NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY VOLUME 33 NUMBER 1 WARSAWhttp://rcin.org.pl, POLAND 1994 ISSN 0065-1583 Polish Academy of Sciences Nencki Institute of Experimental Biology

ACTA PROTOZOOLOGICA

International Journal on Protistology

Editor in Chief Jerzy SIKORA

Editors Hanna FABCZAK and Anna WASIK

Managing Editor Małgorzata WORONOWICZ

Editorial Board

Andre ADOUTTE, Paris Stanisław L. KAZUBSKI, Warszawa Christian F. BARDELE, Tübingen Leszek KUZNICKI, Warszawa, Chairman Magdolna Cs. BERECZKY, Göd John J. LEE, New York Jacques BERGER, Toronto Jiri LOM, Ćeske Budejovice Y.-Z. CHEN, Beijing Pierangelo LUPORINI, Camerino Jean COHEN, Gif-Sur-Yvette Hans MACHEMER, Bochum John O. CORLISS, Albuquerque Jean-Pierre MIGNOT, Aubiere Gyorgy CSABA, Budapest Yutaka NAITOH, Tsukuba Isabelle DESPORTES-LIVAGE, Paris Jytte R. NILSSON, Copenhagen Stanisław DRYL, Warszawa Eduardo ORIAS, Santa Barbara Tom FENCHEL, Helsing0r Dimitrii V. OSSIPOV, St. Petersburg Wilhelm FOISSNER, Salsburg Igor B. RAIKOV, St. Petersburg Vassil GOLEMANSKY, Sofia Leif RASMUSSEN, Odense Andrzej GRĘBECKI, Warszawa, Vice-Chairman Michael SLEIGH, Southampton Lucyna GRĘBECKA, Warszawa Ksenia M. SUKHANOVA, St. Petersburg Donat-Peter HÄDER, Erlangen Jiri VAVRA, Praha Janina KACZANOWSKA, Warszawa Patricia L. WALNE, Knoxville Witold KASPRZAK, Poznań

ACTA PROTOZOOLOGICA appears quarterly.

© NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY, POLISH ACADEMY OF SCIENCES Printed at the MARBIS, 60 Kombatantów Str., 05-070 Sulejówek, Poland

Front cover: Vauchomia nephritica Corliss, 1979. In: The Ciliated Protozoa. 2ed. Pergamon Press, London.

http://rcin.org.pl ACTA Acta Protozoologica (1994) 33: 1 - 51

PROTOZOOLOGICA

An Interim Utilitarian ("User-friendly") Hierarchical Classification and Characterization of the Protists

John O. CORLISS

Albuquerque, New Mexico, USA

Summary. Continuing studies on the ultrastructure and the molecular biology of numerous species of protists are producing data of importance in better understanding the phylogenetic interrelationships of the many morphologically and genetically diverse groups involved. Such information, in turn, makes possible the production of new systems of classification, which are sorely needed as the older schemes become obsolete. Although it has been clear for several years that a Kingdom PROTISTA can no longer be justified, no one has offered a single and compact hierarchical classification and description of all high-level taxa of protists as widely scattered members of the entire eukaryotic assemblage of organisms. Such a macrosystem is proposed here, recognizing Cavalier-Smith's six kingdoms of eukaryotes, five of which contain species of protists. Some 34 phyla and 83 classes are described, with mention of included orders and with listings of many representative genera. An attempt is made, principally through use of well-known names and authorships of the described taxa, to relate this new classification to past systematic treatments of protists. At the same time, the system will provide a bridge to the more refined phylogenetically based arrangements expected by the turn of the century as future data (particularly molecular) make them possible. The present interim scheme should be useful to students and teachers, information retrieval systems, and general biologists, as well as to the many professional phycologists, mycologists, protozoologists, and cell and evolutionary biologists who are engaged in research on diverse groups of the protists, those fascinating "lower" eukaryotes that (with important exceptions) are mainly microscopic in size and unicellular in structure.

Key words. Protists, algae, fungi, protozoa; macrosystematics of the Eukaryota: kingdoms, phyla, classes, orders, and representative genera.

INTRODUCTION eukaryotic algae, and "lower" fungi) have been in a state of great activity, with an increasing number of biologists During the past 20 years, studies on the systematics becoming interested in such research. As our knowledge and evolution of the protists (essentially all protozoa, has grown concerning the cytoarchitecture and the phylogenetic interrelationships of the large number of Address for correspondence: J. O. Corliss, P. O. Box 53008, species (and their higher taxa) involved, so has our Albuquerque. New Mexico 87153, USA. understanding with respect to the most "natural" scheme This paper is dedicated to the memory of Zdzisław Raabe of classification to employ for these ubiquitous and (1909-1972) who, 30 years ago, perceptively foresaw the prob- cosmopolitan eukaryotic - generally microscopic and lems involved in constructing a macrosystem for the Protozoa based on evolutionary principles (Raabe 1964a) and who, in the often unicellular - organisms. In recent years, with the same year, published a comprehensive protozoological textbook development of molecular chronometric techniques (e.g. ! (Raabe 1964b) and, in the preceding year, had founded the international journal Acta Protozoologica. ribosomal RNA sequencing: see Christen 1992), com- http://rcin.org.pl 2 J. O. Corliss bined with ultrastructural investigations and the applica- (Wiley 1981). But such assemblages, so identified, are tion of sophisticated cladistic analyses, the outlook is sometimes used here. I am in sympathy with Raabe's even more auspicious for our learning enough about the (1964a) observation of 30 years ago that it is "not evolution of protistan groups to be able to propose a necessary nor possible to follow the rules of a strict robust classification system that will withstand the test purism as to the monophyletism of groups in of such phylogenetic principles as monophyly and can protozoological systematics". thus be expected to endure for a reasonable number of Scattered controversial matters (ever present in taxo- years. nomy !) are arbitrarily resolved in place, sometimes pure- At the present time, however, we are taxonomically ly by intuition, but with due attention to priority, in a state of flux. We are frustratingly trapped between common sense, courtesy, and stability (Corliss 1972), as existing classifications of protists that are recognized to well as to (my interpretation of) the facts available in be faulty and some future scheme(s) not yet available. the case. I agree with Silva (1984) that a considerable The latter, hopefully closer to the ideal natural system degree of subjectivity is inevitable when anyone at- long awaited, probably will not be ready for at least tempts to construct a macrosystem for a large and several years yet, perhaps not until the turn of the diverse group of organisms, many poorly known, no century. matter what approaches or principles are used nor how This paper represents an earnest attempt to fill in that conscientiously they are followed. long time-gap between available classifications. I In the present effort, I acknowledge my dependence believe that there is a pressing need now for a use- on the insightful analyses of Cavalier-Smith (1981, ful/usable interim system treating the protists overall in 1986, 1989b, 1991b, 1993a-c). He has provided the a manner understandable to the general protozoolo- evolutionary framework for much of the classification gist/phycologist/mycologist and the myriads of cell and presented on the following pages. But I make no attempt evolutionary biologists, biochemists, and general to utilize most of his proposed intermediate-level group- biologists (including students and teachers as well as the ings, his frequently interposed sub-, infra-, and supra- many professional researchers) who use or talk about taxa at kingdom, phyletic, class, and ordinal levels, these fascinating yet often neglected eukaryotes the although I appreciate their value to him. My system also described species of which may have already reached differs from his in other ways (e.g. I have fewer the respectable number of 200,000. I am presenting a protozoan but more chromist phyla, and I cover the compact "user-friendly" taxonomic scheme that is built fungal and plant protists as well); and I offer more along traditional lines but also incorporates the latest detailed comparative descriptions of groups and list ultrastructural and molecular data that are available. many more representative genera for each major taxon A major aim here is to offer the higher protistan taxa covered. As a born "splitter", Cavalier-Smith may indeed in a standard hierarchical arrangement, even if a measure have been guilty of a degree of "taxonomic inflation" in of speculation or presumption concerning relationships his classifications. I have tried to avoid this myself; and must sometimes be invoked to do this. The desired result it may be noted that no taxa are erected as new in this should be a system conveniently understandable to more paper. As our knowledge increases, however, newly than just a few specialists. Finally, in order to link the discovered significant differences between organisms or present with both the past and the future, a deliberate groups of organisms often require their greater, even effort is made to preserve groups and names of groups much greater, separation taxonomically than was pre- either familiar from past classifications or potentially viously given to them. In my scheme, for example, I familiar (or at least palatable!) in cases of certain newer have endorsed far more phyla and classes than appeared groups or names that I have adopted from research in the Levine Report of 14 years ago (Levine et al. 1980). papers of current workers in fields that impact on protis- For details, I have depended heavily on the literature. tological systematics. An INDEX of Taxonomic Names Monographs (and shorter papers as well) by phycologi- is supplied to aid the reader in locating genera or higher cal, protozoological, and mycological specialists on dif- groups of special interest to him or her. Some of my taxa ferent taxa have been indispensable for my may not be identical with putative evolutionary lines of understanding of the composition and taxonomic boun- the very recent literature; that is, they may not be daries of such groups: some of the major works among indisputably monophyletic in nature. In fact, several are these are cited in the immediately following section. The likely paraphyletic and a few perhaps polyphyletic authoritative chapters in four recent treatises (Harrison

http://rcin.org.pl "User-friendly" Classification of the Protists 3 and Corliss 1991, Lee et al. 1985, Margulis et al. 1990, (1993), Leipe and Hausmann (1993), Levine (1988), Parker 1982) deserve special mention; in general, how- Lipscomb (1985, 1991), Lom(1990), Lom and Dykovâ ever (to save space), these individual specialist-contribu- ( 1992), Lynn ( 1981 ), Lynn and Corliss ( 1991 ), Margulis tions - like many of the other numerous scattered (1970, 1981, 1993), Margulis et al. (1990), Margulis et taxonomic papers consulted - are not directly cited in al. (1993), Margulis et al. (1984), Mattox and Stewart this paper. (1984), Melkonian (1984), Melkonian et al. (1991), Mishler and Churchill (1985), Moestrup (1982, 1991), Môhn (1984), Moss (1991), Miiller (1992), Mylnikov FURTHER BACKGROUND INFORMATION (1991), O'Kelly (1992, 1993a,b), O'Kelly and Floyd (1984), Olive (1975), Page and Blanton (1985), Page and Siemensma (1991), Parker (1982), Patterson The protist literature has become so vast, with a (1989a ,b), Patterson and Fenchel (1985), Patterson and continuing avalanche of papers since my reviews of 8-10 Larsen (1991), Patterson et al. (1989), Patterson and years ago (Corliss 1984, 1986a), that no attempt can be Sogin (1993), Patterson and Zolffel (1991), Perkins made here to cite all works of some relevance to my (1991), Powers (1993), Preisig (1989), Preisig et al. present broad topic. The reader is referred to the follow- (1991), de Puytorac et al. (1974, 1987, 1993), Ragan ing publications (which include reviews and overviews (1988), Ragan and Chapman (1978), Raikov (1982), containing bibliographic sections rich in references to Rothschild (1989), Rothschild and Heywood (1987), hundreds of significant individual papers) that are most- Round (1984), Round et al. (1990), Schlegel (1991), ly concerned with recent ultrastructural or molecular Silva (1980), Sleigh (1989), Sluiman (1985), Small and researches directly bearing on protist systematics: Lynn (1985), Smith and Patterson (1986), Sogin (1991), Alexopoulos and Mims (1979), Andersen (1989, Sogin et al. (1989), Sprague (1977), Sprague et al. 1991, 1992), Andersen et al. (1993), Anderson (1983), (1992), Stewart and Mattox (1980), Tappan (1980), Bardele (1987), Baroin et al. (1988), Baroin- Taylor (1978, 1987), van den Hoek et al. (1993), Vick- Tourancheau et al. (1992), Barr (1992), Bold and Wynne erman ( 1992), Vickerman et al. ( 1991 ), Vossbrinck et al. (1985), Bowman et al. (1992), Bremer (1985), Bremer (1987), Wainright et al. (1993), Whittaker (1969, 1977), et al. (1989), Bovee (1991), Broers et al. (1990), Whittaker and Margulis (1978), Woese (1987), Woese Brugerolle (1991a,b), Canning and Lom (1986), et al. (1990), Wolters (1991). Cavalier-Smith (1986, 1987, 1989a,b, 1991a,b, 1993a- For nomenclatural help, the original literature has, c), Chapman and Buchheim (1991), Christensen (1980, once again, been indispensable. But several comprehen- 1989, 1990), Cole and Sheath (1990), Corliss (1979, sive works deserve special mention: Biitschli (1880- 1984, 1986a, 1987, 1989, 1991a), Copeland (1956), Cox 1889), Cavalier-Smith (1993c), Chrétiennot-Dinet et al. (1980), Davidson (1982), Dodge (1979), Douglas et al. (1993), Copeland (1956), Karpov (1990), Krylov and (1991), Dragesco and Dragesco-Kernel's (1986), Farmer Starobogatov ( 1980), Levine et al. ( 1980), Poche (1913), (1993), Felsenstein (1988), Fenchel (1987), Fenchel and de Puytorac et al. (1987), and Silva (1980). Finlay (199 l),Fensome et al. (1993), Fleury et al. (1992), In "pre-protist" days and before the advent of Foissner and Foissner (1993), Foissner (1987, 1993), widespread usage of electron microscopy in study of Foissner et al. (1988), Gajadhar et al. (1991), Grain microorganisms ("Age of Ultrastructure": Corliss, (1986), Green et al. (1989), Grell (1991a,b), Grell et al. 1974), biologists did not find it too difficult to recognize (1990), Hanson (1977), Hasegawa et al. (1993), Haus- or classify the several major groups of algae ("mini- mann et al. (1985), Hawksworth et al. (1983), Hibberd plants") and protozoa ("mini-animals"). Algae were and Norris (1984), Hori and Osawa (1987), Hiilsmann predominantly photosynthetic organisms, often non- (1992), Irvine and John (1984), Karpov (1990), Karpov motile, mainly unicellular or filamentous in organiza- and Mylnikov (1989), Kendrick (1985), Kivic and tion; protozoa were mostly phagotrophic, motile, and Walne (1984), Knoll (1992), Kreier (1977-1978), Kreier unicellular. The bases for separation of groups of species and Baker (1991), Kristiansen and Andersen (1986), at higher taxonomic levels included differences in life Krylov (1981), Krylov and Starobogatov (1980), cycles and pigmentation for algae (e.g. green, red, Kuznicki and Walne (1993), Larsen and Patterson brown, golden-brown) and variation in kinds and num- (1990), Larsson (1986), Lee et al. (1985), Lee and bers of locomotory structures (e.g. pseudopodia, flagel- Kugrens (1992), Leedale (1974, 1980), Leipe et al. la, cilia) and other specialized organelles in the case of

