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Review: plant life in extremely acidic waters
Environmental and Experimental Botany 46 (2001) 203– 211 www.elsevier.com/locate/envexpbot
Review: plant life in extremely acidic waters B. Nixdorf a,*, A. Fyson a,b, H. Krumbeck a a
Department of Water Conser6ation, Brandenburg Uni6ersity of Technology Cottbus, Seestrasse 45, D-15526 Bad Saarow, Germany b Leibnitz-Institute of Freshwater Ecology and Inland Fisheries, Mueggelseedamm 310, D-12587 Berlin, Germany
Abstract In acidic waters, a variety of autotrophic organisms are found including phototrophic bacteria, phytoplankton, filamentous- and micro-benthic algae and macrophytes. To explain the occurrence and distribution of primary producers we must answer the following question. What is acidity and where and how does it influence autotrophic metabolism in aquatic ecosystems? The very low pH per se will have profound effects on the survival and growth of organisms and therefore influence biodiversity. On the other hand, we observed a spatial structuring of phototrophic colonization according to the supply of nutrients at interfaces or specific layers. These are interfaces between sediment and water and the chemocline of meromictic lakes or in the case of planktonic development, chlorophyll maxima in the hypolimnion. Therefore, we attempt to analyze the growth conditions for different types of autotrophic organism in relation to resource demands and the distribution of limiting nutrients in sediments and the water column. Adaptations may be morphological (e.g. size, shape, surface area), physiological (e.g. heterotrophic or mixotrophic metabolism, CO2 concentrating mechanisms, low intrinsic growth rates), behavioral (e.g. diurnal migration) or ecological (low grazing pressure, low losses through sedimentation). © 2001 Elsevier Science B.V. All rights reserved. Keywords: Aquatic ecosystems; Acidity; Phytoplankton; Macrophytes; Adaptations; Limitation
1. Introduction Extremely acidic waters (pHB3.5) include volcanic lakes and streams, acidic mine drainage (AMD) and natural iron rich drainages (Geller et al., 1998). A key to an understanding of survival and growth mechanisms of autotrophic organisms in these environments is a knowledge of the chemistry and the distribution of nutrients and energy sources in the water. Soft water lakes, bogs and * Corresponding author. Tel.: + 49-336-31-8943; fax: + 49336-31-5200. E-mail address: [email protected] (B. Nixdorf).
acid rain-affected lakes generally have a pH\3.5, a very different chemistry and ecology and are not considered in this paper. The extremely acidic waters are characterized by distinct chemical and physical properties influencing the survival and growth of organisms in these ecosystems. 1. Fe(III) concentration is high and has profound consequences for water chemistry. The Fe buffered lakes have high concentrations of Ca2 + and SO24 − and Al3 + . 2. Solubility of metal ions is increased at low pH. This is particularly important in mine waters as the source of the AMD often has a high
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heavy metal content. Oxidation and acid generation can result in extremely high dissolved metal concentrations, potentially toxic to organisms. 3. P solubility is high at low pH but P concentrations in these waters are generally extremely low due to coprecipitation with Fe(III) oxyhydroxides. In sediment pore-waters, P concentrations may be high due to release in association with Fe(III) reduction (Kapfer, 1998). 4. Dissolved inorganic carbon (DIC) concentration. At pH 3 and below, essentially all DIC is in the form of dissolved CO2 and saturation concentration is around 10 − 5 M (Stumm and Morgan, 1996). It can be a limiting factor for autotrophic organisms in these environments (Nixdorf et al., 1998; Steinberg et al., 1999). 5. Dissolved inorganic nitrogen (DIN) is usually − predominately in the NH+ 4 -N form but NO3 N is often also found at measurable concentrations. This is attributable to limited nitrification at low pH values. 6. The photon flux density can be high in acidic waters if they are clear. Several precipitation compounds (Fe, Al) may produce turbidity in the water and decrease the underwater light supply for algae (Nixdorf and Hemm, 2000). 7. Light spectrum may be modified by the presence of dissolved Fe(III) which absorbs most light with a wavelength B500 nm. This affects the photons available for the photoreceptors of the various algal and bacterial groups and will effect the ability of phototrophs to survive and compete. This paper reviews the literature on the characteristics of extremely acidic aquatic ecosystems and the mechanisms and strategies which enable algae and macrophytes to grow in these environments.
nutrients and energy sources. Using this model we conclude that the Lusatian acidic environments are nutrient deficient and poor in energy supply with a tendency to a moderate energy budget in the case of photon flux density in clear water lakes and in the pelagic waters of shallow lakes and wetlands. Whitton and Satake (1996) described highly acidic aquatic environments as relatively simple ecosystems where monocultures of phototrophs such as acid-tolerant green flagellates can grow. A characterization of mining waters as resource deficient environments and their place in the ecosystem classification of Reynolds (1997) is shown in Fig. 1.
3. Community structure
3.1. Algae A number of planktonic and benthic taxa which have been consistently reported in the literature to occur in extremely acidic waters include Chlamydomonas sp. (Chlorophyta), Eunotia exigua (Bacillariophyta) and Euglena mutabilis (Euglenophyta; Lackey, 1938; Hargreaves et al., 1975; Whitton and Diaz, 1981; Nixdorf et al., 1998;
2. Mine waters as ecosystems What type of ecosystem are extremely acidic waters in relation to energy and nutrient supply? Reynolds (1997) attempted an ecosystem classification based on the quantity and availability of
Fig. 1. Characterization of mining waters as resource deficient environments and their place in the ecosystem classification after the concept of Reynolds (1997).
