Hydrobiologia 433: 153156, 2000.

B.A. Whitton, P. Albertano & K. Satake (eds), Chemistry and Ecology of Highly Acidic Environments.
2000 Kluwer Academic Publishers. Printed in the Netherlands.

153

A review on the occurrence and taxonomy of heterotrophic protists

in extreme acidic environments of pH values 3
Gabriele Packroff1 & Stefan Woelfl2
1 UFZ

Centre for Environmental Research Leipzig-Halle, Department of Inland Water Research

Magdeburg, Brueckstrasse 3a, D-39114 Magdeburg, Germany
2 Instituto de Zoologa, Universidad Austral de Chile, Casilla 567, Valdivia, Chile
Key words: acid, taxonomy, protists, ciliate, flagellate

Abstract
The occurrence and some important taxonomic problems of heterotrophic protists from extremely acidic (pH
3) environments are briefly discussed. Almost all information on the occurrence of heterotrophic protists from
extremely acidic environments is restricted to acid mine drainage (AMD) or streams influenced by AMD. Most
of the information is provided for ciliates. Very little information is available on the occurrence of flagellates,
rhizopods and heliozoa in this environment. Within the ciliates Urotricha, Vorticella and Oxytricha dominate
in acidic mining lakes. Actinophrys sp. is the most important heliozoan in these environments. There are many
taxonomic problems which are not solved so far. Live observations and taxonomic methods adapted to the extreme
chemical matrix are necessary for correct identification.

Introduction
Heterotrophic protists can play a important role in extremely acid environments with pH values at or below
3 (Lackey, 1938; Woelfl et al., 1998; Packroff, 1998).
Nevertheless, up to now little information on the occurrence of this group has been available and what
there is mostly comes from acid mine drainage (AMD)
or streams affected by AMD. The lack of information about heterotrophic protists in acid environments
partly reflects the lack of studies, but also results from
the many taxonomic problems. This paper aims to
make it easier to make reliable identifications in future
studies of heterotrophic protists in environments with
pH values 3 by summarizing present knowledge on
their occurrence and taxonomic problems.

combination of observations from living and prepared

cells yields sufficient information for a reliable identification of ciliate species. The following silver stains
are needed for the determination of ciliates: Protargol
methods, wet silver nitrate method and dry silver nitrate method. Detailed descriptions of the methods can
be found in Foissner (1993). The classification of oxytrichids, which are quantitatively important in acidic
(mining) lakes, was in a preliminary and provisional
state until recently (Berger & Foissner, 1997), but has
recently been revised (Berger, 1999). Most species are
difficult to identify, differing only in morphometric
or inconspicuous features. In some cases, information about morphogenesis is needed, which implies
culturing of the organisms. Heliozoans are only determinable as living organisms, although for some
groups of heliozoa scanning electron microscopy is
also helpful (Page & Siemensma, 1991).

Results and discussion

References to literature with taxonomic keys
Taxonomy and problems related to identification
Most of the identification of ciliates in acidic environments is based on live observations only, which is why
the probability of false identification is high. Only the

At the moment, there is no modern identification key

for most of the heterotrophic protozoans. The last
comprehensive review and key to ciliates from Kahl
(19301935) is not very detailed and long outdated.

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Table 1. Summary of literature dealing with protozoa at pH 3
Literature

Group

Species

pH

Study site

Naturally acidic systems

Vallin 1953
Ciliophora

ciliates

2.83.1

Lake Blamisusjoen,
coastal sulphur lake
(Sweden)

Woelfl (pers. comm.)

amoeba cf. Vampyrella

1.1

Rio Agrio: crater

lake outflow
(Argentina)

parasitic amoeba on
bryophyte protonema

2.8

acidic stream
entering Lake
Usoriko
(Japan)
(Satake, this volume)

1.83.0
1.83.0
1.83.0
3.0
2.23.0
1.82.9
3.0
2.6
1.8
3.0
2.6
1.83.0
1.8.2.6
1.8.2.6
2.23.0
3.0

AMD, mostly
streams (U.S.A.)

Sarcodina

Whitton & Satake (pers. Sarcodina

comm.)

Acid mine drainage (AMD) or streams influenced by AMD

Lackey (1938, 1939)
Mastigophora Bodo sp.
Monas sp.
unidentified flagellates
Sarcodina
Actinophrys sol
Vahlkampfia limax
Hartmanella hyalina
Cochliopodium bilimbosum
Acanthocystis aculeata
unidentified rhizopoda
Nuclearia simplex
Amphisia sp.
Ciliophora
Oxytricha sp.
Urotricha sp.
Cyclidium sp.
Drepanomonas sp.
Prorodon sp
Joseph (1953)

Mastigophora Euglena spp.