http://rcin.org.pl 4 J. O. Corliss

protozoa. Ecological characters (e.g. free-living vs revision; although the writer is a past chairman of the parasitic, marine vs fresh-water, sessile vs free-swim- committee, the present paper in no way is to be con- ming, and nutritional proclivities) were also often in- sidered the outcome of the committee's current delibera- voked. Botanists studied the algae; zoologists, the tions, which are continuing without my participation. protozoa. Also, independent of the Society, de Puytorac et al. A few years after the great evolutionary discovery of (1987) and Sleigh (1989), in editions of their well- (the concept of) the prokaryotes and the eukaryotes, the known textbooks on the protozoa and other protists, have "protist perspective" began to be adopted when consider- used taxonomic arrangements mostly of their own ing the "lower" eukaryotes (see historical review in making, although largely based on taxonomic works Corliss 1986a). At about the same time, growing accep- from the literature. tance of the Serial Endosymbiosis Hypothesis explained In addition to the classifications mentioned above that the likely endosymbiotic origins of plastids and involve protists, the most outstanding recent attempt to mitochondria, answering some previously inexplicable bring these organisms together under a single taxonomic questions while raising some new ones concerning the heading - viz. the Pro(toc)tista - has been that of Mar- evolution of organisms possessing such organelles. gulis and colleagues, commencing with such seminal Most botanists have long accepted traditional views papers as those by Whittaker (1969, 1977), Margulis in setting up hierarchical classifications for their (1974), and Whittaker and Margulis (1978) and cul- divisions and classes of algae and "lower" fungi, follow- minating in book form in Margulis et al. (1990). Many ing such great authorities of the past as the Agardhs, workers, including the present author (e.g. note my Blochmann, Chodat, Dangeard, de Bary, Fritsch, enthusiasm for the idea in Corliss 1984, 1986a,b, 1991a) Kjellman, Klebs, Kiitzing, Lamouroux, Lemmermann, and numerous teachers and textbook writers around the Lister, Luther, Pascher, Rabenhorst, Smith, West, Wet- world, have adopted this appealing way of viewing the tstein, Wille, Winter, and Zopf. See the widely accepted living world as divisible taxonomically into five con- systems, with minor changes, adopted in many botanical venient kingdoms, among them the Protista. Some 27-45 and phycological (e.g. Bold and Wynne, 1985; van den phyla are generally assigned to the protist kingdom, in Hoek et al. 1993) textbooks and in numerous recognition of the great diversity (supported today by monographs as well. The zoologists have acted essen- hundreds of ultrastructural observations) found among tially the same with respect to the protozoa, relying on its numerous members (Barnes 1984; Corliss 1984; the works of such leaders as Alexeieff, Balbiani, Karpov 1990; Margulis and Schwartz 1982, 1988). Biitschli, Calkins, Cash, Cepede, Chatton, Deflandre, Other scattered proposals of multikingdom systems for Doflein, Dogiel, Dujardin, Ehrenberg, Entz (Jr. and Sr.), the eukaryotes have not linked the various taxa com- Grasse, Haeckel, Hartmann, Hertwig, Kahl, Kent, posed purely of protists together in a single kingdom Kofoid, Kudo, Lankester, Laveran and Mesnil, Leger, (see the pioneering paper by Leedale 1974; Mohn 1984; Leuckart, O.F. and J. Muller, Penard, Prowazek, and reviews in Corliss 1986a and Lipscomb 1991). Schaudinn, Schewiakoff, Stein, and Wenyon. For ex- Phylogeneticists have made invaluable contributions ample, see the highly popular and authoritative to our understanding of the probable origins of various protozoological volumes by Grell (1973) and Kudo major monophyletic lines of protists, but they have (1966). uniformly been reluctant - to date - to suggest definitive, In more recent years, the Society of Protozoologists hierarchical arrangements of ranked taxa of the principal has established a special committee to produce "up- assemblages of eukaryotes that involve species of dated" systems of protozoan classification: see the protists (e.g. Lipscomb 1991; Patterson 1988; Patterson reports of Honigberg et al. (1964) and Levine et al. and Sogin 1993). On the other hand, cell and evolution- (1980). The resulting schemes have often been con- ary biologist Cavalier-Smith has published a series of sidered authoritative for some years following their heuristic papers during the past dozen years (e.g. promulgation: for example, the popular "Illustrated Cavalier-Smith 1981, 1983, 1986, 1987, 1989b, 1991b, Guide to the Protozoa," edited by Lee et al. (1985), in 1993a-c) in which he has boldly presented novel large measure endorsed the Levine Report. These "con- schemes of eukaryotic classification, naming and rank- sensus" classifications have indeed, in many ways, rep- ing all implicated major groups and generally distribut- resented improvements over previous systems. The ing the protists among all but one (the Animalia) of his Society now has a new committee working on a fresh several kingdoms.

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So, within the past 20-30 years, we have had, first, a Multiple kingdoms of eukaryotes have been sug- clinging to the conventional macrosystems of algae and gested in the past, as mentioned on a preceding page. protozoa originally set up essentially on the basis of The number has most commonly been four, of which morphological data obtainable by use of light micros- often the protists have represented one (except in the copy. Then we have witnessed the "protist revolution," works of Cavalier-Smith, who some years ago foresaw with its emphasis on removing the taxonomic barriers the necessity for the demise of Protista as such: see of old (often including rejection of formal names that references to his relevant papers above and below). had become misleading or meaningless: e.g. Unusual was Môhn's (1984) proposal of 16 kingdoms, "Phytoflagellata" and "Zoomastigophora") on the basis with protists alone comprising 10 of them. of abundant and more precise ultrastructural and If one recognizes kingdoms within the great molecular information. This integrated protistan ap- eukaryotic group, and - for that matter - among the proach so permeated our thinking that there was an prokaryotes as well, then a name of still higher exuberant and intensive drive to lump all protists taxonomic rank must be found for those two "super" together into a single kingdom (although with many assemblages. There is considerable controversy over the separate evolutionary lines within that great as- most appropriate appellation; I am going to employ the semblage), as discussed above. Today, the prevailing term "empire" without strong feelings either pro or con. view among leading protistological researchers is that Thus, the kingdoms described below comprise the em- these "lower" eukaryotes can no longer be properly pire EUKARYOTA. restricted to a single taxonomic kingdom, although few Here, as in following sections, I am presenting a investigators have stated so directly and even fewer - classification in the conventional manner: naming the aside from Cavalier-Smith (1981 et seq.), the most taxon (with authorship and date) and offering a very notable exception - have relieved the problem in a brief diagnosis, description, or characterization, fol- constructive way, by proposing explicit hierarchical lowed by mention of major embraced sub-taxa. I am classifications to contain the multiple kingdoms and essentially endorsing the six (a reasonable number) phyla assignable to the eukaryotic assemblage overall. eukaryotic kingdoms of Cavalier-Smith (1989a): three Thus a single kingdom Protista as such must be laid are comprised solely of protist species, one includes to rest, but long live the protists themselves in all their many, another has only a few; and his sixth, Animalia, awesome diversity! has none at all, in my view. It may be noted that the great bulk of the photosynthetic or "algal" protists, with the important exceptions of the euglenoids and the dinoflagellates, falls into two kingdoms, the Chromista MAJOR GROUPS OF EUKARYOTES and the Plantae; the largely heterotrophic or "protozoan" protists dominate two kingdoms also, the Archezoa and The kingdoms the Protozoa. Mixotrophic species occur mainly in the Chromista (except, again, for numerous members of the Although all the desired information is far from being protozoan phyla Euglenozoa and Dinozoa). The single available, one may find it useful to consider what choice phylum of protists in the kingdom Fungi is composed and what number of kingdoms may best represent the solely of osmotrophic forms; and the heterotrophic, principal groups of eukaryotes as they are known to date. multicellular, multitissued kingdom Animalia is con- Certainly modern evolutionary studies have supplied sidered to be without species of protists. sufficient data to demonstrate the tremendous A brief nomenclatural note regarding authorities for phylogenetically significant diversity among the protists the names of all kingdoms but the (modern) Chromista alone to warrant unequivocably the demise of a single is needed here. I am crediting early workers with the kingdom Protista. Furthermore, the nature of the several names Archezoa, Protozoa, Plantae, Fungi, and high-level groups of these organisms makes clear what Animalia, while aware of the substantial changes over the writer and others have often been reluctant to admit the past 100-240 years in the concepts, circumscription, in the past, viz., that some protists are more closely and composition applied to these top-level groups of related to members of other long-accepted kingdoms or eukaryotic organisms. In the case of the Archezoa, I am asseblages (e.g. Plantae, Fungi, Animalia) than they are disagreeing with both Cavalier-Smith and other workers to each other. by assigning the authorship to Haeckel who, I am con-