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Table 1 Algal colonization of mining lakes in Lusatia (from Nixdorf et al., 2000) and neutral wetlands (from Kadlec and Knight, 1996) Class
Species/taxon in acidic mining lakes
Typical genera in wetlands
Chlorophyceae
Chlamydomonas sp. Scourfieldia cordiformis Ulotrichales Chlorogonium sp. Choricystis sp. Schroederia setigera Stichococcus sp. Ochromonas sp. Chromulina sp. Synura sp. Gymnodinium sp. Peridinium umbonatum Amphidinium elenkinii Lepocinclis o6um Trachelomonas 6ol6ocina E. exigua Eunotia sp. Na6icula sp. Nitzschia sp. Cryptomonas marssonii Cryptomonas erosa Cryptomonas o6ata Normally not found, but see Steinberg et al. (2000)
Chlamydomonas Chlorella Stigeoclonium Oedogonium Spirogyra Hydrodictyon
Chrysophyceae
Dinophyceae
Euglenophyceae Bacillariophyceae
Cryptophyceae
Cyanophyta
Lessmann et al., 2000; Lessmann and Nixdorf, 2001). Chlamydomonas acidophila is commonly found in extreme acidic environments (Rhodes, 1981; Satake and Saijo, 1978; Sheath et al., 1982; Twiss, 1990). The widespread distribution of Chlamydomonas sp. in acidic ponds was documented by Lackey (1938). Dominant classes of phytoplankton in acidic mining lakes in Lusatia (Germany) are Chlorophyceae with the genus Chlorella, Chlamydomonas, Scourfeldia, Chrysophyceae (Ochromonas, Chromulina, Dinobryon), Bacillariophyceae (Eunotia, Fragilaria, Pinnularia), Euglenophyceae (Lepocinclis teres) and Dinophyceae (Peridinium, Gymnodinium) (Nixdorf et al., 1998; Lessmann et al., 2000; Lessmann and Nixdorf, 2001). Filamentous algae belong to Xanthophyceae (Bumilleria klebsiana, Heterococcus sp.) and Chlorophyta (Zygogonium ericetorum, Klebsormidium subtile) and were mainly found in the littoral of lakes (Jacob and Kapfer, 1999).
Ochromonas Chromulina Dinobryon, Mallomonas Gymnodinium Peridinium Euglena, Trichomonas Phacus, Strombomonas Navicula, Fragilaria Pinnularia, Melosira Cyclotella Cryptomonas Rhodomonas, Chilomonas Anabaena, Phormidium, Lyngbia, Microcystis, Oscillatoria
The benthic algal community in mining lakes of Lusatia is characterized by low diversity and occasionally high biomasses of E. mutabilis, E. exigua, Eunotia cf. denticulata, Nitzschia paleaeformis (Kapfer et al., 1999). In meromictic lakes large populations of green sulfur bacteria (Chlorobium limicola) were found (Fyson and Ru¨ cker, 1998). Biodiversity of algae has widely been reported to be reduced with decreasing pH (Blouin, 1989; Whitton and Diaz, 1981; Lessmann et al., 2000; Lessmann and Nixdorf, 2001). A comparison of algal colonization of extremely acidic waters and wetlands is given in Table 1. There are classes present in both environments, e.g. Chlorophyta and Chrysophyta indicating a wide ecological tolerance for these taxa. Colonization by benthic diatoms seems to be very similar in both habitats. Periphyton, which grows attached to emergent and submerged plants in the littoral and in wet-
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lands may be important for the material fluxes in shallow, macrophyte dominated systems. The main difference between the living conditions for algae in the two types of aquatic ecosystem is the limitation of primary production by inorganic carbon and phosphorus in the extremely acidic conditions.
3.2. Macrophytes The most common macrophyte species in the acidic waters of Lusatia are the submerged/floating Juncus bulbosus, and shoreline stands of the emergent Phragmites australis, Typha latifolia and Juncus effusus (Pietsch, 1998). In Table 2 a summary of macrophytes found in extremely acidic waters is given (modified from Fyson, 2000).
4. Algal adaptations Mechanisms of protection against low external pH are essential for survival. In order to survive, all plant cells must maintain near neutral pH in
the cytoplasm. Plants growing in extremely acidic environments must not only exclude H+ to protect metabolic processes but also release H+ in + relation to metabolism of NH+ 4 -N. Excess H − (and OH ) must be sequestered in vacuoles or pumped out (biophysical pH stat) or buffered by organic acids (biochemical pH stat; Smith and Raven, 1979; Raven, 1985a,b). Assimilation of − NO− which may 3 -N generates an excess of OH be released into the medium. On the other hand, use of NH+ 4 -N, the predominant form of nitrogen in most extremely acidic waters, results in an access of H+. This may result in release of H+ into the medium. Such a H+ release is likely a key to survival of aquatic plants in extremely acidic environments. Those species which can grow in such environments where P or DIC are limiting must have special mechanisms for P and C acquisition to support photosynthesis and growth. Mechanisms for survival and growth in extremely acidic waters are considered below for phytoplankton and macrophytes.