Sarcodina
Amoeba proteus
Ciliophora
Paramecium caudatum

2.0 4.0 AMD, streams

(U.S.A.)

Ehrlich (1963)

Mastigophora flagellate cf. Eutrepia

2.5

AMD samples from

copper mine,
enrichment culture
(U.S.A.)
Stored AMD
samples from copper mine
(U.S.A.)

1.84

Culture from AMD

streamers
(U.K.)

Sarcodina

McGinness & Johnson

(1992)

Amoeba spp.

Mastigophora Eutreptia spp.

Continued on p. 155

155
Table 1. contd.
Literature

Group

Johnson (1998)

Mastigophora Eutreptia spp.

Sarcodina
Vahlkampfia sp.
Ciliophora
Cinetochilum sp.

Acidic strip mining lakes

McConathy &Stahl
(1982)

Species

pH

Study site

2.3

AMD, streamers,
cultures (U.K.)

Sarcodina
Ciliophora

Actinophrys sp.
3.0
Strip mining lake
Chilodonella caudata 2.503.00 (U.S.A.)
Oxytricha sp.
Euplotes sp.
Uroleptus sp.

Woelfl et al. (1998)

Packroff (1998)
Packroff (this volume)

Sarcodina
Ciliophora

Actinophrys cf. sol

Urotricha armata
Frontonia sp.
Oxytricha sp.
(Oxytrichidae)
Peritrichida div. sp.

2.33.0

Strip mining lakes

(Germany)

Packroff (unpub.)

Ciliophora

Chilodonellidae
Hypotrichs

2.32.6

artificial substrates
in strip mining lake
(Germany)

3.0

Model ecosystems

Others (model ecosystems)

Bick & Drews (1973)
Ciliophora

Foissner et al. (1991, 1992, 1994, 1995) made a revision for a selection of species (in German) and,
also (Foissner, 1993), for the Colpodea, which are
mainly soil-dwelling ciliates. A comprehensive guide
to plankton ciliates is now also available (Foissner et
al., 1999). A new revision of the Oxytrichidae (Ciliophora, Hypotrichia) (Berger, 1999) has taxonomic
keys to genera and species. A good taxonomic description (in German) of the rhizopoda and heliozoa
is given by Page & Siemensma (1991), while a comprehensive overview of the taxonomy of flagellates is
provided by Patterson & Larsen (1991) and Ettl et al.
(1985, 1990). Unfortunately, the extensive taxonomic
literature is dispersed in many separate papers and
original descriptions.
Literature on heterotrophic protozoa pH 3 (Table 1)
References to heterotrophic protozoa living in acidic
environments at or below pH 3 are relatively few
(Table 1). Data are largely restricted to anthropogenically altered systems, while information on natural

acidic systems are almost absent. Recently, some

amoebae have been found in natural acidic streams
(Woelfl, pers. comm.; Whitton & Satake, pers. comm.:
see Table 1). Most of the records correspond to
ciliates and Sarcodina. In the acidic mining lakes
of Eastern Germany investigated by us, the following taxa or groups dominated: prostomatids (Urotricha armata), peritrichids (Vorticella sp.), hypotrichs
(mainly Oxytricha sp.) and heliozoa (Actinophryscf.
sol). Other ciliate taxa also occurred occasionlly e.g.
members of the genus Frontonia or chilodonellids in
the periphyton or benthos. Some groups important in
the plankton of neutral lakes are lacking entirely e.g.
the oligotrichs.
Lackey (1938) and McConathy & Stahl (1982) also
mentioned hypotrichs in acid mine drainage and strip
mine lakes, and this is supported by our own findings
from acidic mining lakes. Taking into consideration
the ubiquity of ciliates or protozoa in general, it is difficult to judge the reliability of some records, such as
for Paramecium caudatum (Joseph, 1953), Cyclidium
sp. and Prorodon sp. (Lackey, 1938).