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vinced, has been misunderstood with respect to his use Phylum 4. OPALOZOA Cavalier-Smith, 1991 and concept of the term. For the Protozoa, I am crediting Class (1) Proterozoea Cavalier-Smith, 1981 Goldfuss with the name and the general concept, as is Class (2) Opalinatea Wenyon, 1926 Class (3) Kinetomonadea Cavalier-Smith, 1993 conventionally done. Finally, in the case of the "big Class (4) Hemimastigophorea Foissner et al., 1988 three" multicellular "higher" eukaryotic assemblages, I am honoring Linnaeus with all the names (and as of the Phylum 5. MYCETOZOA de Bary, 1859 Class (1) Protostelea Olive & Stoianovitch, 1966 date 1753), although the plants were originally estab- Class (2) Myxogastrea Fries, 1829 lished by him as comprising a kingdom Class (3) Dictyostelea Lister, 1909 VEGETABILIA. Phylum 6. CHOANOZOA Cavalier-Smith, 1989 As is evident, much has happened taxonomically and Class Choanoflagellatea Kent, 1980 nomenclaturally in the 10-year period since my last attempt to review the high-level status of the protists Phylum 7. DINOZOA Cavalier-Smith, 1981 (Corliss 1984). Yet, as will be clear from even a cursory Class 1) Protalveolatea Cavalier-Smith, 1991 Class 2) Dinoflagellatea Bütschli, 1885 glance at the classification of the 34 phyla and 83 classes detailed on the following pages (and see Table 1), the Phylum . CILIOPHORA Doflein, 1901 majority of my formerly proposed 18 "supraphyletic Class 1) Karyorelictea Corliss, 1974 Class 2) Polyhymenophorea Jankowski, 1967 assemblages" and most of the 45 phyla suggested at that (= Heterotrichea Stein, 1859 time have survived in one form or at one level or another. + Spirotrichea Bütschli, 1889) Some significant changes/interpretations have neverthe- Class 3) Colpodea Small & Lynn, 1981 less been made - an indication of the impact of new data Class 4) Phyllopharyngea de Puytorac et al., 1974 Class 5) Nassophorea Small & Lynn, 1981 on postulated phylogenetic interrelationships among the Class 6) Oligohymenophorea de Puytorac et al., 1974 diverse groups of protists and, thus, on their macrosys- Class 7) Prostomatea Schewiakoff, 1896 tematics. And far more information is made available in Class 8) Litostomatea Small & Lynn, 1981 the present - and considerably longer - paper, including Phylum . APICOMPLEXA Levine, 1970 a helpful INDEX of taxonomic names. Class 1) Perkinsidea Levine, 1978 Class 2) Gregarinidea Dufour, 1828 Table 1 Class 3) Coccidea Leuckart, 1879 The taxonomic assignment of 34 phyla and 83 classes of protists Class 4) Haematozoea Vivier, 1982 to kingdoms of the EUKARYOTA Phylum 0. RHIZOPODA von Siebold, 1845 Kingdom I. ARCHEZOA Haeckel, 1894 Class 1) Lobosea Carpenter, 1861 Phylum 1. ARCHAMOEBAE Cavalier-Smith, 1983 Class 2) Entamoebidea Cavalier-Smith, 1991 Class Pelobiontea Page, 1976 Class 3) Filosea Leidy, 1879 Class 4) Granuloreticulosea de Saedeleer, 1934 Phylum 2. METAMONADA Grasse, 1952 (= mostly Foraminiferea d'Orbigny, 1826) Class (1) Trepomonadea Cavalier-Smith, 1993 Class 5) Xenophyophorea Schulze, 1904 Class (2) Retortamonadea Grasse, 1952 Class (3) Oxymonadea Grasse, 1952 Phylum 1. HELIOZOA Haeckel, 1866 Phylum 3. MICROSPORA Sprague, 1977 Class 1) Actinophryidea Hartmann, 1913 Class (1) Rudimicrosporea Sprague, 1977 Class 2) Centrohelidea Kühn, 1926 Class (2) Microsporea Delphy, 1963 Class 3) Desmothoracidea Hertwig & Lesser, 1874 Class 4) Taxopodea Fol, 1883 Kingdom II. PROTOZOA Goldfuss, 1818 Phylum 1. PERCOLOZOA Cavalier-Smith, 1991 Phylum 12. RADIOZOA Cavalier-Smith, 1987 Class (1) Percolomonadea Cavalier-Smith, 1993 Class (2) Heterolobosea Page & Blanton, 1985 Sw£phylum-1- ACANTHARIA Haeckel, 1881 Class (3) Lyromonadea Cavalier-Smith, 1993 Class Acantharea Haeckel, 1881 Class (4) Pseudociliatea Corliss & Lipscomb, 1982 Swfcphylum -2- RADIOLARIA J. Miiller, 1858 Phylum 2. PARABASALA Honigberg, 1973 Class (1) Polycystinea Ehrenberg, 1838 Class (1) Trichomonadea Kirby, 1947 Class (2) Phaeodarea Haeckel, 1879 Class (2) Hypermastigotea Grassi & Foà, 1911 Phylum 13. MYXOZOA Grasse, 1970 Phylum 3. EUGLENOZOA Cavalier-Smith, 1981 Class Myxosporea Butschli, 1881 Class (1) Diplonematea Cavalier-Smith, 1993 Class (2) Euglenoidea Butschli, 1884 Phylum 14. ASCETOSPORA Sprague, 1978 Class (3) Kinetoplastidea Honigberg, 1963 Class Haplosporidea Caullery & Mesnil, 1899

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Kingdom IE. CHROMISTA Cavalier-Smith, 1981 Phylum 4. CHAROPHYTA Rabenhorst, 1863 Class (1) Charophyceae Rabenhorst, 1863 Swbkingdom (I) HETEROKONTA Luther, 1899 Class (2) Conjugatophyceae Engler, 1892 Phylum 1. BICOSOECAE Cavalier-Smith, 1989 SuZ>kingdom (II) BILIPHYTA Cavalier-Smith, 1981 Class Bicosoecidea Grasse & Deflandre, 1952 Phylum 1. RHODOPHYTA Rabenhorst, 1863 Phylum 2. LABYRINTHOMORPHA Page in Levine Class (1) Bangiophyceae Wettstein, 1901 et al., 1980 Class (2) Florideophyceae Warming, 1884 Class (1) Labyrinthulea Cienkowski, 1867 Class (2) Thraustochytriacea Sparrow, 1943 Phylum 2. GLAUCOPHYTA Bohlin, 1901 Class Glaucophyceae Bohlin, 1901 Phylum 3. DICTYOCHAE Haeckel, 1894 Class (1) Silicoflagellatea Borgert, 1891 Kingdom V. FUNGI Linnaeus, 1753 Class (2) Pedinellea Kristiansen, 1990 Phylum CHYTRIDIOMYCOTA Sparrow, 1959 Phylum 4. RAPHIDOPHYTA Chadefaud, 1950 Class Chytridiomycetes Sparrow, 1959 Class Raphidomonadea Chadefaud, 1950 Kingdom VI. AN I M ALIA Linnaeus, 1753

Phylum 5. PHAEOPHYTA Wettstein, 1901 (no taxa of protists here) Class (1) Phaeophyceae Kjellman, 1891 Class (2) Chrysophyceae Pascher, 1914 Class (3) Synurophyceae Andersen, 1987 Class (4) Pelagophyceae Andersen & Saunders, 1993 Empire EUKARYOTA Class (5) Eustigmatophyceae Hibberd & Leedale, 1970 Class (6) Xanthophyceae Allorge in Fritsch, 1935 Kingdom I. ARCHEZOA Haeckel, 1894 Phylum 6. DIATOMAE Agardh, 1824 Class (1) Coscinodiscophyceae Round & Crawford, 1990 Unicellular protists that (allegedly) primitively lack Class (2) Fragilariophyceae Round, 1990 mitochondria, plastids, typical Golgi bodies, Class (3) Bacillariophyceae Haeckel, 1878 hydrogenosomes, and peroxisomes, while manifesting Phylum 7. PSEUDOFUNGI Cavalier-Smith, 1986 various prokaryotic features in their ribosomes and their Class (1) Oomycetes Winter in Rabenhorst, 1879 rRNAs. Energy produced by anaerobic glycolysis. In- Class (2) Hyphochytriomycetes Sparrow, 1959 cluded species are amoeboid or flagellated (with low Swfckingdom (II) HAPTOPHYTA Christensen, 1962 number of flagella), or have no means of independent Phylum HAPTOMONADA Cavalier-Smith, 1989 locomotion. Some free-living, majority symbiotic in Class (1) Pavlovea Cava lier-Smith, 1986 variety of hosts and of small to very small body size. Class (2) Patelliferea Cavalier-Smith, 1993 Entire group is possibly polyphyletic; yet some workers Swbkingdom (III) CRYPTOPHYTA Pascher, 1914 would add the protozoan parabasalans to it as well. Contains three phyla and several classes and orders. Phylum CRYPTOMONADA Ehrenberg, 1838 Class (1) Goniomonadea Cavalier-Smith, 1993 Class (2) Cryptomonadea Stein, 1878

Swbkingdom (IV) CHLORARACHNIOPHYTA Hibberd & Norris, 1984 Kingdom II. PROTOZOA Goldfuss, 1818

Phylum CHLORARACHNIOPHYTA Hibberd & Norris, 1984 Predominantly unicellular, plasmodial, or colonial Class Chlorarachniophyceae Hibberd & Norris, 1984 phagotrophic, colorless protists, wall-less in the trophic Kingdom IV. P L A N T A E Linnaeus, 1753 state. Included species that are capable of photosynthesis (some mixotrophic) typically have cytosolic ^kingdom (I) VIRIDIPLANTAE Cavalier-Smith, 1981 chloroplasts with stacked thylakoids, lacking starch, and Phylum 1. PRASINOPHYTA Christensen, 1962 usually surrounded by three membranes. Nearly univer- Class (1) Pedinophyceae Moestrup, 1991 sally present are tubular (with a few notable exceptions) Class (2) Prasinophyceae Christensen, 1962 cristate mitochondria (when absent, replaced by hydrogenosomes), Golgi bodies, and peroxisomes. Phylum 2. CHLOROPHYTA Pascher, 1914 Class Chlorophyceae Wille in Warming, 1884 Flagellar mastigonemes, if present, never rigid and Phylum 3. ULVOPHYTA Stewart & Mattox, 1978 tubular. Numerous free-living (typically independently Class Ulvophyceae Stewart & Mattox, 1978 motile) and symbiotic species, commonly microscopic

http://rcin.org.pl 8 J. O. Corliss in size. As alleged progenitors of the following four Kingdom V. FUNGI Linnaeus, 1753 kingdoms, the protozoa - not unexpectedly - exhibit the greatest morphological, physiological, and genetic Eukaryotic organisms without plastids or diversity of all. The assemblage, although still broad and phagotrophy (osmotrophic/absorptive nutrition instead) large and very likely paraphyletic, represents a and possessing cell walls containing chitin and B-glu- taxonomic refinement over the classically known cans. Mitochondria (with flattened cristae) and "phylum Protozoa". peroxisomes nearly always present; Golgi bodies or Contains numerous phyla, classes, and orders. individual cisternae present. Contains one phylum of flagellated unicellular (occasionally filamentous) protists; all of the supra-protistan groups have multicel- Kingdom IH. CHROMISTA Cavalier-Smith, 1981 lular mycelia composed of hyphae and are completely without pseudopodia, flagella, or even centrioles. Many Predominantly unicellular, filamentous, or colonial symbiotic species but also many free-living, with the phototrophic protists. Chloroplasts, located in lumen of latter often macroscopic in size. rough endoplasmic reticulum, lack starch and Contains four phyla, only one of which is composed phycobilisomes and have a two-membraned envelope of protists. inside a periplastid membrane (all within the rough, occasionally smooth, ER). Mitochondria (generally with Kingdom VI. ANIMALIA Linnaeus, 1753 tubular cristae), Golgi bodies, and peroxisomes always present. When flagella present, at least one bears rigid, Multicellular, non-photosynthetic, usually phago- tubular, and usually tripartite flagellar hairs or mas- trophic eukaryotes exhibiting a triploblastic body or- tigonemes (most notable exception, the haptophytes). ganization with collagenous connective tissue The relatively few species without plastids share other sandwiched between two dissimilar epithelia. Mito- features in common with majority of forms embraced chondria (with flattened or rarely tubular cristae), Golgi here. Mostly free-living (but some groups not inde- bodies, and peroxisomes always present. Multiple tis- pendently motile); many microscopic in size, with some sues and organ systems, and typically with complex major exceptions (e.g. brown algae). embryological development during ontogeny. Com- Contains several phyla with numerous classes and monly macroscopic in size. Mostly free-living and orders. motile but with some symbiotic groups, latter usually exhibiting osmotrophic nutrition. Contains numerous phyla, classes, and orders, none Kingdom IV. PLANTAE Linnaeus, 1753 of which includes any protists.

Unicellular, colonial, or multicellular phototrophic The phyla and their major lesser taxa protists and multicellular photosynthetic "higher" eukaryotes, all typically (but not universally) with cel- In recent years, the phylum (or, often, in the case of lulosic cell walls in trophic stages. Cytosolic plastids, algae, the division) has become the principal high-level enveloped by two membranes, usually contain starch or taxonomic rank in considering both phylogeny and sys- phycobilisomes. Mitochondria (with flattened cristae), tematics of protists, a fact to which many papers in the Golgi bodies, and peroxisomes always present. Green literature attest (see reviews in Corliss 1984, 1986a, species have stacked thylakoids with chlorophylls a and 1993). And it is widely admitted that the number of phyla b; red algae, totally without flagella, have single unstack- of these "lower" eukaryotes must be a large one, not ed thylakoids covered with phycobilisomes, with surprising in consideration of their great morphological cytosolic starch. Predominantly free-living, and non- and genetic diversity. motile in trophic stages. The "higher" plants, commonly In view of relatively meager molecular data, the macroscopic in size, develop from embryos and are cladistic protistologist faces a difficult problem not only mostly terrestrial and vascular forms with alternation of in identifying these phyla (or appreciating that such a haploid and diploid generations. rank is appropriate for them) but in interrelating them Contains several phyla with quite a number of classes phylogenetically on the protistan sensu lato "tree". Some and orders. evolutionary biologists, on the other hand, feel a need