Table 2 Angiosperm species occurring in waters with a pH around 3 or below (modified after Fyson, 2000) Minimum pH Submerged species J. bulbosus 2.5–2.6 Sparganium 3.1 emersum Emergent species Carex rostrata 2.1–2.5 Eriophorum 2.6 angustifolium J. bulbosus B3.0 J. effusus 2.1–2.5; 2.8 P. australis Schoenoplectus lacustris Typha angustifolia T. latifolia
Reference
Habitat
Chabbi (1999), Pietsch (1998), Fyson (2000) Sand-Jensen and Rasmussen (1978)
Lusatian mining lakes Danish mine streams
Fyson (2000) Fyson (2000)
Lusatian mining lakes Lusatian mining lakes
B3.0
Pietsch (1998)
Lusatian Lusatian pool Lusatian pool Lusatian
B3.0
Pietsch (1998)
Lusatian mining lakes
B3.0; 2.5; 2.5
Pietsch (1998), Whitton and Diaz (1981), Hargreaves et al. (1975)
Lusatian mining lakes; English mine stream pool; English mine stream pool
2.1-2.5; 2.2
Fyson (2000), Hargreaves et al. (1975) Fyson (2000), Whitton and Diaz (1981)
mining lakes mining lake; English mine stream mining lakes; English mine stream mining lakes
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4.1. Morphological adaptations of phytoplankton The planktonic organisms found in extremely acidic lakes are generally nearly spherical (length to width ratio B 2) with few surface irregularities or appendages which gives them a low surface to volume ratio for a given size. On the other hand, the small size of these flagellates gives them a relatively high surface to volume ratio. Small size is likely related to stress in these environments. Other forms e.g. non-motile Chlorophytes (filamentous or spherical) and diatoms (very few species) are also present.
4.2. Adaptations to high iron concentrations Unlike macrophytes, algae do not possess roots and rhizomes which provide an extensive surface area for the accumulation of Fe(III) oxyhydroxides. Algae must also maintain a near neutral cytoplasmic pH. Therefore, they must have an extremely sharp pH gradient outside the cytoplasm. The location of this gradient has not been established. There is no clear accumulation of Fe(III) oxyhydroxides which would likely kill the cells. Therefore, they must have some mechanism such as secretion of siderophores to maintain Fe in solution or their growth rate must outpace Fe(III) oxyhydroxide precipitation.
4.3. Physiological adaptations 4.3.1. Mixotrophy/heterotrophy Algal biomass production is not clearly related to pH or acidity in the Lusatian mining lakes (Nixdorf et al., 1998). Algae developing at very low pH may be able to grow heterotrophically (Chlamydomonas sp., E. exigua) or mixotrophically (Ochromonas sp., Dinophyta) giving these taxa an advantage where DIC, nutrient supplies or light concentrations are low. Various chrysophytes and many Ochromonas sp. are known to exhibit mixotrophy (Andersson et al., 1989; Jones, 1994) which can provide additional carbon for algae in waters where DIC is growth limiting. Such potentially mixotrophic algae are common in the acidic mining lakes. Mixotrophy (Laliberte´ and de la Nou¨ e, 1993), and the ability to migrate
Fig. 2. Nutrient concentrations of total phosphorus and total inorganic carbon, chlorophyll concentration and carrying capacity for carbon and nitrogen using a C, Chl a-relation of 1:50 (after Reynolds, 1997) in the Lusatian acidic mining lake Gru¨ newalde (pH 3) in May 2000.
to deep waters and build chlorophyll maxima (Arvola et al., 1992) is known for some Chlamydomonas sp., another genus abundant in the acidic mining lakes. The role of bacterivorous algae in these lakes has not been established although bacteria have been observed within fixed Ochromonas cells.
4.3.2. Low resource demands Concerning the acidic waters as nutrient and partly energy deficient environments (Fig. 1) one looks for strategists among the autotrophs with low light and low phosphorus and inorganic carbon demands. Many chrysophytes are low-phosphorus and low-light strategists, which enables them to grow in the Lusatian lakes. In Fig. 2, the depth profiles of the planktonic chlorophyll concentration and the carrying capacity of the acidic mining Lake Gru¨ newalde (Lake Plessa 117, pH about 3) is shown for May 2000, a period when the water column was stratified and a clear deep chlorophyll maximum had been established. In
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relation to phosphorus and carbon resources it may be noted that the minimum chlorophyll concentrations were found in the epilimnion where carbon limits the production more than phosphorus and carrying capacity is not reached despite the high underwater light supply. On the other hand, the high chlorophyll concentration below the thermocline indicates a better nutrient supply for the phytoplankton, which reached or even exceeded the carrying capacity for phosphorus and carbon. At least three assumptions for the explanation of these phenomena are possible. First, phytoplankton in deeper water layers with lower photon flux density have higher specific chlorophyll contents. This implies that the internal cell ratio of carbon to chlorophyll which is generally taken to be 1:50 (Reynolds, 1997) is increasing under the described conditions. Second, a decoupling of temporal and spatial resource availability and assimilation by phytoplankton may occur. Then, the measured chlorophyll concentration is a result of an intense carbon assimilation process leading to a decrease in the concentration of inorganic carbon from a level which was sufficient for a phytoplanktonic biomass accumulation at the measured level. A third explanation is employment of mixotrophy or heterotrophy by the algae. In this case, organic carbon sources may contribute to synthesis of chlorophyll and other metabolic processes where inorganic carbon concentrations are low.
4.3.3. Increase in enzyme acti6ity (phosphatase) A further metabolic advantage is the ability of the organisms to produce phosphatases which is an apparent adaptation to the poor nutrient situation in these lakes. The induction of phosphatase activity in acidic waters by aluminium was described by Jannson (1981) and enhanced phosphatase activity of C. acidophila in phosphate deficient environments with an optimum at pH 2 by Boavida and Heath (1986). 4.4. Motility of flagellates The planktonic algal community of the Lusatian acidic lakes is generally dominated by small flagellates (belonging to Chlorophyceae, Chryso-
phyceae, Cryptophyceae, Dinophyceae and Euglenophyceae). Their motility enables them to migrate to layers of the lakes where carbon and nutrient sources in the form of dissolved substrates or particles (e.g. bacteria) are available. The ability of migration in deep layers to build chlorophyll maxima (Arvola et al., 1992) is known for some Chlamydomonas sp. and has often been observed in acidic lakes in Lusatia where increased carbon concentrations in hypolimnion were found followed or accompanied by chlorophyll maxima (Nixdorf et al., 1998; Nixdorf and Kapfer, 1998, see Fig. 3). The small cell dimensions of phytoplankton in acidic waters protect them for losses by sedimentation and sinking according to the Stokes equation. Losses by grazing due to herbivorous zooplankton are low because of the unfavorable conditions for the development of consumers in extremely acidic waters (Wollmann et al., 2000; Deneke, 2000).
