analysis provides highly differentiated information for spring classifications on both global and regional scales (Hahn 2000, Zollho¨fer et al. 2000, Schindler 2005, Schro¨der et al. 2006, Kubı´kova´ et al. 2012, Martin and Brunke 2012). All major groups of organisms should be considered in addition to hydrological and physicochemical characteristics to develop more comprehensive regional typologies (Cantonati et al. 2006). Such typologies are important because some springs may be floristically unremarkable, but contain an unusual fauna, or vice versa (Zollho¨fer 1997). However, Spitale et al. (2012a) found that multitaxon classifications produced congruent results only for some spring types (helocrenes and limnocrenes). Elsewhere, several groups of organisms, including photoautotrophs, meiofauna, and macroinvertebrates, generated different classifications. Reasons for Species Richness: Spatial Heterogeneity at the Microhabitat Scale Geologically, a spring is defined as a place where groundwater reaches the surface (Cantonati et al. 2006, Scarsbrook et al. 2007, Glazier 2009). Its characteristics (e.g., hydrological stability) are determined by the hydrogeological features of the parent aquifer (van der Kamp 1995). Despite their usually

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small size, springs have high ecological value (Odum 1971). Some, including karst flowing springs, are large and often have seasonally variable discharge or form scenic waterfalls appreciated by the general public, which is otherwise often unaware of the existence or importance of spring habitats (Cantonati et al. 2010a). The biological complexity generated by the mosaic of microhabitats was highlighted by Illies and Botosaneanu (1963). Gooderham et al. (2007) suggested an upper stream zonation scheme that recognized an upstream heterogeneous zone (UHZ) characterized by a high ratio of structural component size to stream width. Structural components include large rocks, tree roots, and woody debris, all of which can constrain the morphology, hydraulics, and habitat distribution of small headwater streams. This situation is maintained by the benign hydraulic conditions in small headwater streams, which can uncouple the link between physical and biological heterogeneity and also fail to move the stream bed and bank material. It follows that low stream force within the UHZ is ultimately responsible for its greater internal physical heterogeneity than downstream reaches and is a fundamental driver of its structure and ecology. In addition to large morphological components, sand and fine detritus can accumulate under stable conditions. In a study of spring invertebrates of a landslide area in Carinthia (Austria), Staudacher and Fu¨reder (2007) found that high species diversity and abundance were linked primarily to habitat complexity and to the occurrence of lotic and lentic areas in the eucrenal zone. Lencioni et al. (2012) identified a larger number of chironomid genera and species in more hydromorphologically heterogeneous springs with diverse microhabitats in the European Alps, with many taxa showing preferences for particular spring types and substrata. No taxa were exclusive to helocrenes, hygropetric rheocrenes, or rheolimnocrenes, but several taxa occurred only in rheocrenes, rheohelocrenes, hygropetric rheocrenes, or limnocrenes. Organisms that are abundant in springs, such as chironomids (Ferrington 1995, Stur and Wiedenbrug 2006, Lencioni et al. 2012), can influence community- and ecosystem-level properties. In a large, spring-fed stream in northern Michigan (Carp Creek) micropatches around individual chironomids and their retreats affected periphyton species diversity and algal production (Pringle 1985). Disturbance in Spring Habitats: Low or High? Springs are often regarded as relatively stable ecosystems. However, only perennial springs fed by deep, large, nonkarstic aquifers are actually stable.

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The reduced variability of some environmental factors in such springs and their relatively discrete boundaries led several scientists to choose them as model ecosystems (Glazier 2009). Odum (1957) considered the chemostatic, steady-state ecosystem of the Silver Springs in Florida (USA) as a natural ‘‘giant constant temperature laboratory’’ in which to investigate energy flux and function in trophic food webs. Headwaters originating from large springs in various locations in North America (Minckley 1963, Pringle 1985, Kemp and Boynton 2004) differ from the type of springs studied by the authors of most papers in this special issue, which have lower discharge, smaller surface area, and considerable variation in environmental conditions. Disturbance is central to lotic ecology (Stanley et al. 2010). Stevenson (1996) stated that the dynamic, disturbance-driven nature of benthic habitats is important for understanding the complex relationships between benthic algal abundance and current velocity. A study by Scarsbrook et al. (2007) supported the hypothesis that flow permanence and variability are the primary determinants of invertebrate community patterns in springs. Marked patchiness of microhabitats appears to characterize lotic systems in general, but these patches are much more stable in springs than further downstream. For example, in the Adamello-Brenta Nature Park in the southeastern Alps, after spates, cyanobacteria-dominated macroscopic periphyton was almost completely removed from the stream bed, but remained almost unaffected by scour in the springs themselves (MC, unpublished data). In the Berchtesgaden National Park, Germany, headwaters are frequently faunally and floristically impoverished because of scour during spates and snow cover, whereas the source area (eucrenal) is much more stable (Gerecke and Franz 2006). Thus, springs fed by slope detritus aquifers can function as refugia for many invertebrates, e.g., in the alluvial plain of a glacial stream in the Swiss Alps (Klein and Tockner 2000) and in lowland rivers with interrupted surface flow during summer drought in Sicily (Gerecke 1991). When fed by 0-order basins with small storage capacity and short flow paths, smaller springs and headwaters can be closely linked to hillslope processes and can be characterized by more spatial and temporal variation in environmental factors than downstream reaches (Gomi et al. 2002). Cantonati et al. (2012a, b) found high proportions of xerotolerant, pseudaerial diatoms (Johansen 2010) and other benthic algae indicating a small, variable discharge or periodic drought, whereas some recently described diatom species appear to be typical of intermittently