156
References
Berger, H., 1999. Monograph of the Oxytrichidae (Ciliophora,
Hypotrichia). In Dumont, H. J. & M. J. A. Werger (eds), Monographiae Biologicae. Volume 78. Kluwer Academic Publishers,
Dordrecht: 1079 pp.
Berger, H. & W. Foissner, 1987. Morphology and biometry of some
soil hypotrichs (Protozoa:Ciliophora). Zool. Jb. Syst. 114: 193
229.
Bick, H. & E. Drews, 1973. Selbstreinigung und Ciliatenbesiedlung in saurem Millieu (Modellversuche). Hydrobiologia 42:
393402.
Ehrlich, H. L., 1963. Microorganisms in acid drainage from a copper
mine. J. Bact. 86: 350352.
Ettl, H., G. Gaertner, H. Heynig & D. Mollenhauer (eds), 1985,
1990. Ssswasserflora von Mitteleuropa. Bd. 1 Chrysophyceae
und Haptophyceae, 1985; Bd. 6 Dinophyceae (Dinoflagellida),
1990. Gustav Fischer Verlag, Jena, Stuttgart, Lbeck, Ulm.
Foissner, W., 1993. Colpodea (Ciliophora). G. Fischer Verlag,
Stuttgart, Jena, New York: 798 pp.
Foissner, W., H. Berger & F. Kohmann, 1992. Taxonomische
und kologische Revision der Ciliaten des Saprobiensystems.
Bd. II: Peritrichida, Heterotrichida, Odontostomatida. Informationsberichte des Bayer. Landesamtes fr Wasserwirtschaft, Heft
5/92: 520 pp.
Foissner, W., H. Berger & F. Kohmann, 1994. Taxonomische und
kologische Revision der Ciliaten des Saprobiensystems. Bd. III:
Hymenstomata, Prostomatida, Nassulida. Informationsberichte
des Bayer. Landesamtes fr Wasserwirtschaft, Heft 1/94: 548 pp.
Foissner, W., H. Berger & J. Schaumburg, 1999. Identification and
ecology of limnetic plankton ciliates. Informationsberichte des
Bayer. Landesamtes fr Wasserwirtschaft, Heft 3/99: 793 pp.
Foissner, W., H. Berger, H. Blatterer & F. Kohmann, 1995. Taxonomische und kologische Revision der Ciliaten des Saprobiensystems. Bd. IV: Gymnostomatea, Loxodes, Suctoria. Informationsberichte des Bayer. Landesamtes fr Wasserwirtschaft, Heft
1/95: 540 pp.
Foissner, W., H. Blatterer, H. Berger & F. Kohmann, 1991. Tax-

onomische und kologische Revision der Ciliaten des Saprobiensystems. Bd. I: Cyrtophorida, Oligotrichida, Hypotrichida,
Colpodea. Informationsberichte des Bayer. Landesamtes fr
Wasserwirtschaft, Heft 1/91: 478 pp.
Johnson, D. B., 1998. Biological abatement of acid mine drainage:
The role of acidophilic protozoa and other indigenous microflora.
In Geller, W., H. Klapper & W. Salomons (eds), Acidic Mining
Lakes. Springer Verlag, Berlin, Heidelberg, New York: 285301.
Joseph, J. M., 1953. Microbiological study of acid mine waters:
Preliminary report. Ohio J. Science 2: 123127.
Kahl, A., 1930-1935. Wimpertiere oder Ciliata (Infusoria). In Dahl,
F. (ed.), Die Tierwelt Deutschlands. G. Fischer Verlag, Jena: 886
pp.
Lackey, J. B., 1938. The flora and fauna of surface waters polluted
by acid mine drainage. Publ. Health Rep. 53: 14991507.
Lackey, J. B., 1939. Aquatic life in waters polluted by acid mine
waste. Publ. Health Rep. 54: 740746.
McConathy, J. R. & J. B. Stahl, 1982. Rotifera in the plankton
and among filamentous algal clumps in 16 acid strip-mine lakes.
Trans. Ill. Acad. Sci. 75: 8590.
McGinness, S. & D. B. Johnson, 1992. Grazing of acidophilic
bacteria by a flagellated protozoan. Microb. Ecol. 23: 7586.
Page F. C. & F. J. Siemensma, 1991. Nackte Rhizopoda und
Heliozoa. Gustav Fischer Verlag, Stuttgart, New York
Packroff, G., 1998. Protozoen in Tagebaurestseen qualitative
und quantitative Aspekte. Deutsche Gesellschaft fr Limnologie,
Krefeld, Tagungsberichte.
Patterson, D. J. & J. Larsen, 1991. The Biology of Free-Living
Heterotrophic Flagellates. Systematics Association, Clarendon
Press, Oxford.
Satake, K., 2000. Iron accumulation on the cell wall of the aquatic
moss Drepanocladus fluitans in an acid lake at pH 3.43.8.
Hydrobiologia. 433: 2530
Vallin, S., 1953. Zwei azidotrophe Seen im Kstengebiet von Nordschweden, Rep. Inst. Freshw. Res. Drottningholm 34: 167189.
Woelfl, S., B. Zippel & G. Packroff, 1998. Planktongesellschaften
der mitteldeutschen Tagebaurestseen. Deutsche Gesellschaft fr
Limnologie, Frankfurt, Tagungsberichte: 376380