5. Physiological and biochemical adaptations in macrophytes J. bulbosus L. is the only submerged angiosperm known to grow in waters with a pH of 3 and below (Sand-Jensen and Rasmussen, 1978; Pietsch, 1998) and is often abundant in the extremely acidic Lusatian mine lakes and streams. This species may also exhibit extensive growth following liming of acid rain affected lakes (Roelofs et al., 1984, 1994). The ability of J. bulbosus to take up CO2 both through roots and shoots may give it a competitive advantage in low pH environments where essentially all DIC is in the form of CO2 (Sveda¨ ng, 1992). In the extremely acidic aquatic ecosystems of Lusatia, the high DIC (CO2) concentration in sediment pore-waters (Lessmann et al., 1999) is likely a key to the success of this species. Species relying on uptake of HCO3 will likely not grow in these acidic environments because of the absence of this form of DIC. Emergent species can take CO2 directly from the atmosphere and therefore have no CO2 supply problem. In extremely acidic mining lakes, phosphate concentrations are typically extremely low due to
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coprecipitation of P with Fe(OH)3. This will likely limit growth of macrophytes. Phosphorus and DIC concentrations may be much higher in sediment pore-water here due to release of P coprecipitated with Fe(III) oxyhydroxides and to decomposition of organic materials in anoxic conditions. The presence of iron-rich coatings (plaques) on root surfaces of aquatic macrophytes like Typha and other species growing in metal-rich, acidic environments may reduce the entry of iron and other heavy metals into the plant (Taylor and Crowder, 1983; Taylor et al., 1984; Crowder and St.-Cyr, 1991). Iron plaques on J. bulbosus from the acidic mining lakes of Lusatia have been described by Chabbi (1999) who determined that iron accumulates in roots as far as the outer surface of the endodermis. J. bulbosus and other aquatic angiosperms has an extensive aerenchyma which carries oxygen to the roots (Chabbi, 1999). The release of O2 from roots is probably essential for survival of plants rooted into anoxic sediments and also provides local oxidizing conditions for iron plaque formation. Fluctuation in environmental conditions is an important factor influencing the colonization and survival of both algae and macrophytes and algae in extremely acidic waters. Where waters are impacted by industrial or mining activities, there are often substantial changes in water level and flow rate as well as water chemistry, which are independent of weather or seasonal factors. An example is the rising water level of the Lusatian mining lakes.
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ecosystems, ranging from wetlands and streams to lakes (small meromictic as well as large and deep). Dominant classes of extremely acidic mining waters (pHB 3.5) are Chlorophyceae, Chrysophyceae, Bacillariophyceae, Euglenophyceae and Dinophyceae (Lackey, 1938; Hargreaves et al., 1975; Whitton and Diaz, 1981; Nixdorf et al., 1998; Jacob and Kapfer, 1999; Lessmann and Nixdorf, 2001). The diversity of macrophytes in extremely acidic waters is generally low (Hargreaves et al., 1975; Whitton and Diaz, 1981; Pietsch, 1998; Fyson, 2000). In Lusatia, the submerged/floating J. bulbosus and the emergent P. australis and Typha sp. are typically dominant species (Pietsch, 1998; Fyson, 2000). Wetlands have been extensively planted, particularly in North America, for the treatment of AMD (Kadlec and Knight, 1996). However, knowledge on the mechanisms for survival and growth in these acidic aquatic ecosystems is extremely limited. In the case of algae, the roles of cell size and shape, motility, mixotrophy and heterotrophy, and changes is metabolism (production of phosphatase, increase in carbon use efficiency have been mooted but require further study. Laboratory algal culture studies are needed to characterize these mechanisms. As far as macrophytes are concerned, studies on adaptations of J. bulbosus should be extended to other species. In particular, the role of sediment chemistry in growth of these plants in extremely acidic aquatic ecosystems needs to be addressed. Acknowledgements
6. Conclusions The flooded, open cast lignite pits of Lusatia (Germany) are impacted by the oxidation of iron sulphides (e.g. pyrite and marcasite) and thus, are extremely acidic, with a pH 1.9– 3.5 and high Fe and sulfate concentrations. These conditions result in chemical and trophic environments for phototrophic organisms characterized by ionic stress and nutrient limitations. Nevertheless, these extreme living conditions support a wide variety of photoautotrophs in diverse acidic aquatic
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Taylor, G.J., Crowder, A.A., 1983. Use of the DCB technique for extraction of hydrous iron oxides from roots of wetland plants. Am. J. Bot. 70, 1254 – 1257. Taylor, G.J., Crowder, A.A., Rodden, R., 1984. Formation and morphology of an iron plaque on the roots of Typha latifolia L. grown in solution culture. Am. J. Bot. 71, 666 – 675. Twiss, M.R., 1990. Copper tolerance of Chlamydomonas acidophila (Chlorophyceae) isolated from acidic, coppercontaminated soils. J. Phycol. 26, 655 – 659. Whitton, B.A., Diaz, B.M., 1981. Influence of environmental factors on photosynthetic species composition in highly acidic waters. Verh. Int. Verein. Limnol. 21, 1459 – 1465. Whitton, B.A., Satake, K., 1996. Phototrophs in highly acidic waters: an overview. In: Proceedings of the International Symposium on Acidic Deposition and Its Impacts. Tsukuba, Japan, pp. 204 – 211. Wollmann, K., Deneke, R., Nixdorf, B., Packroff, G., 2000. The dynamics of planktonic food webs in 3 mining lakes across a pH gradient (pH 2 – 4). Hydrobiology 433, 3 –14.