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wet spring habitats (Cantonati and Lange-Bertalot 2006, 2009, 2011, Cantonati et al. 2009c). On the other hand, certain invertebrates are potential indicators of flow permanence in springs (Scarsbrook et al. 2007). As a general rule, the presence of larger populations of taxa with limited recolonization capacity and sensitivity to drought, e.g., crustacean macroinvertebrates and water mites, indicates springs with stable flow (Gerecke et al. 2009a). On the other hand, temporary springs are characterized by a high proportion of taxa with drought-resistant eggs or developmental stages (Oligochaeta and microcrustaceans), taxa that are able to survive on the surface near groundwater (niphargids and some hydrobiid mollusks), or insects with a high dispersal and recolonization capacity (several species of chironomid midges and limnephilid caddisflies). Despite the apparently more stable environmental conditions, Spitale et al. (2012b) found higher variability of diatom and macroinvertebrate assemblages in the eucrenal zone of spring-fed streams in a study of longitudinal distribution (eucrenal–epirhithral) and seasonality. Attempts to test the Intermediate Disturbance Hypothesis (Connell 1978) have not produced consistent results for spring habitats. The high diversity of spring organisms may be a result of the coexistence of contrastingly disturbed microenvironments resulting from the mosaic nature of many spring habitats. Species richness in alpine rheocrenes with low levels of disturbance is intermediate between that in the kryal (high levels of disturbance) and the rhithral (medium levels of disturbance) zones (Ward 1994). Several authors found an increase in macroinvertebrate assemblage diversity from the spring (low disturbance) to downstream habitats (intermediate disturbance) (Erman 1992, Bonettini and Cantonati 1996, Kiss and Schmera 1996). Epilithic and epiphytic diatom assemblages in springs on siliceous substrata with moderately variable environmental factors were more diverse than those in carbonate spring-fed streams with higher disturbance resulting from faster currents (Cantonati et al. 2006 and references therein). Verdonschot (2006) compared the invertebrate fauna of groundwater- and rainwater-fed streams and found more species in the latter, which experienced a larger daily range in temperature. However, relationships between disturbance, variability, and diversity are not always predictable. Death and Barquıń (2012) found that spring-fed streams with low hydrological disturbance had low diversity in Spain but high diversity in New Zealand and attempted to explain such apparently contradictory findings by differences in insect life histories. Bo-

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nettini and Cantonati (1996) reported that macroinvertebrate diversity was highest in springs with low flow, but lowest in a spring with high flow variability, whereas von Fumetti and Nagel (2012) found the highest macroinvertebrate diversity in 2 relatively stable springs but the lowest in a highly variable spring. The role of anthropogenic disturbance requires further studies. Ilmonen et al. (2012) found lower bryophyte richness in springs affected by human activities, e.g., forest management and drainage, but macroinvertebrate richness did not differ between impacted and reference springs. Species Richness and the Role of the Substratum Springs are biodiversity hotspots (Scarsbrook et al. 2007, Ilmonen et al. 2012) and require protection to preserve their habitat (Cantonati et al. 2006, 2010c). Weigand (1998) reported .500 invertebrate taxa from 792 springs in the Kalkalpen National Park, Austria, and Gerecke et al. (2009a) recorded 735 invertebrate taxa in a survey of 75 springs in the Berchtesgaden National Park, Germany (1994–2005). Spitale et al. (2012a) found that, of 84 springs in the Italian Alps, low-discharge and small-surface springs were frequently the most species-rich, at least for microbiota (copepods, chironomids, water mites, diatoms, nematodes). Weigand (1998) noted that the number of invertebrate taxa was significantly higher in small springs on carbonate substrata than in large karst springs, probably because of the diversity of suitable microhabitats. Cantonati et al. (1996) found the highest number of cyanobacteria in a small, hygropetric rheocrene spring in the Adamello-Brenta Nature Park, Italian Alps. Diversity varies among lithological substrata and microhabitats (choriotopes), and different groups of organisms show contrasting patterns. Cantonati et al. (2007) provided guidance for substratum selection when sampling benthic algae in springs. Werum and Lange-Bertalot (2004) distinguished between characteristic diatom assemblages on different geological formations (cf. Cantonati and Lange-Bertalot 2006). As found for stream invertebrates (Braukmann 1987), zoobenthos, cyanobacteria, and nondiatom algae were more diverse, but diatom diversity was lower on carbonate substrata (Bonettini and Cantonati 1996, Cantonati et al. 1996, Cantonati 1998, 2008). Dumnicka et al. (2007) found that substratum type (fine vs coarse substrata) was the main discriminatory factor affecting invertebrate density, whereas community composition was related to geographical location. In contrast, in the Berchtesgaden Alps,