http://rcin.org.pl "User-friendly" Classification of the Protists 9 to assemble such groups into still higher packages (e.g. to my DISCUSSION section for lengthier consideration superphyla, infra- and subkingdoms, and kingdoms) and of some major evolutionary or taxonomic problems. also to subdivide them unmercifully at lower ranks, For a convenient summary of the classification interposing between phyla and classes such ranks as sub- presented in this paper, the reader is referred to Table 1 and infraphyla and superclasses (not to mention inter- mediate taxa at ordinal, familial, and generic levels as Phyla of Kingdom ARCHEZOA well). I can understand the rationale involved in the latter practices, for they allow the user of the resulting In addition to the three quite disparate phyla schemes to appreciate the clustering of certain taxa that described below, some workers have suggested the share key characters. Yet, for the general user, the inclusion here, also, of the parabasalan flagellates teacher and the student, and the person interested in (considered as the second phylum of the kingdom having a classification helpful in information retrieval, PROTOZOA in the present work) and/or of the too much detail is not a desirable feature, in my opinion. family Entamoebidae (in a class of the protozoan Also, the introduction of intermediate ranks often re- phylum Rhizopoda here). Other taxonomists conser- quires new names, adding to the memory burden of the vatively feel that this entire kingdom itself should be non-specialist. Therefore, in the present treatment of the subsumed by the PROTOZOA. protists, I am usually omitting reference to many of the "intermediate" ranks employed, for example, in the Phylum 1. ARCH AMOEBAE Cavalier-Smith, 1983 longer works of Cavalier-Smith (e.g. 1993c). Whenever possible, I have adopted phyletic names Amoeboid or amoeboflagellated (generally a poorly familiar from the literature, as long as the composition motile single flagellum) protists with characteristics and the rank of the taxon have not been too drastically of the kingdom (q.v.), although presumed presence changed over time (see DISCUSSION). With respect to of 70s ribosomes not yet confirmed. Microaerobic, the spelling of names of protist phyla, especially the with symbiotic bacteria; free-living, mostly fresh- prefixes and suffixes, I have - once again - tried to water habitats. maintain traditional forms of the words. In particular, I have retained the phylum/division ending "-a" (excep- Class Pelobiontea Page, 1976 tionally, -"ae" and one time "-i") so long used in both (syn. Karyoblastea Margulis, 1974 p.p.) botanical and zoological taxonomic literature. For clas- Single class, thus with characters of phylum. Two ses, I have used the traditional protozoological and orders recognized by some workers: Mastigamoebida botanical suffixes of "-ea" and "-phyceae" (occasional- Frenzel, 1892; and Phreatamoebida Cavalier-Smith, ly, "-cetes"); and for subclasses, "-ia". My orders end in 1991, latter solely for the genus Phreatamoeba. "-ida"; but, in the interest of saving space, not many Mastigamoeba, Mastigella, Mastigina, Pelomyxa, orders are included on the following pages. Phreatamoeba As an aid to readers of various backgrounds with respect to protistological high-level systematics, names Phylum 2. METAMONADA Grasse, 1952 of a goodly number of representative or common or familiar genera (plus some new within the past several Bi-, quadri-, octo- (or occasionally more) flagellated years) are given under the lowest-ranked taxa listed protists, mostly symbiotic species, with characters of within a specific phylum. The INDEX will serve as a the kingdom (q.v.), including 70s ribosomes and (e.g. convenient guide to the page-locations of these generic Giardia) 16s rRNA. Some free-living, majority intes- names. tinal symbionts of various hosts. Parabasalans (see My ordering of phyla within a kingdom is basically second phylum of kingdom Protozoa) are here tenta- (meant to be) phylogenetic. An alphabetical arrangement tively excluded from the present phylum. would be of little value. On the other hand, to make up for our ignorance of "true" evolutionary interrelation- Class (1) Trepomonadea Cavalier-Smith, 1993 ships, a measure of "educated guess-work" (= healthy One or two karyomastigonts, each with 1-4 flagella; speculation?) is required in quite a number of instances. contractile axostyle absent; cytostomal-cytopharyn- Quite often, brief comments are offered in place in geal apparatus present; few cell-surface cortical controversial situations; otherwise, the reader is referred microtubules. Free-living or symbiotic.

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Order 1. Diplomonadida Wenyon, 1926 Order 1. Minisporida Sprague, 1972 Brugerolleia, Giardia, Hexamita, Octomitus, Burkea, Buxtehudea, Chytridiopsis, Hessea Spironucleus, Trepomonas, Trigonomonas Order 2. Microsporida Balbiani, 1882 Order 2. Enteromonadida Brugerolle, 1975 Culicospora, Encephalitozoon, Endoreticulatus, Caviomonas, Enteromonas, Trimitus Enterocytozoon, Glugea, Gurleya, Loma, Microfilum, Mrazekia, Nosema, Perezia, Pleistophora, Spraguea, Class (2) Retortamonadea Grasse, 1952 Stempellia, Tardivesicula, Telomyxa, Thelohania, Generally with characteristics given for the first class Tricornia, Tuzetia, Unikaryon, Vairimorpha (above), but with cortical microtubules over entire body surface. Mostly intestinal symbionts (e.g. of Phyla of Kingdom PROTOZOA insects and mammals). Single order. Order Retortamonadida Grasse, 1952 Phylum 1. PERCOLOZOA Cavalier-Smith, 1991 Chilomastix, Retortamonas Unicellular, non-pigmented protozoa allegedly primi- Class (3) Oxymonadea Grasse, 1952 tively lacking Golgi bodies; peroxisomes usually One or more karyomastigonts, each with 4 flagella; present; mitochondria or, more rarely, hydrogeno- basal bodies of flagellar pairs are connected by a somes present; mitochondrial cristae flat, sometimes paracrystalline paraxostyle in which are embedded discoidal, atypical of kingdom. Flagella usually anterior ends of axostylar microtubules; axostyles present, 1-4 (occasionally more), without mas- typically contractile; cytopharynx absent. Intestinal tigonemes; some species are amoeboflagellates, symbionts of insects. Single order. several of which never have flagella; fresh-water and Order Oxymonadida Grasse, 1952 marine habitats. Monocercomonoides, Notila, Oxymonas, Pyrsonym- pha, Saccinobaculus Class (1) Percolomonadea Cavalier-Smith, 1993 Non-amoeboid, quadriflagellated forms; striated Phylum 3. MICROSPORA Sprague, 1977 rootlets absent. Exhibiting the most primitive char- acters of the phylum and comprising only a single Minute, unicellular, obligate intracellular symbionts, genus, species here have been assigned by past with characteristics of the kingdom (including 70s workers to the following much larger class. ribosomes); sporoplasm uni- or binucleate; no flagel- Percolomonas lated stage in life cycle; underdeveloped Golgi(?) Class (2) Heterolobosea Page & Blanton, 1985 bodies; resistant spores contain complex extrusome, Monopodial amoeboid trophic form; transitory with polar tube and cap; one layer of thick spore wall flagellated stage, sometimes missing altogether; chitinous. Commonly in variety of cells of diverse striated rootlets present; close association of rough fresh-water, marine, or terrestrial hosts, mainly endoplasmic reticulum with mitochondria. Fruiting arthropods (especially insects) and fishes, but includ- bodies present in the first order, absent in the second. ing even other protists. Name of the phylum is, Is the genus Fonticula here or in Rhizopoda? unfortunately, identical to the generic name of a green Order 1. Acrasida Schröter, 1886 algal protist in the kingdom Plantae. Acrasis, Pocheina Order 2. Schizopyrenida Singh, 1952 Class (1) Rudimicrosporea Sprague, 1977 Adelphamoeba, Gruberella, Heteramoeba, Naeg- Extrusion apparatus rudimentary, with thick leria, Paratetramitus, Pernina, Pseudovahlkampfia, (manubroid) non-spiraled polar tube and no Singhamoeba, Tetramastigamoeba, Tetramitus, polaroplast or posterior vacuole. Single order. Vahlkampfia Order Metchnikovellida Vivier, 1975 Amphiacantha, Desportesia, Metchnikovella Class (3) Lyromonadea Cavalier-Smith, 1993 Anaerobic flagellates with hydrogenosomes and no Class (2) Microsporea Delphy, 1963 peroxisomes; harp-shaped structure of microtubules; Complex extrusion apparatus, with coiled polar tube, two pair anterior flagella, 1-4 nuclei. Only two polaroplast and posterior vacuole typically present. genera. Many species in second order. Lyromonas, Psalteriomonas

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Class (4) Pseudociliatea Corliss & Lipscomb, 1982 with persistent nucleolus; many fresh-water free- Multiflagellated, multinucleate forms with living forms, but also number of important symbiotic mitochondria (with rigid discoid cristae) and species (e.g. human blood parasites); some species peroxisomes. Single genus, with several species. photosynthetic, with chloroplasts in cytosol with Some workers have appended these protists to the chlorophylls a and b and enveloped in three phylum Euglenozoa (below). membranes but lacking starch. Three classes; a pos- Stephanopogon sible fourth, Pseudociliatea, now appears in phylum 1, Percolozoa (above), and a possible fifth, Hemimas- Phylum 2. PARABASALA Honigberg, 1973 tigophorea, is placed tentatively in phylum 4, Opalozoa (below). The bodonids plus the Unicellular, almost exclusively symbiotic, flagellates trypanosomatids might deserve taxonomic separation with mastigont system typically with multiple flagella from the euglenoids proper at the level of subphylum. and one or more nuclei; 70s ribosomes; no mitochondria but hydrogenosomes in a double en- Class (1) Diplonematea Cavalier-Smith, 1993 velope; characteristic complex parabasal body ap- Phagotrophic flagellates (two equal flagella) lacking paratus (= Golgi body). Wide range of hosts, includ- chloroplasts, pellicular plates, kinetoplasts, paraxial ing humans, but many species in termites and wood- rods; plate-like mitochondrial cristae; feeding ap- feeding roaches. Some workers place this phylum in paratus with vanes and two supporting rods. Single the kingdom Archezoa. genus. Diplonema (syn. Isonema) Class (1) Trichomonadea Typically 4-6 flagella; pelta and non-contractile axos- Class (2) Euglenoidea Butschli, 1884 tyle part of each mastigont (one exception); trophic Unicellular or colonial, bi- (rarely more) flagellated form in one genus (Dientamoeba) permanently forms; phagotrophic, photosynthetic (with paramylon amoeboid with no flagella. storage product), osmotrophic, or mixotrophic; all Order Trichomonadida Kirby, 1947 pigmented species with stigma (eyespot) containing Bullanympha, Calonympha, Devescovina, Dien- (3-carotene derivatives and other carotenoid pig- tamoeba, Ditrichomonas, Hexamastix, Histomonas, ments. Numerous species. The exact taxonomic Monocercomonas, Pseudotrichomonas, Snyderella, placement within the class of a number of species Trichomonas symbiotic in copepods (especially members of such genera, themselves of doubtful validity, as Con- Class (2) Hypermastigotea Grassi & Foà, 1911 radinema, Paradistigma, Parastasia, and others) Mastigont system with numerous flagella and multi- must await further study. ple Golgi bodies; basal bodies of flagella often ar- Order 1. Euglenida Butschli, 1884 ranged in closely packed longitudinal or spiral rows; Astasia, Colacium, Distigma, Euglena, Eutreptia, single nucleus. Khawkinea, Phacus, Trachelomonas Order 1. Lophomonadida Light, 1927 Order 2. Euglenamorphida Leedale, 1967 Joenia, Lophomonas, Mesojoenia, Microjoenia Euglenamorpha, Hegneria Order 2. Trichonymphida Poche, 1913 Order 3. Rhabdomonadida Leedale, 1967 Barbulanympha, Deltotrichonympha, Holomas- Menoidium, Rhabdomonas tigotoides, Hoplonympha, Kofoidia, Macrospironym- Order 4. Heteronematida Leedale, 1967 pha, Spirotrichonympha, Teranympha, Trichonympha Entosiphon, Heteronema, Peranema, Petalomonas, Ploeotia, Sphenomonas Phylum 3. EUGLENOZOA Cavalier-Smith, 1981 Class (3) Kinetoplastidea Honigberg, 1963 Forms with 1 -4 flagella, with paraxial rods and non- Small, colorless flagellates with 1-2 flagella (arising tubular mastigonemes; with peroxisomes and com- from pocket and possessing paraxial rod) and monly discoidal mitochondrial cristae, latter atypical prominent kinetoplast (distinctive body of massed of kingdom; cytoskeleton of microtubules reinforcing DNA) within single mitochondrion, latter typically cortex; Golgi bodies well developed; nuclear division extending length of body; numerous peroxisomes http://rcin.org.pl 12 J. O. Corliss