Review: plant life in extremely acidic waters B. Nixdorf a,*, A. Fyson a,b, H. Krumbeck a a
Department of Water Conser6ation, Brandenburg Uni6ersity of Technology Cottbus, Seestrasse 45, D-15526 Bad Saarow, Germany b Leibnitz-Institute of Freshwater Ecology and Inland Fisheries, Mueggelseedamm 310, D-12587 Berlin, Germany
Abstract In acidic waters, a variety of autotrophic organisms are found including phototrophic bacteria, phytoplankton, filamentous- and micro-benthic algae and macrophytes. To explain the occurrence and distribution of primary producers we must answer the following question. What is acidity and where and how does it influence autotrophic metabolism in aquatic ecosystems? The very low pH per se will have profound effects on the survival and growth of organisms and therefore influence biodiversity. On the other hand, we observed a spatial structuring of phototrophic colonization according to the supply of nutrients at interfaces or specific layers. These are interfaces between sediment and water and the chemocline of meromictic lakes or in the case of planktonic development, chlorophyll maxima in the hypolimnion. Therefore, we attempt to analyze the growth conditions for different types of autotrophic organism in relation to resource demands and the distribution of limiting nutrients in sediments and the water column. Adaptations may be morphological (e.g. size, shape, surface area), physiological (e.g. heterotrophic or mixotrophic metabolism, CO2 concentrating mechanisms, low intrinsic growth rates), behavioral (e.g. diurnal migration) or ecological (low grazing pressure, low losses through sedimentation). © 2001 Elsevier Science B.V. All rights reserved. Keywords: Aquatic ecosystems; Acidity; Phytoplankton; Macrophytes; Adaptations; Limitation
1. Introduction Extremely acidic waters (pHB3.5) include volcanic lakes and streams, acidic mine drainage (AMD) and natural iron rich drainages (Geller et al., 1998). A key to an understanding of survival and growth mechanisms of autotrophic organisms in these environments is a knowledge of the chemistry and the distribution of nutrients and energy sources in the water. Soft water lakes, bogs and * Corresponding author. Tel.: + 49-336-31-8943; fax: + 49336-31-5200. E-mail address: [email protected] (B. Nixdorf).
acid rain-affected lakes generally have a pH\3.5, a very different chemistry and ecology and are not considered in this paper. The extremely acidic waters are characterized by distinct chemical and physical properties influencing the survival and growth of organisms in these ecosystems. 1. Fe(III) concentration is high and has profound consequences for water chemistry. The Fe buffered lakes have high concentrations of Ca2 + and SO24 − and Al3 + . 2. Solubility of metal ions is increased at low pH. This is particularly important in mine waters as the source of the AMD often has a high
S0098-8472/01/$ - see front matter © 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 9 8 - 8 4 7 2 ( 0 1 ) 0 0 1 0 4 - 6
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heavy metal content. Oxidation and acid generation can result in extremely high dissolved metal concentrations, potentially toxic to organisms. 3. P solubility is high at low pH but P concentrations in these waters are generally extremely low due to coprecipitation with Fe(III) oxyhydroxides. In sediment pore-waters, P concentrations may be high due to release in association with Fe(III) reduction (Kapfer, 1998). 4. Dissolved inorganic carbon (DIC) concentration. At pH 3 and below, essentially all DIC is in the form of dissolved CO2 and saturation concentration is around 10 − 5 M (Stumm and Morgan, 1996). It can be a limiting factor for autotrophic organisms in these environments (Nixdorf et al., 1998; Steinberg et al., 1999). 5. Dissolved inorganic nitrogen (DIN) is usually − predominately in the NH+ 4 -N form but NO3 N is often also found at measurable concentrations. This is attributable to limited nitrification at low pH values. 6. The photon flux density can be high in acidic waters if they are clear. Several precipitation compounds (Fe, Al) may produce turbidity in the water and decrease the underwater light supply for algae (Nixdorf and Hemm, 2000). 7. Light spectrum may be modified by the presence of dissolved Fe(III) which absorbs most light with a wavelength B500 nm. This affects the photons available for the photoreceptors of the various algal and bacterial groups and will effect the ability of phototrophs to survive and compete. This paper reviews the literature on the characteristics of extremely acidic aquatic ecosystems and the mechanisms and strategies which enable algae and macrophytes to grow in these environments.
nutrients and energy sources. Using this model we conclude that the Lusatian acidic environments are nutrient deficient and poor in energy supply with a tendency to a moderate energy budget in the case of photon flux density in clear water lakes and in the pelagic waters of shallow lakes and wetlands. Whitton and Satake (1996) described highly acidic aquatic environments as relatively simple ecosystems where monocultures of phototrophs such as acid-tolerant green flagellates can grow. A characterization of mining waters as resource deficient environments and their place in the ecosystem classification of Reynolds (1997) is shown in Fig. 1.