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invertebrate communities clearly reflected substratum composition, with some species associations restricted to fine detritus and others to hard mineral substrata. Communities on organic substrata had a higher proportion of typically crenal species, whereas species preferring hard substrata also were found further downstream in hypocrenal and epirhithral zones (Schro¨der et al. 2006). Diatom (Cox 1988) and invertebrate (Reiss 2011) assemblage composition varies among microhabitats (water plants, silt, sand grains, cobbles). Soininen and Eloranta (2004) found that epilithic, epiphytic, and epipelic diatoms in boreal rivers in southern Finland were distinctly different, and that several species showed a preference for one or other substratum. In the southeastern Alps, crenal diatom assemblages were more species-rich and diverse (Shannon–Wiener) on bryophytes than on stones (Cantonati 1998, Angeli et al. 2010), and several diatom taxa showed a significant preference for a particular substratum (Cantonati and Spitale 2009, Cantonati et al. 2012a). However, variance partitioning showed that the percentage of diatom community variance explained by environmental variables (40%) exceeded that explained by substratum (stones vs bryophytes, 3%) (Cantonati and Spitale 2009). Bertrand et al. (2004) and Passy (2006) suggested that bryophytes are a neutral substratum for diatoms in running waters, but others found assemblage differences related to the host bryophyte species (Poulıćˇkova´ et al. 2004) or to morphological characteristics, such as leaf form (Pentecost 1991). Johansen (1999) proposed the term bryophytic diatoms for species associated with bryophytes. A bryophilous diatom genus, Microfissurata, was described recently (Cantonati et al. 2009c). Cantonati et al. (2012a) advocate using bryophytes as a target substratum for diatom collections in springs because bryophytes usually host more diverse assemblages than do stones (Cantonati and Spitale 2009) and are usually available and easy to sample. Bryophyte diatom communities have been studied for a long time in many parts of the world (Cantonati et al. 2009c and references therein), but investigations on other algae associated with bryophytes are extremely rare. Such assemblages also differ markedly between stones and bryophytes. Epilithon has more taxa and higher Shannon–Wiener diversity than epibryon (Cantonati 2008). Rare and Red List Species Most oligotrophic aquatic habitats are headwaters or the springs from which they originate. Lowe and Likens (2005) emphasized the importance of headwa-

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ters for rare and endangered species and as refugia for riverine species during specific stages of their life histories. Evidence is growing that water quality, biodiversity, the ecological integrity of freshwater systems, and thus, their capacity to provide ecosystem services all depend on headwater stream function (Gomi et al. 2002, Lowe and Likens 2005, Meyer et al. 2007). Oligotrophic aquatic habitats have been neglected by ecologists and taxonomists, whose attention has been focused on anthropogenically affected aquatic environments (eutrophication, acidification). Oligotrophic habitats are threatened by direct (exploitation for hydropower and drinking water, land reclamation, nutrient enrichment, etc.) and indirect (diffuse airborne pollution, climate change) impacts. They often are located in protected areas, which facilitates their conservation, and they are important reference sites for biomonitoring and ecological restoration projects (Kociolek and Stoermer 2009). The diatom flora of oligotrophic habitats has received renewed attention only in the last 15 y, but can provide important information on their integrity. A recently described species, Cymbella tridentina Lange-Bertalot, Cantonati et Scalfi, was absent from structurally modified or N-enriched springs and is likely to be a valuable indicator of the naturalness of the upper reaches of mountain springs on carbonate substrata (Cantonati et al. 2010c). Most strictly oligotraphentic diatom taxa are endangered and on a Red List proposed for Central Europe by LangeBertalot (1996). Many new diatom taxa are still being discovered in oligotrophic habitats, even in a well investigated area such as Central Europe (Werum and Lange-Bertalot 2004). Thus, shoe-horning taxa into species aggregates common to meso- and eutrophic waters must be avoided. During recent research projects on springs in the European Alps, 11 new species and 2 new diatom genera were described (Cantonati and Lange-Bertalot 2006, 2009, 2010, 2011, Cantonati et al. 2009c, 2010b). Moser et al. (1998) reported 40% new species for the freshwater diatom microflora of New Caledonia, probably because of the high number of oligotrophic to ultraoligotrophic inland waters. Werum (2001) found highest taxon richness, Shannon–Wiener diversity, and evenness in diatom assemblages in springs on siliceous substrata in mid-altitude mountains of Germany unaffected by anthropogenic impacts. The condition of these springs was effectively indicated by the proportion of rare or endangered Red List taxa, which was significantly reduced in sites affected by acid deposition and higher NO32 concentrations or by intermittent discharge. Spring capture had more pronounced effects on the proportion of Red List species than on the

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Shannon–Wiener diversity index. Diatom Red List species typically constitute 40–50% of crenic species in protected areas of the European Alps (Cantonati 1998, Cantonati and Spitale 2009, Cantonati and LangeBertalot 2010, Cantonati et al. 2012a) but decline significantly in more densely inhabited areas (Werum and Lange-Bertalot 2004, Taxbo¨ck and Preisig 2007, Angeli et al. 2010; Table 2). Limited data on other algal groups, complicated by rapid changes in taxonomy and nomenclature, often hamper the designation of rare taxa. Based on river and stream studies over 20 y (Rott et al. 1999), ,50% of cyanobacteria and nondiatom algae in springs of the Alps can be considered rare (Cantonati 2008, Cantonati et al. 2012b), whereas a much lower percentage of rare taxa is found in streams. Taxonomic analyses of other groups also reveal new species and interesting evolutionary and biogeographical scenarios. At least 12 new caddisfly species have been discovered in ravine springs in Florida (A. K. Rasmussen, M. L. Pescador, and S. C. Harris, Florida A&M University, unpublished data). The water mite Apheviderulix welwitschioides Gerecke, Smith et Cook, belongs to a family found recently in Mediterranean springs, and other members of the genus occur in the interstitial zones of streams in the Sahara and California, a pattern revealing that this clade is old and was distributed around the Tethys Sea before the formation of the Atlantic Ocean. One species of Ignacarus, a genus known from hypersaline springs on the Iberian Peninsula, is the only known freshwater mite that reproduces viviparously (Moreno-Alcaraz et al. 2008). Lebertia hygropetrica Gerecke from the Southern Alps is a representative of a plesiotypic subgenus (Brentalebertia) containing another crenobiontic water mite from Central Europe and a stream-dwelling species endemic to the Canary Islands (Gerecke 2008, 2009, Gerecke et al. 2009b). This list of remarkable findings could easily be extended, and many discoveries are to be expected, especially in areas not covered by the Holocene glaciations. Ilmonen et al. (2012) found more Red List bryophyte and macroinvertebrate taxa in undisturbed springs than in springs affected by forest management and drainage. Relevant percentages of Red List invertebrates in springs are given in several papers (Ilmonen et al. 2012, Martin and Brunke 2012). However, developing a general threat assessment for spring-dwelling animals is difficult because the most interesting taxa are still poorly documented. In the few Red Lists available for Central European aquatic insects, spring-dwelling species are often classified as endangered simply because their pre-