(known as glycosomes) present; free-living or sym- Four (in first order) to many flagella, apical or ar- biotic, with latter (including blood parasites, often ranged in oblique longitudinal rows; typically one highly pathogenic) exhibiting elaborate life cycles (first order) or either two or many nuclei; no frequently involving two hosts. peroxisomes; osmotrophic nutrition; all species sym- Order 1. Bodonida Hollande, 1952 biotic, endocommensals principally in amphibian Bodo, Cephalothamnium, Cryptobia, Ichthyobodo, hosts. Differences between members of first and Procryptobia, Rhynchomonas second order, all not listed here, may require greater Order 2. Trypanosomatida Kent, 1880 taxonomic separation in the future. The entire class Blastocrithidia, Crithidia, Endotrypanum, Her- is rather atypical of the phylum Patterson's petomonas, Leishmania, Leptomonas, Phytomonas, (1986a) recent taxon Slopalinida also embraced Trypanosoma Proteromonas, which I have placed in the preceding class, Proterozoea. Phylum 4. OPALOZOA Cavalier-Smith, 1991 Order 1. Karotomorphida Cavalier-Smith, 1993 Karotomorpha Predominantly small, free-living, unicellular, Order 2. Opalinida Poche, 1913 uninucleate, biflagellated protozoa with tubular Cepedea, Opalina, Protoopalina, Protozelleriella, mitochondrial cristae and totally lacking chloroplasts, Zelleriella cortical alveoli, and rigid tubular mastigonemes. Likely a paraphyletic assemblage, many of its Class (3) Kinetomonadea Cavalier-Smith, 1993 species have not yet been well studied by modern Free-living uninucleate forms with 2-4 flagella, techniques. Cavalier-Smith (1993b, c) assigns some peroxisomes, usually unique extrusomes (kineto- 20 generally small orders here, many new, only a few cysts); mitochondrial cristae flat or with branched are considered below. Among problematical groups tubules; some species with axopodial axonemes possibly in this phylum, mostly in my class 1, are nucleated by axoplast associated with exceptionally various proteomyxids s.l., Ebria, Phagodinium, long centrioles. Possibly multiple orders in this class, Phagomyxa and the fungus-like Nephromyces. which includes some of the "helioflagellates" of the literature. Class (1) Proterozoea Cavalier-Smith, 1981 Ancyromonas, Dimorpha, Heliomonas, Histiona, Generally with characters of phylum; rarely, with Reclinomonas, Tetradimorpha flattened mitochondrial cristae; a few groups contain symbiotic forms. Many minute, little-studied free- Class (4) Hemimastigophorea Foissner, Blatterer & living marine, fresh-water, and soil flagellates or Foissner, 1988 amoeboflagellates may belong here (some included Small, colorless, multiflagellated, phagotrophic (but in partially tentative lists of genera given below). no permanent cytostome) protists with "infracilia- Order 1. Heteromitida Cavalier-Smith, 1993 ture" reminiscent of ciliates; mitochondrial cristae Amastigomonas, Anisomonas, Apusomonas, Cer- saccular-tubular; no paraxial rods, no mastigonemes; comonas, Diphyllea, Discocelis, Heteromita, Jakoba, two microtubule- bearing pellicular plates; complex Leucodictyon, Massisteria, Proteromonas, Pseudo- extrusomes. Found primarily in soils. Some workers spora, Thaumatomastix consider this class as possibly a separate phylum, and Order 2. Cyathobodonida Cavalier-Smith, 1993 even closer to the phylum Euglenozoa (above) than Cyathobodo, Kathablepharis, Leucocryptos, Phalan- indicated here. Single order, three genera. sterium, Platychilomonas, Pseudodendromonas, Order Hemimastigida Foissner et al., 1988 Spongomonas Hemimastix, Spironema, Stereonema Order 3. Plasmodiophorida Cook, 1928 (name better credited to Zopf, 1885?) Phylum 5. MYCETOZOA de Bary, 1859 Octomyxa, Plasmodiophora, Polymyxa, Sorodiscus, (syns. ± EUMYCETOZOA Zopf, 1885, and Spongospora, Tetramyxa, Woronina MYXOMYCETES & MYXOMYCOTA auctt. pp) Class (2) Opalinatea Wenyon, 1926 (syns. Protociliata Metcalf, 1918, Paraflagellata Free-living, unicellular or syncytial plasmodial Corliss, 1955, Slopalinida Patterson, 1986 p.p.) forms, non-flagellated in their uni- or multinucleate http://rcin.org.pl "User-friendly" Classification of the Protists 13

phagotrophic stages; mitochondrial cristae tubular; species may have quite complex basket-like loricae uni- or multicellular aerial fruiting bodies of siliceous costae arranged longitudinally. These (sporophores or sorocarps) bearing one to many widely distributed protists (especially in marine spores with cellulosic or chitinous walls; spore ger- habitats), known familiarly as the collar flagellates, mination produces amoeboid or uni- or biflagellated have also been called choanoflagellates, choanomo- cells. Widely distributed in decaying vegetation. Per- nads, craspedomonads, craspedophyceans and even haps the characterization of the whole phylum should craspedomonadophyceans. Cavalier-Smith's phyletic be expanded to include many of the taxonomically name, originally published as "Choanociliata", enigmatic marine plasmodial protists with emended by him in 1989. Single class with single reticulopodia studied by Grell (e.g. 1985, 1991b) and order: names both credited to Kent here. placed by him in an order Promycetozoida Grell, 1985: for example, Corallomyxa, Megamoebomyxa, Class Choanoflagellatea Kent, 1880 and Thcilassomyxa. But relationships of such genera (syn. Craspedophyceae Chadefaud, 1960) to the Rhizopoda (Lobosea or maybe the athalamid Order Choanoflagellida Kent, 1880 Granuloreticulosea), or even to certain heterokonts Acanthoeca, Acanthoecopsis, Bicosta, Calliacantha, (in the kingdom Chromista), remain unresolved pos- Codosiga, Conion, Diaphanoeca, Monosiga, Par- sibilities. Phylum contains both cellular and "acel- vicorbicula, Pleurasiga, Proterospongia, Salpin- lular" slime molds. goeca, Stephanoeca

Class (1) Protostelea Olive & Stoianovitch, 1966 Single amoeboid cells, with filose pseudopodia, give Phylum 7. DINOZOA Cavalier-Smith, 1981 rise to simple sorocarps (= sporocarps) of one to few spores on delicate, narrow stalk. Several species Biflagellated, uninucleate protozoa with amphiesmal (amoeboflagellates, in effect) have a flagellated vesicles or cortical alveoli (containing cellulosic stage in their life cycle. plates in some groups), tubular (sometimes ampul- Cavostelium, Ceratiomyxa, Protostelium liform) mitochondrial cristae, and peroxisomes; one flagellum typically with paraxial rod; ca. 50% of Class (2) Myxogastrea Fries, 1829 extant species pigmented, with chloroplasts contain- Generally with characters of phylum, as largest group ing chlorophylls a and c, enveloped by three (rarely of the plasmodial (or "acellular") slime molds. Mul- two) membranes, lacking phycobilisomes, and lo- tiple orders recognized. cated in cytosol; non-pigmented and some colored Badhamia, Comatricha, Cribraria, Didymium, species phagotrophic; nucleus haploid, typically with Echinostelium, Fuligo, Licea, Lycogala, Physarum, distinctive chromosomes consisting primarily of non- Stemonitis, Trichia, Tubulina protein complexed DNA. Assemblage at one time called the "Mesokaryota" because of its alleged pos- Class (3) Dictyostelea Lister, 1909 session of a combination of pro- and eukaryotic Cellular slime molds from soil with triphasic life characters. First of three phyla known collectively as cycle: unicellular amoeboid microphage, pseudoplas- the "Alveolata", a super-category designated a modium (slug) formed by aligned aggregating parvkingdom by Cavalier-Smith (1993c). Possibly myxamoebae, and multicellular sorocarp on branched assignable somewhere here is the puzzling "giant or unbranched stalks. protist" Hochbergia (a cephalopod symbiont measur- Acytostelium, Dictyostelium, Polysphondylium ing 1-2 mm in length: Shinn and McLean, 1989).

Phylum 6. CHOANOZOA Cavalier-Smith, 1989 Class (1) Protalveolatea Cavalier-Smith, 1991 Atypical dinozoa; closed mitosis, but mitotic spindle Free-living, uniflagellated, colorless, unicellular or intranuclear; chromatin of normal eukaryotic form; colonial forms with non-discoid flattened (atypical of all non-photosynthetic species, mostly free-living kingdom) mitochondrial cristae; single flagellum phagotrophs but some marine forms totally symbiotic surrounded by collar of microvilli (actin filaments (osmotrophic); typically unicellular and uninucleate, internally) used in microphagous feeding; marine but symbiotic forms may be branched and multi-

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nucleate. Several quite distinctive orders may be terrestrial habitats, but symbiotic and symphoriontic justifiable here. Some of the included genera require species associated with great variety of host or- further study to be certain of their taxonomic assign- ganisms. Sometimes known as the INFUSORIA ment. auctt. (a very old and vague term) or by the more apt Colponema, Ellobiopsis, Oxyrrhis, Thalassomyces name of HETEROKARYOTA Hickson, 1903, the cilioprotists comprise one of the largest protist phyla, Class (2) Dinoflagellatea Btitschli, 1885 with 8-10 classes and many orders. Second member With characters of phylum, as its major class; mostly of "Alveolata" group. unicellular species, but some form colonies (especial- ly catenoid); often free-living, auto- or phagotrophic Class (1) Karyorelictea Corliss, 1974 or both (mixotrophic), but some groups symbiotic Flattened body, often ribbon-like and contractile; (osmotrophic); members of a major endosymbiotic habitat commonly interstitial niches of marine sands sub-taxon have no pellicular alveoli and very low (one major genus fresh-water); two to many non- number of chromosomes with histones clearly dividing (and essentially diploid) macronuclei present, but dinospores prove their position here. formed anew at organism's fission from dividing Widely distributed forms, mostly planktonie. Multi- diploid micronuclei; postciliodesmata charac- ple orders in literature, with half of contained species teristically present; generally without cortical alveoli; represented by fossil forms (but only genera with many species without definitive mouth but living species are listed below). Class described here phagotrophic via non-ciliated area of ventral surface. is essentially the equivalent of botanists' Pyr- The group, considered primitive by a number of rhophyta Pascher, 1914, and Dinophyceae Fritsch, workers, is divisible into two orders. But the class 1927. itself should perhaps be reduced to a subordinate Alexandrium, Amoebophrya, Amphidinium, Blas- taxon of (part of) the next class, below: see comments todinium, Ceratium, Chytriodinium, Cryp- there. thecodinium, Cystodinium, Dinophysis, Duboscq- Kentrophoros, Loxodes, Remanella, Trachelocerca, uella, Erythropsidinium, Glenodinium, Gleodinium, Trachelonema, Tracheloraphis Gonyaulax, Gymnodinium, Gyrodinium, Haplozoon, Kofoidinium, Noctiluca, Oodinium, Oxytoxum, Class (2) Polyhymenophorea Jankowski, 1967 Peridinium, Polykrikos, Prorocentrum, Protoperi- (syns. Heterotrichea Stein, 1859 plus Spirotrichea dinium, Ptychodiscus, Pyrocystis, Pyrophacus, Btitschli, 1889, in effect; and Postciliodes- Rhizodinium, Roscojfia, Symbiodinium, Syndinium, matophora Gerassimova & Seravin, 1976 p.p.) Thoracosphaera, Zooanthella Diverse body shapes and sizes (some quite large), of both free-living (marine and fresh-water) and sym- Phylum 8. CILIOPHORA Doflein, 1901 biotic species; some groups with postciliodesmata; characteristically with many conspicuous buccal Commonly with numerous longitudinal rows of cilia membranelles, plus compound somatic ciliature (single or paired), with perkinetal fission (cirri) in some groups. Based on recent rRNA (homothetogenic, as opposed to the symmetrogenic analyses, supported by ultrastructural observations, of flagellates), and distinctive kinetidal infraciliature; some workers would split this huge and probably many have complex oral ciliature; cortical alveoli paraphyletic assemblage into at least two classes characteristic of most groups; mitochondrial cristae (thus elevating Polyhymenophorea to some supra- tubular, often curved; in anaerobic species, level or even eliminating it), with my first class mitochondria may be missing or replaced by Karyorelictea embraced by the heterotrich moiety hydrogenosomes; nuclear apparatus heterokaryotic, and the remainder of my polyhymenophoreans as- typically with one or more diploid micronuclei and signed to a spirotrich group. Here, each such major one or more polyploid macronuclei; sexual section is conservatively treated as a subclass. Each phenomenon of conjugation; heterotrophs nutrition- has many orders (the first one would also have two ally, but some species have photosynthetic algal subclasses of its own, the karyorelictians and the protists as endosymbionts. Widely distributed, often heterotrichians s.s., if it were elevated to independent conspicuous forms, mostly free-living in aquatic and class status).