3. Community structure
3.1. Algae A number of planktonic and benthic taxa which have been consistently reported in the literature to occur in extremely acidic waters include Chlamydomonas sp. (Chlorophyta), Eunotia exigua (Bacillariophyta) and Euglena mutabilis (Euglenophyta; Lackey, 1938; Hargreaves et al., 1975; Whitton and Diaz, 1981; Nixdorf et al., 1998;
2. Mine waters as ecosystems What type of ecosystem are extremely acidic waters in relation to energy and nutrient supply? Reynolds (1997) attempted an ecosystem classification based on the quantity and availability of
Fig. 1. Characterization of mining waters as resource deficient environments and their place in the ecosystem classification after the concept of Reynolds (1997).
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Table 1 Algal colonization of mining lakes in Lusatia (from Nixdorf et al., 2000) and neutral wetlands (from Kadlec and Knight, 1996) Class
Species/taxon in acidic mining lakes
Typical genera in wetlands
Chlorophyceae
Chlamydomonas sp. Scourfieldia cordiformis Ulotrichales Chlorogonium sp. Choricystis sp. Schroederia setigera Stichococcus sp. Ochromonas sp. Chromulina sp. Synura sp. Gymnodinium sp. Peridinium umbonatum Amphidinium elenkinii Lepocinclis o6um Trachelomonas 6ol6ocina E. exigua Eunotia sp. Na6icula sp. Nitzschia sp. Cryptomonas marssonii Cryptomonas erosa Cryptomonas o6ata Normally not found, but see Steinberg et al. (2000)
Chlamydomonas Chlorella Stigeoclonium Oedogonium Spirogyra Hydrodictyon
Chrysophyceae
Dinophyceae
Euglenophyceae Bacillariophyceae
Cryptophyceae
Cyanophyta
Lessmann et al., 2000; Lessmann and Nixdorf, 2001). Chlamydomonas acidophila is commonly found in extreme acidic environments (Rhodes, 1981; Satake and Saijo, 1978; Sheath et al., 1982; Twiss, 1990). The widespread distribution of Chlamydomonas sp. in acidic ponds was documented by Lackey (1938). Dominant classes of phytoplankton in acidic mining lakes in Lusatia (Germany) are Chlorophyceae with the genus Chlorella, Chlamydomonas, Scourfeldia, Chrysophyceae (Ochromonas, Chromulina, Dinobryon), Bacillariophyceae (Eunotia, Fragilaria, Pinnularia), Euglenophyceae (Lepocinclis teres) and Dinophyceae (Peridinium, Gymnodinium) (Nixdorf et al., 1998; Lessmann et al., 2000; Lessmann and Nixdorf, 2001). Filamentous algae belong to Xanthophyceae (Bumilleria klebsiana, Heterococcus sp.) and Chlorophyta (Zygogonium ericetorum, Klebsormidium subtile) and were mainly found in the littoral of lakes (Jacob and Kapfer, 1999).
Ochromonas Chromulina Dinobryon, Mallomonas Gymnodinium Peridinium Euglena, Trichomonas Phacus, Strombomonas Navicula, Fragilaria Pinnularia, Melosira Cyclotella Cryptomonas Rhodomonas, Chilomonas Anabaena, Phormidium, Lyngbia, Microcystis, Oscillatoria
The benthic algal community in mining lakes of Lusatia is characterized by low diversity and occasionally high biomasses of E. mutabilis, E. exigua, Eunotia cf. denticulata, Nitzschia paleaeformis (Kapfer et al., 1999). In meromictic lakes large populations of green sulfur bacteria (Chlorobium limicola) were found (Fyson and Ru¨ cker, 1998). Biodiversity of algae has widely been reported to be reduced with decreasing pH (Blouin, 1989; Whitton and Diaz, 1981; Lessmann et al., 2000; Lessmann and Nixdorf, 2001). A comparison of algal colonization of extremely acidic waters and wetlands is given in Table 1. There are classes present in both environments, e.g. Chlorophyta and Chrysophyta indicating a wide ecological tolerance for these taxa. Colonization by benthic diatoms seems to be very similar in both habitats. Periphyton, which grows attached to emergent and submerged plants in the littoral and in wet-
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lands may be important for the material fluxes in shallow, macrophyte dominated systems. The main difference between the living conditions for algae in the two types of aquatic ecosystem is the limitation of primary production by inorganic carbon and phosphorus in the extremely acidic conditions.
3.2. Macrophytes The most common macrophyte species in the acidic waters of Lusatia are the submerged/floating Juncus bulbosus, and shoreline stands of the emergent Phragmites australis, Typha latifolia and Juncus effusus (Pietsch, 1998). In Table 2 a summary of macrophytes found in extremely acidic waters is given (modified from Fyson, 2000).
4. Algal adaptations Mechanisms of protection against low external pH are essential for survival. In order to survive, all plant cells must maintain near neutral pH in
the cytoplasm. Plants growing in extremely acidic environments must not only exclude H+ to protect metabolic processes but also release H+ in + relation to metabolism of NH+ 4 -N. Excess H − (and OH ) must be sequestered in vacuoles or pumped out (biophysical pH stat) or buffered by organic acids (biochemical pH stat; Smith and Raven, 1979; Raven, 1985a,b). Assimilation of − NO− which may 3 -N generates an excess of OH be released into the medium. On the other hand, use of NH+ 4 -N, the predominant form of nitrogen in most extremely acidic waters, results in an access of H+. This may result in release of H+ into the medium. Such a H+ release is likely a key to survival of aquatic plants in extremely acidic environments. Those species which can grow in such environments where P or DIC are limiting must have special mechanisms for P and C acquisition to support photosynthesis and growth. Mechanisms for survival and growth in extremely acidic waters are considered below for phytoplankton and macrophytes.