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ferred habitats are endangered. However, the main problem is that the regional diversity of the most frequently encountered taxa in spring habitats, i.e., members of numerous dipteran families, microcrustaceans, and water mites, is poorly known. Faunal inventories of spring habitats undoubtedly produce remarkable results, even in parts of the world that are considered well documented. An ongoing long-term monitoring project of limestone spring habitats in the Berchtesgaden National Park (Upper Bavaria) contributed 7 new dipteran species and §30 new faunal records for Germany (Gerecke and Franz 2006, RG, unpublished data). Studies on springs in the Gesaüse National Park (Styria) contributed 7 new species and .100 new records for Austria (Gerecke et al. 2012). Least-Impaired Habitat Relicts In areas where human effects are widespread, springs can be the least-affected freshwater habitats. They serve as refugia for sensitive organisms and hold a large percentage of the regional species pool (habitat islands; Werum 2001). Werum and LangeBertalot (2004) found 52% of the freshwater pennate diatom microflora of Central Europe in mountain springs near Frankfurt, Germany. Botosaneanu (1995) defined taxa found only in unimpacted springs in densely inhabited and heavily exploited areas as geographic relicts. This term is unfortunate because it might be confused with biogeographical patterns that depend on thermal conditions of springs, e.g., organisms that colonized a wider range of habitat types during colder or warmer periods but are now confined to springs (Nielsen 1950, Hynes 1970, Cantonati et al. 2006). The flatworm Crenobia alpina Dana, a classical glacial relict, lives in headwaters because it cannot tolerate warm temperatures, whereas the caddisfly Rhyacophila laevis Pictet, is considered a Tertiary relict, which colonized large parts of central Europe in warmer periods. It now lives in springs because it cannot tolerate low winter temperatures in running waters (Fischer 1996). Similarly, benthic diatoms with boreal distributions colonize the deeper parts of lakes with cold, almost-constant temperatures at the southern edge of their distribution range (e.g., Kingston et al. 1983). To avoid confusion with geographic (sensu Botosaneanu 1995), glacial, or Tertiary relicts, we propose least-impaired habitat relicts to replace Botosaneanu’s geographic relicts. Springs as Threatened Habitats Freshwater makes up only 0.01% of the world’s water, occupying ,0.8% of the Earth’s surface. However, this small fraction supports almost 6% of

27

Springs in Vorarlberg, Austria, Alps Western Carpathians Southeastern Alps

Carbonate springs

Pre-Alpine carbonate springs Carbonate springs Carbonate springs

Areas of Basel and Zu¨rich, Switzerland Verona Province, pre-Alpine Beauce region, Orleánais, northern France Bavaria

21 3

DBNP, southeastern Alps JPNP, southeastern Alps ABNP, southeastern Alps

Carbonate springs and streams Low-altitude carbonate springs Lake Tovel (epilithon euphotic zone) Mountain springs Helocrene springs (spring fens) Lake Garda

Springs (all main lithologies)

17 25 14

24

30 110

10

GNP, northeastern Alps ABNP, southeastern Alps ABNP, southeastern Alps Trentino, CRENODAT, southeastern Alps Vicinities of Frankfurt

Carbonate springs Crystalline high-mountain lakes Carbonate and crystalline springs Springs (all main lithologies)

5 9

N

Danta di Cadore, southeastern Alps BNP, northeastern Alps

Location

Mire pools Carbonate springs

Habitat type

8

30 24 23

38 33 33

41 40 40

43

52 50 48 45

72 54

% RL

118 138 135

75

197

131 60

254

100

86 104

TNT

42

32 36

54

26

26 30

MNTc

Taxbo¨ck and Preisig 2007 Angeli et al. 2010 Bertrand et al. 1999 Fritscher 2004

NO32

Gesierich and Kofler 2010 Frańkova´ et al. 2009 Spitale et al. 2011

Werum and Lange-Bertalot 2004 Cantonati and Spitale 2009 Cantonati 2004 Cantonati et al. 2009b

Cantonati et al. 2011b Cantonati and LangeBertalot 2010 Cantonati 2012 Tolotti 2001 Cantonati 1998 Cantonati et al. 2012a