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Subclass 1. Heterotrichia Stein, 1859 ly surrounded, in the old cyrtophorids, by nematodes- The classically known heterotrichs s.l. plus the newer mata (= cytopharyngeal basket or cyrtos); macro- protoheterotrichs and possibly (as discussed above) nucleus characteristically heteromerous in many (but the karyorelictids (see my class 1). not suctorian) species; suctorians also atypical in Anigsteinia, Ascobius, Avelia, Blepharisma, other ways: polystomic with sucking tentacles, non- Brachonella, Caenomorpha, Clevelandella, Climaco- ciliated trophic stage carnivorous, commonly stomum, Condylostoma, Epalxella, Fabrea, Fol- stalked, reproduction by budding; chonotrichs liculina, Geleia, Lagotia, Licnophora, Metopus, likewise specialized: heteromerous macronucleus Mylestoma, Nyctotheroides, Nyctotherus, Paracichli- but no nematodesmata, sessile forms (ectosymbionts dotherus, Peritromus, Phacodinium, Protocruzia, on crustaceans), limited ciliation, reproduction by Reichenowella, Saprodinium, Sicuophora, Spiros- budding. Three subclasses with several orders. tomum, Stentor, Transitella Acineta, Ancistrocoma, Brooklynella, Chilodochona, Chilodonella, Chlamydodon, Cyathodinium, Subclass 2. Spirotrichia Butschli, 1889 Dendrocometes, Dendrosoma, Dysteria, Endos- The classically known oligotrichs s.l. (i.e. oligotrichs phaera, Ephelota, Hcirtmannula, Heliochona, Helio- s.s. + tintinnids s.l. = today's choreotrichs) and the phrya, Hypochona, Isochona, Lobochona, Lorico- old hypotrichs s.l. (i.e the pre-1980 stichotrichs and phrya, Lwoffia, Lynchella, Ophryodendron, Pciraci- sporadotrichs). neta, Phalacrocleptes, Phascolodon, Podophrya, Amphisiella, Aspidisca, Australothrix, Bakuella, Cir- Raabella, Rhabdophrya, Sphenophrya, Spirochona, rhogaster, Codonella, Cyrtostrombidium, Diophry- Stylochona, Tachyblaston, Thecacineta, Tokophrya, opsis, Diophrys, Discocephalus, Euplotes, Favella, Trichochona, Trichophrya, Trochilia, Vasichona Gastrostyla, Halteria, Kahliella, Kerona, Kiitricha, Laboea, Lamtostyla, Leegaardiella, Lohmanniella, Class (5) Nassophorea Small & Lynn, 1981 Nolaclusilis, Onychodromus, Oxytricha, Pelagohal- Characterized by common possession of highly dis- teria, Pelagostrombidium, Plagiotoma, Strobilidium, tinctive "nasse" or cyrtos in cytopharyngeal area; Strombidium, Stylonychia, Territricha, Tintinnopsis, hypostomial frange prominent or reduced to few Tontonia, Tricoronella, Undella, Uronychia, pseudomembranelles; fibrous trichocysts; mostly Urosomoides, Urostyla, Wallackia, Xystonellopsis, free-living, fresh-water forms. Several orders, but Yvonniellina peniculines (e.g. Paramecium) are excluded (see 6th subclass of next class, below), leaving only (some of) Class (3) Colpodea Small & Lynn, 1981 the old cyrtophorids here. Somatic dikinetids, reticulate silverline system, and Furgasonia, Leptothorax, Microthorax, Nassula, somatic stomatogenesis; posterior kinetosome has Nassulopsis, Pseudomicrothorax, Scaphidiodon, well developed transverse microtubular ribbon ex- Zosterodasys tending posteriorly, forming LKm fiber by paralleling and overlapping with ribbons from more anterior Class (6) Oligohymenophorea de Puytorac et al., 1974 dikinetids; oral ciliature consists of right and left Somatic kineties, unless entirely absent, often com- ciliary fields; mainly terrestrial or edaphic forms. posed of monokinetids; buccal apparatus, when Two subclasses, second one solely for five small present, consists basically of paroral (formerly un- families; great bulk of the species are in the nominate dulating membrane, UM) dikinetid on right and subclass, which contains half a dozen orders. several membranelles or polykinetids (AZM) on left; Aristerostoma, Bresslaua, Bryometopus, Bryophrya, distinct, overlapping kinetodesmata; mucocysts com- Bursaria, Bursaridium, Colpoda, Cosmocolpoda, mon, with explosive trichocysts in some species. Six Cyrtolophosis, Grandoria, Grossglockneria, Haus- quite diverse subclasses warrant separate descriptions manniella, Kreyella, Maryna, Mycterothrix, here. Platyophrya, Pseudoglaucoma, Sorogena, Thylaki- dium, Trihymena, Woodruffia Subclass 1. Hymenostomatia Delage & Herouard, 1896 Class (4) Phyllopharyngea de Puytorac et al., 1974 Somatic monokinetids; right-most postoral kinety Cytopharynx lined with radially arranged leaf-like stomatogenic; buccal ciliature tetrahymenal (UM + microtubular ribbons (= phyllae), themselves typical- AZM). Two orders, second - the ophryoglenids - with

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a unique watchglass organelle and a complex life Opercularia, Ophrydium, Opisthonecta, Orboper- cycle as obligate histophagous symbionts. cularia, Pallitrichodina, Platycola, Polycycla, Bursostoma, Colpidium, Curimostoma, Espejoia, Propyxidium, Rhabdostyla, Scyphidia, Semi- Glaucoma, Ichthyophthirius, Jaocorlissia, Lambor- trichodina, Trichodina, Trichodinopsis, Urceolaria, nella, Monochilum, Ophryoglena, Tetrahymena, Vaginicola, Vorticella, Zoothamnium Turaniella

Subclass 2. Scuticociliatia Small, 1967 Subclass 5. Apostomatia Chatton & Lwoff, 1928 Paroral dikinetid in three distinct segments, with Ciliary rows typically spiraled, widely spaced or stomatogenesis via third and/or scutico-vestige; cilia- sometimes entirely missing; cytostome incon- tion usually sparse, with thigmotactic area anteriorly, spicuous (or absent), usually associated with unique caudal cilium posteriorly; mitochondria long and rosette; well-developed kinetodesmata; often poly- sometimes fused into huge chondriome. Convention- morphic life cycle, with most species ectosymbionts ally, three orders: the philasterids, the pleuro- (phoronts) on marine crustaceans. Three orders. nematids, and the totally symbiotic thigmotrichs. Ascophrys, Askoella, Chromidina, Collinia, Con- Ancistrum, Ancistrumina, Boveria, Cinetochilum, idiophrys, Cyrtocaryum, Eoettingeria, Gym- Cohnilembus, Conchophthirus, Cyclidium, Dexio- nodinioides, Hyalophysa, Opalinopsis Ophiurae- tricha, Dragescoa, Entodiscus, Eenchelia, Hemi- spira, Phtorophrya, Vampyrophrya speira, Histiobalantium, Hysterocineta, Loxocepha- lus, Miamiensis, Myxophthirus, Parauronema, Subclass 6. Peniculinia Faure-Fremiet in Corliss, 1956 Paurotricha, Peniculistoma, Philaster, Pleurocoptes, Buccal cavity contains paroral membrane, peniculi, Pleuronema, Proboveria, Ptychostomum, Schizo- and quadrulus; oral nematodesmata also present; calyptra, Thigmocoma, Thigmophrya, Uronema, somatic dikinetids; cortical alveoli distinct; explosive Urozona trichocysts; predominantly monomorphic, free- living, fresh-water microphagous forms. Assigned to Subclass 3. Astomatia Schewiakoff, 1896 the class Nassophorea (above) by some taxonomic Mouthless forms, endosymbionts mostly in annelids ciliatologists. (usually, but not exclusively, terrestrial oligochaetes) Clathrostoma, Disematostoma, Frontonia, Eem- but one group in amphibians and turbellarians; fre- badion, Marituja, Neobursaridium, Paramecium, quently with well developed cortical endoskeleton, Stokesia, Urocentrum, Wenrichia often with elaboration of some kind of holdfast or- ganelle at anterior end of body. Two or three orders. Class (7) Prostomatea Schewiakoff, 1896 Anoplophrya, Buetschliella, Cepedietta, Clausilo- Mouth at or near anterior end of body, with relatively cola, Contophrya, Durchoniella, Haptophrya, Hopli- simple oral ciliature; usually somatic monokinetids; tophrya, Intoshellina, Lomiella, Maupasella, Radio- nematodesmata form rhabdos; toxicysts common; a phrya, Steinella brosse characteristic of most species. Two orders, Prostomatida Schewiakoff, 1896, and the much larger Subclass 4. Peritrichia Stein, 1859 Prorodontida Corliss, 1974. Many of the old rhab- Prominent oral ciliary field; somatic ciliature reduced dophorids are here, but some are in the following to telotrochal band; widely distributed forms, many class as well. The taxonomic place of a few genera stalked and sedentary (though others mobile), some is controversial. colonial, some loricate, all with aboral scopula; dis- Bursellopsis, Coleps, Helicoprorodon, Holophrya, persal typically by migratory larval form (= telo- Metacystis, Nolandia, Placus, Plagiocampa, troch); often with strongly contractile myonemes, Planicoleps, Prorodon, Pseudobalanion, Pseudo- body and/or stalk; fusion of micro- and macrocon- prorodon, Spathidiopsis, Tiarina, Urotricha, Vasicola jugants. Symbiotic mobiline species have distinctive denticulate ring on aboral surface of the body. Two orders. Class (8) Litostomatea Small & Lynn, 1981 Apiosoma, Astylozoon, Carchesium, Cothurnia, El- Relatively inconspicuous or non-specialized oral lobiophrya, Epistylis, Haplocaulus, Lagenophrys, ciliature; somatic monokinetids with two transverse

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microtubular ribbons; kinetodesmata short, non-over- Class (1) Perkinsidea Levine, 1978 lapping; oral ciliature derived from adjacent somatic Flagellated forms, typically with two unequal flagel- kinetids with transverse microtubular ribbons sup- la, but with most of apical complex organelles and porting cytopharynx, latter (in many species) sur- with cortical alveoli; large posterior vacuole with rounded by nematodesmata (= rhabdos). Some diverse inclusions; some species with dinoflagellate- species with toxicysts. Three or four subclasses with like trichocysts, some with contractile vacuoles; number of orders, including groups classically known parasites of oysters or predators on various other as haptorids, vestibuliferans/trichostomes, pleuros- protists. Two orders, one for each included genus. tomes, and entodiniomorphids. Balantidium is the Colpodella (syn. Spiromonas), Perkinsus only ciliate parasitic in humans. See also the com- ments under Prostomatea, above. Class (2) Gregarinidea Dufour, 1828 Actinobolina, Alloiozona, Amphileptus, Arach- Mature gamonts large, extracellular, exhibiting nodinium, Askenasia, Balantidium, Blepharocorys, syzygy, with production of essentially isogamous Bryophyllum, Chaenea, Cycloposthium, Cyclotri- gametes, but male gametes may be flagellated (with chium, Didesmis, Didinium, Dileptus, Enchelys, En- basal body of nine singlet instead of usual eukaryotic todinium, Gorillophilus, Isotricha, Lacrymaria, triplet microtubules); zygotes undergo meiosis and Lagynophrya, Lepidotrachelophyllum, Litonotus, sporogony within gametocystic membrane; trophonts Loxophyllum, Mesodinium, Ophryoscolex, Para- with mucron or epimerite; all species in digestive bundleia, Paraisotricha, Phialinides, Plagiopyla, tract or body cavity of invertebrates or lower chor- Pseudotrachelocerca, Pycnothrix, Quasillagilis, dates. Three or four orders recognized. Rhabdoaskenasia, Rhinozeta, Sonderia, Spathidium, Actinocephalus, Ancora, Caulleryella, Cos- Triadinium, Trichospira, Troglodytella, Vestibulon- tnetophilus, Diplocystis, Doliospora, Gonospora, gum Gregarina, Lankesteria, Lecudina, Monocystis, Ophryocystis, Porospora, Rhynchocystis, Schizocys- tis, Selenidioides, Selenidium, Siedleckia, Stepha- Phylum 9. APICOMPLEXA Levine, 1970 nospora, Stylocephalus, Uradiophora, Zygocystis

Unicellular endosymbionts or predators characterized Class (3) Coccidea Leuckart, 1879 by having, at some stage in life cycle, an apical Gamonts typically intracellular; female gamont be- complex typically composed of polar rings, rhoptries, comes macrogamete without division, syzygy micronemes, and usually a conoid; highly com- generally absent, microgametes many and with two pressed smooth-membraned cisternae (= alveoli) or three flagella having basal bodies ultimately with usually present in cell cortex of infective stage; sub- typical nine triplet microtubules; within oocystic pellicular microtubules and micropores common; membrane, zygote produces sporoblasts which, in flagella restricted (except in first class) to own membranes, produce two or more sporozoites; microgametes or missing entirely; mitochondrial cris- infective sporozoite invades host cell and, charac- tae tubular, much reduced, or even absent. Except for teristically, grows and divides to form multiple recent (and still bit disputed) addition of Perkinsus to merozoites capable of invading other host cells; even- phylum, the whole assemblage remains essentially tually, some merozoites develop into gamonts, repeat- identical to SPOROZOA Leuckart, 1879, the name ing cycle; highly resistant oocyst can survive outside now treated by many workers as a synonym of host body (e.g. in soil) for long time before ingestion APICOMPLEXA. Four classes, somewhat con- and continued development and invasion, typically, troversial, recognized here. Two classes proposed by of host's gut epithelial cells. Most species parasitologists (see Levine 1988) were subsequently monoxenous. Three orders (Eimeriida Leger, 1911 by used by Corliss (1991c) as "group" names: Conoidea far the largest) commonly recognized. for classes 2 and 3 (below), and Aconoidea for 4; to Adelea, Aggregata, Besnoitia, Caryospora, which he added Zoosporea for class 1. This is the Coelotropha, Cryptosporidium, Cyclospora, Diplo- third (and last: but see GLAUCOPHYTA?) phylum spora, Dobellia, Dorisiella, Eimeria, Frenkelia, of the "Alveolata" assemblage (others are the Goussia, Grellia, Haemogregarina, Hepatozoon, dinoflagellates and the ciliates: see above). Isospora, Karyolysus, Klossia, Klossiella, http://rcin.org.pl 18 J. O. Corliss