Table 2 Angiosperm species occurring in waters with a pH around 3 or below (modified after Fyson, 2000) Minimum pH Submerged species J. bulbosus 2.5–2.6 Sparganium 3.1 emersum Emergent species Carex rostrata 2.1–2.5 Eriophorum 2.6 angustifolium J. bulbosus B3.0 J. effusus 2.1–2.5; 2.8 P. australis Schoenoplectus lacustris Typha angustifolia T. latifolia
Reference
Habitat
Chabbi (1999), Pietsch (1998), Fyson (2000) Sand-Jensen and Rasmussen (1978)
Lusatian mining lakes Danish mine streams
Fyson (2000) Fyson (2000)
Lusatian mining lakes Lusatian mining lakes
B3.0
Pietsch (1998)
Lusatian Lusatian pool Lusatian pool Lusatian
B3.0
Pietsch (1998)
Lusatian mining lakes
B3.0; 2.5; 2.5
Pietsch (1998), Whitton and Diaz (1981), Hargreaves et al. (1975)
Lusatian mining lakes; English mine stream pool; English mine stream pool
2.1-2.5; 2.2
Fyson (2000), Hargreaves et al. (1975) Fyson (2000), Whitton and Diaz (1981)
mining lakes mining lake; English mine stream mining lakes; English mine stream mining lakes
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4.1. Morphological adaptations of phytoplankton The planktonic organisms found in extremely acidic lakes are generally nearly spherical (length to width ratio B 2) with few surface irregularities or appendages which gives them a low surface to volume ratio for a given size. On the other hand, the small size of these flagellates gives them a relatively high surface to volume ratio. Small size is likely related to stress in these environments. Other forms e.g. non-motile Chlorophytes (filamentous or spherical) and diatoms (very few species) are also present.
4.2. Adaptations to high iron concentrations Unlike macrophytes, algae do not possess roots and rhizomes which provide an extensive surface area for the accumulation of Fe(III) oxyhydroxides. Algae must also maintain a near neutral cytoplasmic pH. Therefore, they must have an extremely sharp pH gradient outside the cytoplasm. The location of this gradient has not been established. There is no clear accumulation of Fe(III) oxyhydroxides which would likely kill the cells. Therefore, they must have some mechanism such as secretion of siderophores to maintain Fe in solution or their growth rate must outpace Fe(III) oxyhydroxide precipitation.
4.3. Physiological adaptations 4.3.1. Mixotrophy/heterotrophy Algal biomass production is not clearly related to pH or acidity in the Lusatian mining lakes (Nixdorf et al., 1998). Algae developing at very low pH may be able to grow heterotrophically (Chlamydomonas sp., E. exigua) or mixotrophically (Ochromonas sp., Dinophyta) giving these taxa an advantage where DIC, nutrient supplies or light concentrations are low. Various chrysophytes and many Ochromonas sp. are known to exhibit mixotrophy (Andersson et al., 1989; Jones, 1994) which can provide additional carbon for algae in waters where DIC is growth limiting. Such potentially mixotrophic algae are common in the acidic mining lakes. Mixotrophy (Laliberte´ and de la Nou¨ e, 1993), and the ability to migrate
Fig. 2. Nutrient concentrations of total phosphorus and total inorganic carbon, chlorophyll concentration and carrying capacity for carbon and nitrogen using a C, Chl a-relation of 1:50 (after Reynolds, 1997) in the Lusatian acidic mining lake Gru¨ newalde (pH 3) in May 2000.
to deep waters and build chlorophyll maxima (Arvola et al., 1992) is known for some Chlamydomonas sp., another genus abundant in the acidic mining lakes. The role of bacterivorous algae in these lakes has not been established although bacteria have been observed within fixed Ochromonas cells.
4.3.2. Low resource demands Concerning the acidic waters as nutrient and partly energy deficient environments (Fig. 1) one looks for strategists among the autotrophs with low light and low phosphorus and inorganic carbon demands. Many chrysophytes are low-phosphorus and low-light strategists, which enables them to grow in the Lusatian lakes. In Fig. 2, the depth profiles of the planktonic chlorophyll concentration and the carrying capacity of the acidic mining Lake Gru¨ newalde (Lake Plessa 117, pH about 3) is shown for May 2000, a period when the water column was stratified and a clear deep chlorophyll maximum had been established. In
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relation to phosphorus and carbon resources it may be noted that the minimum chlorophyll concentrations were found in the epilimnion where carbon limits the production more than phosphorus and carrying capacity is not reached despite the high underwater light supply. On the other hand, the high chlorophyll concentration below the thermocline indicates a better nutrient supply for the phytoplankton, which reached or even exceeded the carrying capacity for phosphorus and carbon. At least three assumptions for the explanation of these phenomena are possible. First, phytoplankton in deeper water layers with lower photon flux density have higher specific chlorophyll contents. This implies that the internal cell ratio of carbon to chlorophyll which is generally taken to be 1:50 (Reynolds, 1997) is increasing under the described conditions. Second, a decoupling of temporal and spatial resource availability and assimilation by phytoplankton may occur. Then, the measured chlorophyll concentration is a result of an intense carbon assimilation process leading to a decrease in the concentration of inorganic carbon from a level which was sufficient for a phytoplanktonic biomass accumulation at the measured level. A third explanation is employment of mixotrophy or heterotrophy by the algae. In this case, organic carbon sources may contribute to synthesis of chlorophyll and other metabolic processes where inorganic carbon concentrations are low.