Reference

NO32, capturing NO32

NO32, altered shore morphology

org pol (str) org pol

ctp ctp

ctp ctp

Impacts

TABLE 2. Oligotrophic habitats (bold indicates springs) ranked by decreasing percentage of threatened Red List (Lange-Bertalot 1996) diatom taxa. % RL = % diatom taxa belonging to the sum of all threatened Red List categories, N = Number of sampling stations, TNT = total number of taxa found, MNTc = maximum number of taxa counted in 1 sample, ctp = close to pristine, org pol = organic pollution, str = streams, ABNP = Adamello-Brenta Natural Park (Trentino, Italy), CRENODAT Project (Autonomous Province of Trento = Trentino, Italy), DBNP = Dolomiti Bellunesi National Park (Veneto Region, Italy), CESSPA Project (Province of Verona, Veneto Region, Italy), BNP = Berchtesgaden National Park (Bavaria, Germany), GNP = Gesaüse National Park (Styria, Austria), JPNP = Julian Prealps Natural Park (Friuli Venezia Giulia Autonomous Region, Italy). Bold indicates springs habitats and % RL.

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all described species (Dudgeon et al. 2006). Inland waters and freshwater biodiversity are valuable natural resources in scientific, cultural, economic, and aesthetic terms and provide a variety of valuable goods and services that contribute to economic productivity and maintain genetic diversity (Covich et al. 2004, Dudgeon et al. 2006). Their conservation and management are critical to human welfare. Freshwaters are experiencing far greater declines in biodiversity than the most affected terrestrial ecosystems (e.g., Sala et al. 2000, Strayer and Dudgeon 2010) and deserve greater conservation effort (Loreau et al. 2001). To date no comprehensive global analysis of freshwater biodiversity is available. Existing data are biased in terms of geography, habitat type, and taxonomy, and many communities and habitats have not been monitored at all (Dudgeon et al. 2006). This bias is exacerbated by the loss of taxonomic expertise and collections. Steinman et al. (2010) suggested that future research should prioritize interdisciplinary investigations to address environmental problems and protect water resources within an economic, social, and political context. Further studies on springs must be more strategic to complement existing knowledge and target specific pressures (Cantonati et al. 2012a, b, Lencioni et al. 2012, Spitale et al. 2012a, b). As sources of high-quality water, springs are frequently places of cultural and mythological significance. However, public awareness that these habitats are also of great importance for nature conservation is still very limited. Springs are often exploited to obtain drinking water or to generate hydroelectric power. These pressures are likely to increase as a result of climate change, given a predicted reduction and increasing irregularity of precipitation (Cantonati et al. 2007). Springs are extremely sensitive to disturbance because of their small size and the importance of the fringing semiaquatic habitats. In most cases, water abstraction results in the destruction of the original morphology and severe impoverishment of the biota. National or regional legislation on the use of spring and groundwater for drinking focuses on prevention of microbiological contamination. It usually involves protecting the area around the spring (fencing), but also requires excavation of the spring mouth down to the bedrock (or aquifer) and construction of closed, mostly concrete, housing including several deposition basins. This practice removes the natural spring habitat and its organisms. Uncaptured springs are often compromised in farmed areas by nutrient enrichment, trampling cattle, sediment input, and damage or removal of the surrounding vegetation or in forests by forest management that alters their hydrology (Weigand 1998, Cantonati et al.

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2006, Frańkova´ et al. 2009, Gesierich and Kofler 2010, Reiss 2011, Ilmonen et al. 2012). In many European regions, natural spring habitats have virtually disappeared and, even in protected areas, their numbers are shrinking. A spring inventory by Zollho¨fer (1997) in the Kanton of Aargau, Switzerland, showed that, even in 1880, .75% springs were affected by water abstraction and transformation into wells, and by 1990, 95% were affected. Identifying and mapping their spatial distribution is an essential, but poorly appreciated, prerequisite to protecting and managing spring habitats (Cantonati et al. 2007). Springs are explicitly mentioned in environmental legislation in only a few countries (e.g., Finland; Ilmonen et al. 2012), and organized initiatives to protect springs are rare (Hotzy 2007). Springs and small headwater catchments (,10 km2) are not covered by the European Union Water Framework Directive (EU-WFD 2000), and the only spring type mentioned in Annex I (Natural habitat types of community interest whose conservation requires the designation of special areas of conservation) of the 1992 European Union Directive on the conservation of natural habitats and of wild fauna and flora are calcareous tufa springs as ‘‘7220 Petrifying springs with tufa formation (Cratoneurion)’’, priority habitat type (EU-HD 1992, Evans 2006, Jokic and Galz 2007). Nutrient enrichment and higher water temperature can impede calcification and tufa formation in these springs, resulting in the decline of characteristic taxa (Rott 1991, Rott et al. 1999, 2012, Golubic´ et al. 2008, Sanders and Rott 2009). Further legislation is required to protect other types of springs and headwater catchments in general. Springs and Biodiversity Conservation At smaller geographical scales, species turnover (ßdiversity) between drainage basins and water bodies is substantial, and many freshwater species have restricted ranges (e.g., Strayer et al. 2004). Combined with endemism, these attributes result in a lack of substitutability among freshwater habitat units, and protection of one or a few water bodies preserves only a small proportion of freshwater biodiversity within a region (Dudgeon et al. 2006). Single springs rarely contain a significant number of rare and Red List diatom species (Cantonati and Spitale 2009, Cantonati and Lange-Bertalot 2010, Cantonati et al. 2012a). Similar observations on aquatic lichens, cyanobacteria, nondiatom algae, and zoobenthos highlight the marked heterogeneity of spring habitats (Bonettini and Cantonati 1996, Cantonati 2008, Nascimbene et al. 2011, Cantonati et al. 2012b). Bond and Chase (2002)