Lankesterella, Legerella, Sarcocystis, Schellackia, belong here, as well as the baffling symbiotic Blas- Selysina, Toxoplasma, Tyzzeria, Wenyonella tocysts (see comments on this genus under FUNGI), and the curious apseudopodial Luffisphaera. Class (4) Haematozoea Vivier, 1982 Acanthamoeba, Amoeba, Arcella, Balamuthia, Apical complex without conoid or conoidal rings and Cashia, Centropyxis, Chaos, Cochliopodium, Cucur- rudimentary in other features; mitochondria simple bitella, Difflugia, Flabellula, Hartmannella, Hydra- or absent entirely; motile zygote (= ookinete) moeba, Leptomyxa, Lesquereusia, Mayorella, penetrates vector-host's gut wall, producing Nebela, Netzelia, Paramoeba, Platyamoeba, Ros- numerous "naked" sporozoites which migrate to culus, Saccamoeba, Stereomyxa, Thecamoeba, lumen of salivary glands, ready for transmission to Trichamoeba, Trichosphaerium, Vannella, Vexillifera next definitive host; in formation of gametes, basal bodies contain nine singlet microtubules but single Class (2) Entamoebidea Cavalier-Smith, 1991 flagellum produced exhibits typical 9 + 2 pattern. All With lobose pseudopodia, single nucleus, etc., but species heteroxenous: merogony and formation of totally lacking mitochondria, peroxisomes, and gamonts in blood cells of vertebrates; maturation of hydrogenosomes; small, if any, Golgi bodies; no gametes, fertilization, and sporogony in gut of blood- flagella; intranuclear centrosome present only during sucking arthropods. mitotic prophase. Some workers have suggested that Order 1. Haemosporida Danilewsky, 1885 this seemingly primitive group of symbiotic amoebae Haemoproteus, Hepatocystis, Leucocytozoon, Plas- may (better) belong in the kingdom Archezoa. It is modium, Saurocytozoon not clear whether genera allegedly related to En- Order 2. Piroplasmida Wenyon, 1926 tamoeba (e.g. Endamoeba, Endolimax, lodamoeba) Anthemosoma, Babesia, Dactylosoma, Echinozoon, should be assigned here or in subclass 1, above. Theileria Dientamoeba - long placed in the family En- tamoebidae - is now known, of course, to be a flagel- Phylum 10. RHIZOPODA von Siebold, 1845 la-less member of the flagellate phylum PARABASALA (above). Non-flagellated (except for gametes of class 4), Entamoeba (plus any other genera?) unicellular or plasmodial phagotrophs lacking aerial sporangia; typically, pseudopodia serve in both Class (3) Filosea Leidy, 1879 locomotion and feeding; all non-photosynthetic Hyaline, filiform pseudopodia, sometimes branched forms, except for groups with endosymbiotic algae; and occasionally anastomosing; some species naked, Golgi bodies and mitochondria (generally with many with bottle-shaped tests. Several orders. tubular cristae) always present except in class 2 where Amphorellopsis, Centropyxiella, Chardezia, Chlamy- mitochondrial absence considered secondary; species dophrys, Cyphoderia, Euglypha, Gromia, Latero- typically uninucleate (some exceptions) and free- myxa, Nuclearia, Ogdeniella, Paulinella, Penardia, living (except for totally endosymbiotic forms of Pseudodifflugia, Sphenoderia, Trinema, Vampyrella small class 2 and very few scattered other species). Classically, phyla 10-12 sensu lato were combined Class (4) Granuloreticulosea de Saedeleer, 1934 under a super-taxon called the "Sarcodina". Granular, delicate, reticulate pseudopodia forming anastomosing networks; few species naked, others in Class (1) Lobosea Carpenter, 1861 single-chambered organic or calcareous test with no Pseudopodia lobose or somewhat filiform; body often alternation of generations, but great majority in tests naked, but also groups with tests (composed of or- (organic, agglutinated, or calcareous) of one to many ganic and/or inorganic materials, with single aper- chambers with reticulopodia protruding from aper- ture). Predominantly free-living forms in soil, fresh- tures and/or test wall perforations and with alternation water, or marine habitats, widely distributed. Two of haploid sexual and diploid asexual generations; subclasses and number of orders; but the class may known gametes uni- or biflagellated or amoeboid; be a polyphyletic assemblage. The genera Copro- uni- or multinucleate forms, with asexual generation myxa and Guttulinopsis (and some other former of some groups possessing dimorphic nuclei - one or mycetozoa proving difficult to assign) might also more larger somatic nuclei and usually numerous http://rcin.org.pl "User-friendly" Classification of the Protists 19

small generative nuclei, a heterokaryotic condition ally placed here, have been removed: the dimorphids reminiscent of that of ciliates; species phagotrophic to the Opalozoa (see above) and the ciliophryids to (although some with endosymbiotic algae) and prac- the Dictyochae (in kingdom Chromista, below). Class tically all marine, benthic forms; many more fossil 4 contains but one genus of unusual, small, biflagel- than contemporary genera described; class essentially lated marine forms possibly more closely related to composed of the foraminifers (Foraminiferea d'Or- certain members of the next phylum, RADIOZOA. bigny, 1826: see genera below), with additionally Familiar name and conventional understanding of included separate, but dubiously distinct, orders "the Heliozoa" maintained, although considerably Athalamida Haeckel, 1862 (e.g. Arachnula and refined over classical usage; still, some workers Biomyxa) and Monothalamida Haeckel, 1862 (e.g. might prefer to elevate all or some of my classes to Amphitrema, Lieberkuehnia, Microgromia). Several independent phyletic status. Classically, the heliozoa orders, numerous families, and many hundreds of s.l. and the radiozoa were combined under a super- genera (a few with living species listed below) of taxon called the "Actinopoda", based on their com- forams. Does Komokia (still) belong here? mon possession of axopodial pseudopodia. Allogromia, Ammodiscus, Ammonia, Boderia, Class (1) Actinophryidea Hartmann, 1913 Bolivina, Carterina, Discorbis, Elphidium, Glabra- Actinophrys, Actinosphaerium, Camptonema tella, Globigerinella, Guttulina, Hastigerina, Heterotheca, Iridia, Metarotaliella, Microglabratel- Class (2) Centrohelidea Kiihn, 1926 la, Myxotheca, Nonion, Ovammina, Patellinella, Acanthocystis, Actinocoryne, Cienkowskya, Gymnos- Planorbulina, Polystomella, Quinqueloculina, phaera, Hedraiophrys, Heterophrys, Raphidiophrys Rhizammina, Rosalina, Rotaliella, Saccammina, Class (3) Desmothoracidea Hertwig & Lesser, 1874 Schizammina, Schwagerina, Selenita, Sorites, Spiril- Clathrulina, Hedriocystis, Orbulinella lina, Spiroloculina, Textularia, Triloculina, Uvigerina Class (4) Taxopodea Fol, 1883 Class (5) Xenophyophorea Schulze, 1904 Sticholonche Relatively huge (up to 25 cm in diameter, although only ca. one mm in thickness) but little studied marine Phylum 12. RADIOZOA Cavalier-Smith, 1987 benthic protists with multinucleate plasmodial stage enclosed in branched-tube system which, in turn, is Typically spherical marine planktonic organisms, within agglutinated test; presumably with filose or often of large body size, characteristically having reticulose pseudopodia and biflagellated gametes. central capsule with pores; stiff axopodial Some 36 species described from dozen genera; exact microtubules never in spiral pattern; endoskeleton rank of taxon and its placement among other protists either siliceous or of strontium sulfate, in latter case remains uncertain. with radially arranged spicules; unicellular, oc- Galatheammina, Psammetta, Stannophyllum casionally colonial; single nucleus in early vegetative stage, organisms often becoming multinucleate sub- sequently; some species produce biflagellated Phylum 11. HELIOZOA Haeckel, 1866 swarmer cells, not to be confused with symbiotic dinoflagellates often present. Based on numerous Unicellular phagotrophs with axopodia containing differences within the assemblage, phylum probably rigid microtubular axonemes; microtubules typically best divided into two subphyla, with two classes in arrayed hexagonally, often nucleating on envelope of the second much larger and more familiar group. nucleus; kinetocysts common; mitochondrial cristae typically tubular; trophic stage usually without flagel- Subphylum 1. Acantharia Haeckel, 1881 la; short filopodia in some species; several groups with stalks, one with perforated shell or test; mostly Class Acantharea Haeckel, 1881 fresh-water, some marine. Controversial whether four Acanthochiasma, Acantholithium, Acanthometra, classes named below are closely enough interrelated Amphilonche, Astrolonche, Astrolophus, Haliom- to warrant being clustered into one phylum; two other matidium, Lithoptera, Pleuraspis, Pseudolithium, taxa (of once-called "helioflagellates"), convention- Xiphacantha

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Subphylum 2. Radiolaria J. Müller, 1858 session of "spores" with polar filaments inside. Be- cause of their pericellular stages, and the similarity Class (1) Polycystinea Ehrenberg, 1838 (in development) of their polar capsules with Cenosphaera, Coccodiscus, Collosphaera, Col- cnidarian nematocysts, the MYXOZOA are placed lozoum, Halosphaera, Octodendron, Plagiacantha, in the Animalia by some taxonomists. Single class. Rhizosphaera, Spongodrymus, Thalassicolla, Tha- lassophysa Class Myxosporea Butschli, 1881 Ceratomyxa, Chloromyxum, Fabespora, Globo- Class (2) Phaeodarea Haeckel, 1879 spora, Henneguya, Hoferellus, Kudoa, Lomosporus, Atlanticella, Aulacantha, Aulosphaera, Aulotractus, Myxidium, Myxobolus, Myxoproteus, Ortholinea, Castanella, Challengeria, Challengeron, Coelo- Parvicapsula, Sinuolinea, Sphaeromyxa, Sphaero- dendrum, Conchopsis, Halocella, Medusetta, spora, Trilospora, Unicapsula, Unicauda, Wardia, Phaeodina Zschokkella

Phylum 13. MYXOZOA Grasse, 1970 Phylum 14. ASCETOSPORA Sprague, 1978

Symbiotic forms with valved multicellular spores Endosymbionts of (mainly) marine invertebrates, having polar capsules with extrusible filaments; spores unicellular or with production of cells trophic stages amoeboid (binucleate sporoplasm) or (sporoplasms) within cells; no polar capsules or fila- plasmodial (multinucleate); no flagellated stage; ments; no flagellated stage in life cycle; mitochondria with tubular to irregular-shaped cristae; mitochondrial cristae tubulo-vesicular; unique somatic and generative nuclei somewhat reminiscent haplosporosomes characteristic of most included of condition in ciliates, some foraminifereans, and species. Small but perhaps polyphyletic assemblage some radiolarians; commonly coelozoic or histozoic requiring more study; here it is tentatively considered in marine and fresh-water fishes, but a number of to embrace one or both of the groups Paramyxidea fresh-water species are found in body cavity or intes- Chatton, 1911 and Marteiliidea Desportes & tinal epithelium of aquatic oligochaetes, probably Ginsburger-Vogel, 1977 (as well as the haplo- undergoing an alternate stage in full life cycle of sporidians proper), without giving them specific fresh-water fish symbionts. Assemblage contains a ranks. Nephridiophaga no longer here (Lange 1993)? number of orders; but conventional breakdown into two major groups, Myxosporidia Butschli, 1881 and Class Haplosporidea Caullery & Mesnil, 1899 Actinomyxidia Stole, 1899, has recently become Haplosporidium, Marteilia, Minchinia, Paramar- highly suspect because of findings, confirmed ex- teilia, Paramyxa, Urosporidium perimentally, that some forms formerly assigned to each are only stages in the life cycle of single myxosporidian species that seem to require two hosts. Phyla of Kingdom CHROMISTA Tetractinomyxon sipunculid symbiont, may survive by transfer to a myxosporidian order. No ac- Four subkingdoms are recognized here in apprecia- tinomyxidian generic names are listed below since, tion of significant differences among members of often being of more recent date than myxosporidian their included taxa. Some workers may prefer com- ones and/or legally possibly only "collective" names, pletely independent status for these four groupings, they may well be suppressed in future taxonomic but the last three are relatively very small and are works (Kent et al. 1994). Phylum contains several probably best treated as I have done below; at least, orders; but I consider the enigmatic Helicosporidium they ought to be appended in some way to the of the literature, sometimes placed here, to be a Chromista until/unless further comparative data member of the kingdom Fungi. Classically, the clearly indicate otherwise. The general relationship myxosporidians s.l. and the microsporidians (see of the informal group of "stramenopiles" (Patterson kingdom Archezoa) were lumped together under the 1989a) to this kingdom is considered in my DISCUS- name "Cnidosporidia", based on their common pos- SION section.