4.3.3. Increase in enzyme acti6ity (phosphatase) A further metabolic advantage is the ability of the organisms to produce phosphatases which is an apparent adaptation to the poor nutrient situation in these lakes. The induction of phosphatase activity in acidic waters by aluminium was described by Jannson (1981) and enhanced phosphatase activity of C. acidophila in phosphate deficient environments with an optimum at pH 2 by Boavida and Heath (1986). 4.4. Motility of flagellates The planktonic algal community of the Lusatian acidic lakes is generally dominated by small flagellates (belonging to Chlorophyceae, Chryso-
phyceae, Cryptophyceae, Dinophyceae and Euglenophyceae). Their motility enables them to migrate to layers of the lakes where carbon and nutrient sources in the form of dissolved substrates or particles (e.g. bacteria) are available. The ability of migration in deep layers to build chlorophyll maxima (Arvola et al., 1992) is known for some Chlamydomonas sp. and has often been observed in acidic lakes in Lusatia where increased carbon concentrations in hypolimnion were found followed or accompanied by chlorophyll maxima (Nixdorf et al., 1998; Nixdorf and Kapfer, 1998, see Fig. 3). The small cell dimensions of phytoplankton in acidic waters protect them for losses by sedimentation and sinking according to the Stokes equation. Losses by grazing due to herbivorous zooplankton are low because of the unfavorable conditions for the development of consumers in extremely acidic waters (Wollmann et al., 2000; Deneke, 2000).
5. Physiological and biochemical adaptations in macrophytes J. bulbosus L. is the only submerged angiosperm known to grow in waters with a pH of 3 and below (Sand-Jensen and Rasmussen, 1978; Pietsch, 1998) and is often abundant in the extremely acidic Lusatian mine lakes and streams. This species may also exhibit extensive growth following liming of acid rain affected lakes (Roelofs et al., 1984, 1994). The ability of J. bulbosus to take up CO2 both through roots and shoots may give it a competitive advantage in low pH environments where essentially all DIC is in the form of CO2 (Sveda¨ ng, 1992). In the extremely acidic aquatic ecosystems of Lusatia, the high DIC (CO2) concentration in sediment pore-waters (Lessmann et al., 1999) is likely a key to the success of this species. Species relying on uptake of HCO3 will likely not grow in these acidic environments because of the absence of this form of DIC. Emergent species can take CO2 directly from the atmosphere and therefore have no CO2 supply problem. In extremely acidic mining lakes, phosphate concentrations are typically extremely low due to
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coprecipitation of P with Fe(OH)3. This will likely limit growth of macrophytes. Phosphorus and DIC concentrations may be much higher in sediment pore-water here due to release of P coprecipitated with Fe(III) oxyhydroxides and to decomposition of organic materials in anoxic conditions. The presence of iron-rich coatings (plaques) on root surfaces of aquatic macrophytes like Typha and other species growing in metal-rich, acidic environments may reduce the entry of iron and other heavy metals into the plant (Taylor and Crowder, 1983; Taylor et al., 1984; Crowder and St.-Cyr, 1991). Iron plaques on J. bulbosus from the acidic mining lakes of Lusatia have been described by Chabbi (1999) who determined that iron accumulates in roots as far as the outer surface of the endodermis. J. bulbosus and other aquatic angiosperms has an extensive aerenchyma which carries oxygen to the roots (Chabbi, 1999). The release of O2 from roots is probably essential for survival of plants rooted into anoxic sediments and also provides local oxidizing conditions for iron plaque formation. Fluctuation in environmental conditions is an important factor influencing the colonization and survival of both algae and macrophytes and algae in extremely acidic waters. Where waters are impacted by industrial or mining activities, there are often substantial changes in water level and flow rate as well as water chemistry, which are independent of weather or seasonal factors. An example is the rising water level of the Lusatian mining lakes.
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ecosystems, ranging from wetlands and streams to lakes (small meromictic as well as large and deep). Dominant classes of extremely acidic mining waters (pHB 3.5) are Chlorophyceae, Chrysophyceae, Bacillariophyceae, Euglenophyceae and Dinophyceae (Lackey, 1938; Hargreaves et al., 1975; Whitton and Diaz, 1981; Nixdorf et al., 1998; Jacob and Kapfer, 1999; Lessmann and Nixdorf, 2001). The diversity of macrophytes in extremely acidic waters is generally low (Hargreaves et al., 1975; Whitton and Diaz, 1981; Pietsch, 1998; Fyson, 2000). In Lusatia, the submerged/floating J. bulbosus and the emergent P. australis and Typha sp. are typically dominant species (Pietsch, 1998; Fyson, 2000). Wetlands have been extensively planted, particularly in North America, for the treatment of AMD (Kadlec and Knight, 1996). However, knowledge on the mechanisms for survival and growth in these acidic aquatic ecosystems is extremely limited. In the case of algae, the roles of cell size and shape, motility, mixotrophy and heterotrophy, and changes is metabolism (production of phosphatase, increase in carbon use efficiency have been mooted but require further study. Laboratory algal culture studies are needed to characterize these mechanisms. As far as macrophytes are concerned, studies on adaptations of J. bulbosus should be extended to other species. In particular, the role of sediment chemistry in growth of these plants in extremely acidic aquatic ecosystems needs to be addressed. Acknowledgements
6. Conclusions The flooded, open cast lignite pits of Lusatia (Germany) are impacted by the oxidation of iron sulphides (e.g. pyrite and marcasite) and thus, are extremely acidic, with a pH 1.9– 3.5 and high Fe and sulfate concentrations. These conditions result in chemical and trophic environments for phototrophic organisms characterized by ionic stress and nutrient limitations. Nevertheless, these extreme living conditions support a wide variety of photoautotrophs in diverse acidic aquatic
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