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showed that species diversity becomes increasingly important to ecosystem functioning at higher (regional) spatial scales. Ricklefs (1987) stressed that local diversity depends upon regional diversity and that the reduction and fragmentation of habitat area can lead to a decline in both regional and local diversity to a lower level from which there is no recovery. Thus, conservation efforts will have to include a large area and number of springs, including different spring types and lithological substrata. Some types of springs have a greater potential to contribute to biodiversity conservation because they are more species-rich and host more specialized taxa than others. Studies by Cantonati et al. (2006) and Spitale et al. (2012a) suggest that helocrenes, rheohelocrenes, and hygropetric rheocrenes host the most specialized and taxon-rich communities and should receive particular protection (Cantonati et al. 2009c, 2012a, b, Cantonati and Lange-Bertalot 2010, Gerecke et al. 2011). However, other spring habitats also may support unusual communities, e.g., rock-face seepages (Collier and Smith 2006) or thermal springs (Nikulina and Kociolek 2011), and even very small springs can contribute effectively to freshwater biodiversity conservation. However, only larger springs can support larger animals, e.g., large (previously unknown) fish in karstic freshwater desert springs in the Arabian peninsula (Krupp 1992). Preservation of unimpacted freshwater bodies and their biodiversity remains a priority, but even damaged habitats can support significant portions of their original biodiversity (Dudgeon et al. 2006). Rosenzweig (2003) advocates a reconciliation ecology approach to enhancing species richness in humandominated landscapes. Established practices, such as stream restoration or more sustainable water abstraction, are only rarely applied to springs, and data on their success are still rare. Cantonati et al. (2009a) studied the potential of residual habitats after spring capture and showed a dramatic reduction in both diatom and zoobenthos densities. Microhabitats and their location were very important in determining which cyanoprokaryotes and algae colonized the residual habitat. Few guidelines exist for management and conservation of springs (Sada et al. 2005, Scarsbrook et al. 2007) or for spring bioassessment (Keleher and Rader 2008a). Methods should be spring-specific and appropriate for the geographic area (Potapova and Charles 2002, Soininen 2007, Cantonati et al. 2012a, b). Using well-known taxa that are frequently treated as biodiversity indicators (typically vertebrates, vascular plants, and butterflies) and little-known taxa (such as termites, antlions, buprestid, and scarab

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beetles), Van Jaarsveld et al. (1998) looked for complementary sets (grids) in which each taxon was represented at least once. However, they found little support for the idea that complementary species sets are congruent across taxa, or that complementary sets are congruent with richness (hotspots, coldspots, or both) or areas harboring rare taxa. Thus, higher taxa have little value as surrogates for species, undermining proposals to use indicator species or higher taxa as basic biodiversity conservation planning tools. Conservation management requires reliable speciesbased information for many taxonomic groups from comprehensive surveys (Spitale et al. 2012a). Current Research and Implications for Future Studies Renewed interest in spring ecosystems is reflected by the increase in studies in the European Alps since the 1990s and the number of recent investigations in Europe and elsewhere (Ilmonen and Paasivirta 2005, Sada et al. 2005, Barquıń and Death 2006, Gerecke and Franz 2006, Staudacher and Fu¨reder 2007, Taxbo¨ck and Preisig 2007, Soninkhishig et al. 2008, Frańkova´ et al. 2009, Wojtal et al. 2009, Rott et al. 2010; IJ, personal communication; J. D. Wehr, Fordham University, and R. Sheath, California State University San Marcos, personal communication), including PhD studies (Barquıń 2004, Bertuzzi 2008, Spitale 2008, Frańkova´ 2009, Gesierich 2009, Reiss 2011; M. Mogna, University of Eastern Piedmont, personal communication; L. Taxbo¨ck, University of Zu¨rich, personal communication). This special issue addresses a number of relevant themes. The 1st group of papers focuses on spring biota, particularly those organisms that are less often studied or are particularly relevant to crenic ecosystems (diatoms, Cantonati et al. 2012a; benthic pro- and eukaryotic algae other than diatoms, Cantonati et al. 2012b; chironomids, Lencioni et al. 2012). The role of environmental factors including temperature (Glazier 2012) and substratum for taxon distribution, community composition, and richness (Cantonati et al. 2012a, Kubı´kova´ et al. 2012) are discussed. Several authors developed distribution models (Lencioni et al. 2012) or defined specific spring types with either a multitaxon approach or based on particular taxonomic groups (Cantonati et al. 2012a, b, Martin and Brunke 2012, Spitale et al. 2012a). The 2nd group of papers describes investigations of small-scale distribution patterns and longitudinal change from spring to stream (diatoms, benthic algae, bryophytes, and macroinvertebrates) and over time (Guasch et al. 2012, Kapfer et al. 2012, Rott et al. 2012, Spitale et al. 2012b). The 3rd group of papers analyzes the

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responses of crenic biota to natural (flow) variability (Death and Barquıń 2012, von Fumetti and Nagel 2012) and to anthropogenic disturbance (Ilmonen et al. 2012). Multitaxon studies provide an opportunity to discuss the benefits of an integrated vs single-taxon approach to the classification of springs and the definition of spring types (Cantonati et al. 2012a, Spitale et al. 2012a). Kapfer et al. (2012) evaluated the suitability of spring ecosystems as sites for long-term ecological research to study environmental change. This evaluation was important because springs can integrate the effects of direct and indirect impacts on the whole drainage basin in time and space (Cantonati et al. 2006; Fig. 1). The use of biota for monitoring reflects the combined effects of geology, climate, and anthropogenic impacts and potentially could provide a measure of groundwater quality and the status of individual aquifers (Williams 1991). A range of multivariate techniques was used to identify the most relevant environmental factors (Cantonati et al. 2012a, b). The importance of disturbance with respect to flow variability was studied using the gypsum-spheres method (von Fumetti and Nagel 2012), and relationships were investigated between diversity and disturbance in different geographical locations (Death and Barquıń 2012). Flow variability (ephemeral vs perennial springs, stable- vs variable-discharge springs), the marked heterogeneity of springs, and the structural complexity within spring habitats are considered the main reasons for high regional species richness. Some diatom, benthic algal, and invertebrate species were identified as indicators of periodic and intermittent springs (Scarsbrook et al. 2007, Cantonati et al. 2012a, b), and the resilience of crenic invertebrate communities to habitat degradation was tested (Ilmonen et al. 2012). Topics meriting further study include: 1) continued development of habitat-type and geographic areaspecific indices to evaluate the quality of crenic habitats (Cantonati et al. 2012a, b, Martin and Brunke 2012), 2) development and testing of new strategies for nondestructive methods of spring capture and for restoration of damaged habitats, 3) improvement of long-term ecological research in springs through international networking and the use of existing biological and physicochemical records, 4) investigations of functional aspects in crenoecology, 5) detailed taxonomic research using morphological and molecular methods, and 6) autecological studies of spring biota to improve their use as indicators. Conclusions Springs, although mostly small, are often numerous with diverse morphological, hydrological, and chemical

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characteristics. They can be the least-impacted aquatic habitats in a region and are often species-rich, providing a refuge for rare and sensitive, sometimes endemic, taxa. Thus, they contribute significantly to regional biodiversity (Sherwood and Sheath 1999, Minckley and Unmack 2000, Di Sabatino et al. 2003, Gervasio et al. 2004, Glazier 2009). Given their importance for the conservation of aquatic biodiversity, sufficient representative crenic types must be protected in different geographic areas. Interest in research on springs has increased in recent years, but this interest has been restricted to a few geographical areas. Given the increasing pressures on, and the predicted reduction in, high-quality freshwater resources, the attention of governments must be drawn to the need for the better protection of crenic ecosystems. Further targeted research and better dissemination of results will help to achieve this goal. Acknowledgements We are grateful to Pamela Silver for supporting this special issue, the Museo delle Scienze of Trento (Autonomous Province of Trento) for providing funding for page charges for papers authored or coauthored by MC, the University and Scientific Research Department of the Autonomous Province of Trento for funding the CRENODAT Project (Biodiversity assessment and integrity evaluation of springs of Trentino—Italian Alps—and long-term ecological research, 2004–2008) from which at least 5 papers in this issue resulted. Literature Cited ANGELI, N., M. CANTONATI, D. SPITALE, AND H. LANGEBERTALOT. 2010. A comparison between diatom assemblages in two groups of carbonate, lowland springs with different levels of anthropogenic disturbances. Fottea 10:115–128. BARQUIŃ, J. 2004. Spatial patterns of invertebrate communities in spring and runoff-fed streams. PhD Thesis, Massey University, Palmerston, New Zealand. BARQUIŃ, J., AND R. G. DEATH. 2006. Spatial patterns of macroinvertebrate diversity in New Zealand springbrooks and rithral streams. Journal of the North American Benthological Society 25:768–786. BERTRAND, J., J. P. RENON, AND O. MONNIER. 1999. Les diatomeés des sources du rebord karstique de la Beauce de la re´gion orleánaise. Symbioses 1:3–14. BERTRAND, J., J. P. RENON, O. MONNIER, AND L. ECTOR. 2004. Relation «diatomeés e´piphytes-bryophytes» dans les tourbie`res du Mont Loze`re (France). Vie Milieu 54: 59–70. BERTUZZI, E. 2008. Le sorgenti delle Alpi: complessita`, biodiversita` e indicatori di naturalita`/integrita`. Tesi per il conseguimento del Dottorato di Ricerca in Scienze Ambientali, University of Urbino, Urbino, Italy.

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BOND, E., AND J. M. CHASE. 2002. Local and regional controls of ecosystem function. Ecology Letters 5:467–470. BONETTINI, A. M., AND M. CANTONATI. 1996. Macroinvertebrate assemblages of springs of the River Sarca catchment (Adamello-Brenta Natural Park, Trentino, Italy). Crunoecia 5:71–78. BOON, P. J., AND C. M. PRINGLE. 2009. Assessing the conservation value of fresh waters: an international perspective. Cambridge University Press, Cambridge, UK. BOTOSANEANU, L. 1995. Springs as refugia for geographic relicts. Crunoecia 4:5–9. BRAUKMANN, U. 1987. Zoozo¨nologische und saprobiologische Beitra¨ge zu einer allgemeinen regionalen Bachtypologie (Zoocoenological and saprobiological contributions to a general regional typology of brooks). Archiv fu¨r Hydrobiologie (Beiheft) 26:1–355. CANTONATI, M. 1998. Diatom communities of springs in the Southern Alps. Diatom Research 13:201–220. CANTONATI, M. 2004. Le diatomee di tre sorgenti del Parco Naturale delle Prealpi Giulie (Italia nord-orientale). Gortania—Atti Museo Friulano di Storia Naturale 25: 95–108. CANTONATI, M. 2008. Cyanoprokaryotes and algae other than diatoms in springs and streams of the Dolomiti Bellunesi National Park (Northern Italy). Algological Studies 126:113–136. CANTONATI, M. 2012. Kieselalgen (Bacillariophyceae oder Diatomeae). Vielfalt der Quellen – Quelle der Vielfalt. Schriften des Nationalparks Gesaüse 7:86–99. CANTONATI, M., N. ANGELI, E. BERTUZZI, D. SPITALE, AND H. LANGE-BERTALOT. 2012a. Diatoms in springs of the Alps: spring types, environmental determinants, and substratum. Freshwater Science 31:499–524. CANTONATI, M., E. BERTUZZI, AND A. SCALFI. 2010a. CRENODAT (Biodiversity assessment and integrity evaluation of springs of Trentino - Italian Alps - and long-term ecological research): project design and preliminary results. Pages 121–132 in E. Beheim, G. S. Rajwar, M. Haigh, and J. Krecek (editors). Integrated Watershed Management: Perspectives and Problems (Proceedings of the Headwater ’05 Conference, Bergen, Norway, June 2005). Springer, Amsterdam, The Netherlands. CANTONATI, M., E. BERTUZZI, A. SCALFI, AND V. CAMPANA. 2009a. The potential importance for spring conservation of residual habitats after flow capturing: a case study. Verhandlungen der Internationalen Vereinigung fu¨r theoretische und angewandte Limnologie 30:1267–1270. CANTONATI, M., R. GERECKE, AND E. BERTUZZI. 2006. Springs of the Alps—sensitive ecosystems to environmental change: from biodiversity assessments to long-term studies. Hydrobiologia 562:59–96. CANTONATI, M., R. GERECKE, I. JU¨TTNER, AND E. J. COX (EDITORS). 2011a, Springs: neglected key habitats for biodiversity conservation. Journal of Limnology 70(Supplement 1). CANTONATI, M., AND H. LANGE-BERTALOT. 2006. Achnanthidium dolomiticum sp. nov. (Bacillariophyta) from oligotrophic mountain springs and lakes fed by dolomite aquifers. Journal of Phycology 42:1184–1188.

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CANTONATI, M., AND H. LANGE-BERTALOT. 2009. Geissleria gereckei sp. nov. (Bacillariophyta) from leaf-litter covered stones of very shaded carbonate mountain springs with extremely low discharge. Phycological Research 57:171–177. CANTONATI, M., AND H. LANGE-BERTALOT. 2010. Diatom biodiversity of springs in the Berchtesgaden National Park (northern Alps, Germany), with the ecological and morphological characterization of two species new to science. Diatom Research 25:251–280. CANTONATI, M., AND H. LANGE-BERTALOT. 2011. Diatom monitors of close-to-pristine, very-low alkalinity habitats: three new Eunotia species from springs in Nature Parks of the south-eastern Alps. Journal of Limnology 70:209–221. CANTONATI, M., H. LANGE-BERTALOT, AND N. ANGELI. 2010b. Neidiomorpha gen. nov. (Bacillariophyta): a new freshwater diatom genus separated from Neidium Pfitzer. Botanical Studies 51:195–202. CANTONATI, M., H. LANGE-BERTALOT, F. DECET, AND J. GABRIELI. 2011b. Diatoms in very-shallow pools of the site of community importance Danta di Cadore Mires (southeastern Alps), and the potential contribution of these habitats to diatom biodiversity conservation. Nova Hedwigia 93:475–507. CANTONATI, M., H. LANGE-BERTALOT, A. SCALFI, AND N. ANGELI. 2010c. Cymbella tridentina sp. nov. (Bacillariophyta), a crenophilous diatom from carbonate springs of the Alps. Journal of the North American Benthological Society 29:775–788. CANTONATI, M., R. MORESCHINI, E. BERTUZZI, AND P. OSS CAZZADOR. 2007. Detailed spring inventory of two areas of special interest for nature conservation within the Adamello-Brenta Natural Park (south-eastern Alps, Trentino, Italy). Monografie del Museo Tridentino di Scienze Naturali 4:327–334. CANTONATI, M., E. ROTT, AND E. PIPP. 1996. Ecology of cyanophytes in mountain springs of the River Sarca catchment (Adamello-Brenta Regional Park, Trentino, Northern Italy). Algological Studies 83:145–162. CANTONATI, M., E. ROTT, D. SPITALE, N. ANGELI, AND J. KOMA´REK. 2012b. Are benthic algae related to spring types? Freshwater Science 31:481–498. CANTONATI, M., S. SILVIA, N. ANGELI, G. GUELLA, AND R. FRASSANITO. 2009b. Environmental controls of epilithic diatom depth-distribution in an oligotrophic lake characterized by marked water-level fluctuations. European Journal of Phycology 44:15–29. CANTONATI, M., AND D. SPITALE. 2009. The role of environmental variables in structuring epiphytic and epilithic diatom assemblages in springs and streams of the Dolomiti Bellunesi National Park (south-eastern Alps). Fundamental and Applied Limnology – Archiv fu¨r Hydrobiologie 174:117–133. CANTONATI, M., VAN DE VIJVER, AND H. LANGE-BERTALOT. 2009c. Microfissurata gen. nov. (Bacillariophyta), a new diatom genus from dystrophic and intermittently-wet terrestrial habitats. Journal of Phycology 45:732–741.

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