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Subkingdom (I) HETEROKONTA Luther, 1899 Phylum 3. DICTYOCHAE Haeckel, 1894

Essentially with characters of the kingdom sensu Mixture of pigmented and non-pigmented stricto: organisms with chloroplasts (unless secon- heterokonts, free-swimming or stalked, marine and darily lost) located within rough endoplasmic fresh-water habitats; often with anteriorly directed reticulum instead of free in cytosol, and with mas- tentacles; one apically inserted flagellum typically tigonemes (unless flagella lost) as rigid, tripartite, with two rows of tripartite mastigonemes and some- tubular hairs, on one or both flagella, functioning in times small scales; second flagellum often reduced to thrust reversal. Bulk of the chromist species belong basal body; some species (silicoflagellates, mostly to phyla of this well-established and nearly univer- marine fossil forms) with complex basket-shaped sally accepted major taxonomic assemblage of "the external siliceous skeleton. Two classes. The second, heterokonts": the name - in one form or another (e.g. whose members have long been studied by some workers call it the HETEROKON- phycologists, is here credited to Kristiansen (1990), TOPHYTA) - and the concept are both deserving of although Cavalier-Smith (1986) had also established preservation. it as a class some four years earlier and Mohn (1984) and Karpov (1990) have both independently con- sidered it as a new class (and a new phylum as well!). Phylum 1. BICOSOECAE Cavalier-Smith, 1989 The pedinellids s.l., which include some of the "helioflagellates" (see Davidson 1982) of the litera- Small, free-living, fresh-water or (few) marine, ture, may be polyphyletic; Cavalier-Smith (1993c) planktonic biflagellated (one flagellum with mas- has at least partially relieved that condition by remov- tigonemes), heterotrophic non-pigmented forms typi- ing Oikomonas to a separate class of its own, although cally living in loricae (attached by the second, smooth I have not done so here. Some workers vernacularly flagellum), and feeding on bacteria; some stalked, refer to (some or all of) the pedinelleans (or pedinel- some form colonies. lophyceans) as actinomonads.

Class (1) Silicoflagellatea Borgert, 1891 Class Bicosoecidea Grasse & Deflandre, 1952 Dictyocha (only genus with living species) Bicosoeca, Cafeteria, Pseudobodo Class (2) Pedinellea Kristiansen, 1990 Actinomonas, Ciliophrys, Oikomonas, Parapedinel- Phylum 2 LABYRINTHOMORPHA la, Pedinella, Pseudopedinella, Pteridomonas Page in Levine et al., 1980 Phylum 4. RAPHIDOPHYTA Chadefaud, 1950 Non-pigmented protists, trophic stage with ectoplas- mic network of spindle-shaped or spherical non- Biflagellated forms with or occasionally without amoeboid cells that move by gliding within network; plastids, fresh-water and marine; motile or palmelloid unique cytoplasmic organelles, bothrosomes (first unicells; Golgi bodies in ring, over anterior surface described as sagenetosomes); tubular mitochondrial of nucleus; unique extrusome in many species. cristae; known zoospores biflagellated, one bearing Phylum is also known as "the chloromonads"; but this mastigonemes, other naked; in marine, generally is inappropriate, because Chloromonas is a genus of coastal, waters, often associated with, or ectosym- green algal protists in the kingdom Plantae. bionts of, aquatic angiosperms and certain algal protists. Class Raphidomonadea Chadefaud, 1950 Chattonella, Gonyostomum, Heterosigma, Mero- Class (1) Labyrinthulea Cienkowski, 1867 tricha, Olisthodiscus, Vacuolaria Labyrinthula Phylum 5. PHAEOPHYTA Wettstein, 1901 Class (2) Thraustochytriacea Sparrow, 1943 Aplanochytrium, Labyrinthuloides, Thraustochy- Photosynthetic heterokonts predominantly with trium chlorophylls a plus c and leucosin and fat (or para-

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mylon, glucose, or laminarin) as storage products; Class (6) Xanthophyceae Allorge in Fritsch, 1935 often siliceous scales covering body; charac- (syns. Heterochloridea Pascher, 1912 p.p., teristically, a pair of flagella with anteriorly project- Tribophyceae Hibberd, 1981) ing one bearing rigid tubular mastigonemes; some Botrydiopsis, Brachynema, Bumilleriopsis, loricate species; many fresh-water forms with distinc- Gloeobotrys, Gloeopodium, Heterogloea, Mal- tive statospore; other groups almost entirely marine lodendron, Ophiocytium, Pleurochloris, Reticulos- (e.g. brown algae); diverse morphological types: phaera, Tribonema, Vaucheria unicellular (some amoeboid), colonial, filamentous or thalloid (multicellular); sizes small to very large (brown seaweeds, kelp, up to 60 meters in length). Phylum 6. DIATOMAE Agardh, 1824 Entire assemblage is essentially the golden-brown (plus some yellow-green) algae of the literature Pigmented unicells (occasionally colonial) with minus diatoms, silicoflagellates, and haptophytes but secreted silica frustule consisting of two valves and including the browns and eustigmatophytes (although one or two girdle bands; non-flagellated except for latter without chlorophyll c, usually possess but single posterior flagellum on microgametes of one single flagellum, and eyespot independent of group (gametes of other groups amoeboid); yellow- chloroplast). Conservatively, I include six major clas- brown plastids; mainly planktonie forms widespread ses, which contain a number of orders and numerous in fresh-water and especially marine habitats, with genera and species; but additional classes may be numerous fossils; some species in moist soils. Many justified (e.g. for Reticulosphaera and Vaucheria, in thousands of diatoms have been described, usually as class 6 below). Zoologists have traditionally claimed belonging to the botanical division conventionally a number of motile chrysomonads s.l. as members of known as BACILLARIOPHYTA Engler & Gild, the "old" Protozoa, assigning them mostly to a single 1924, and assigned to two major distinct groups order (Chrysomonadida Engler, 1898). (centric and pennate); but at least three classes (Cos- cinodiscophyceae Round & Crawford, 1990; Class (1) Phaeophyceae Kjellman, 1891 Fragilariophyceae Round, 1990; Bacillariophyceae (syns. Melanophyceae Rabenhorst, 1863, Haeckel, 1878) are now recognized, with numerous Fucophyceae Warming, 1884) subclasses and orders plus several hundred genera Alaria, Arthrocladia, Chordaria, Costaria, Cys- (Round et al. 1990). toseira, Dictyota, Ectocarpus, Fucus, Gijfordia, Achnanthes, Amphipleura, Amphora, Auricula, Homosira, Laminaria, Litosiphon, Macrocystis, Bacillaria, Bacteriastrum, Biddulphia, Coscinodis- Myrionema, Sargassum, Scytosiphon, Sorocarpus, cus, Cyclophora, Cyclotella, Cylindrotheca, Sporochnus, Stilopsis, Streptophyllum, Utriculidium, Cymatopleura, Cymbella, Diadesmis, Diatoma, Xiphophora, Zonaria Fragilaria, Frustulia, Grammatophora, Gyrosigma, Class (2) Chrysophyceae Pascher, 1914 Hanzschia, Hemidiscus, Hydrosilicon, Lennoxia, Lic- Anthophysa, Chromulina, Chrysamoeba, Chryso- mophora, Lithodesmium, Lyrella, Melosira, Minuto- capsa, Chrysococcus, Chrysodendron, Dermato- cellus, Navicula, Nitzschia, Odontella, Pleurosigma, chrysis, Dinobryon, Epipyxis, Hibberdia, Podosira, Rhizosolenia, Stephanodiscus, Sticho- Microglena, Monochrysis, Ochromonas, Poterio- chrysis, Thalassionema, Thalassiosira, Toxarium, ochromonas, Rhizochromulina (maybe better in class Trice ratium 4?), Sarcinochrysis, Spumella, Triparma, Uroglena

Class (3) Synurophyceae Andersen, 1987 Phylum 7. PSEUDOFUNGI Cavalier-Smith, 1986 Mallomonas, Mallomonopsis, Synura, Tesselaria

Class (4) Pelagophyceae Andersen & Saunders, 1993 Osmotrophic, minute symbionts on other protists and Pelagococcus, Pelagomonas aquatic plants or in hosts ranging from grapes and potatoes to fishes; in fresh-water (mostly) or marine Class (5) Eustigmatophyceae Hibberd & Leedale, 1970 habitats or in soil; bi- or u ni flagellated zoosporic Chlorobotrys, Eustigmatos, Monodopsis, Nan- stage; uninucleate or coenocytic walled protoplast in nochloropsis, Pseudocharaciopsis, Vischeria vegetative stage. Long conventionally considered as

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a class in the kingdom FUNGI along with the chytrid Phylum HAPTOMONADA Cavalier-Smith, 1989 protists, which do belong there. Synonymous names for the group include OOMYCOTA Dick, 1990 and With characters of subkingdom. Essentially PSEUDOMYCOTA Barr, 1992. The latter name, synonyms for the name of (most of) the assemblage like PSEUDOFUNGI, is also attractive in emphasiz- are COCCOLITHOPHORA Lemmermann, 1903, ing the pseudo-fungal characters of these heterokont and PRYMNESIOPHYTA Casper, 1972 (latter protists, which are quite unlike the so-called name generally credited to "Hibberd, 1976", where "Eumycota" or true fungi. Two classes are recog- first Latin diagnosis is to be found). Contains two nized. classes: first (Pavlovea Cavalier-Smith, 1986) for the allegedly primitive genus Pavlova; second (Patel- liferea Cavalier-Smith, 1993) for all other genera (a Class (1) Oomycetes Winter in Rabenhorst, 1879 few of which are given below). If future ultrastruc- Zoospores typically with two flagella, anterior one tural and molecular studies show still greater dif- with two rows of rigid mastigonemes, posterior ferences compared with the Chromista proper, as- smooth or with only fine flexuous hairs; cytoplasmic semblage can be redefined and elevated to separate and nucleus-associated microtubules. kingdom or assigned elsewhere (e.g. to the Protozoa, Achlya, Albugo, Brevilegnia, Lagenidium, Lep- where it was at one time included in an order Coc- tomitus, Myzocytium, Olpidiopsis, Peronos- colithophorida). clerospora, Peronospora, Phytophthora, Pythium, Calciosolenia, Canistrolithus, Chrysidalis, Chryso- Rhipidium, Saprolegnia, Sclerospora, Verrucalvus, chromulina, Coccolithus, Emiliania, Isochrysis, Zoophagus Ophiaster, Phaeocystis, Pleurochrysis, Prymnesium, Umbilicosphaera Class (2) Hyphochytriomycetes Sparrow, 1959 Zoospores with single, anterior flagellum (with mas- tigonemes); cytoplasmic and nucleus-associated Subkingdom (III) CRYPTOPHYTA Pascher, 1914 microtubules absent. Following recent convention, I have dropped the "id" originally in the class name Group of protists mostly photosynthetic, unicellular, between the "tr" and the "io". and motile (biflagellated, with bipartite mas- Anisolpidium, Hyphochytrium, Rhizidiomyces tigonemes generally on both); usually paired thylakoids, chlorophylls a and c, and two phycobilins; unique features: nucleomorph, ejectosome, and Subkingdom (II) HAPTOPHYTA Christensen, 1962 periplast; mitochondrial cristae flattened; distinct gul- let; chloroplast endoplasmic reticulum typically Typically photosynthetic unicellular biflagellated present; fresh-water and marine habitats. By protists characterized principally by possession of a zoologists at one time considered an order, Cryp- haptonema, unique filiform appendage located be- tomonadida Senn, 1900, of the "old" Protozoa. tween anteriorly arising flagella, often very long (sometimes coiled) and containing 6-8 singlet Phylum CRYPTOMONADA Ehrenberg, 1838 microtubules; atypical of kingdom, neither flagellum bears tubular mastigonemes; commonly two parietal With characters of subkingdom. Contains two clas- plastids, each with single pyrenoid; chloroplast en- ses: first (Goniomonadea Cavalier-Smith, 1993) for doplasmic reticulum present; with rare exception, allegedly primitive forms (e.g. phagotrophic body covered by layers of small organic scales in turn goniomonads); second (Cryptomonadea Stein, often covered by large unmineralized scales (coc- 1878) for all others. As in the cases of subkingdoms coliths) on which calcium carbonate crystallized as II (above) and IV (below), future molecular data may calcite or aragonite; single Golgi body, fan-shaped indicate a different phylogenetic/taxonomic place- near anterior end of cell; mitochondrial cristae ment for this assemblage. tubular; mostly marine, few fresh-water; a few Chilomonas, Chroomonas, Cryptomonas, Gonio- species form colonies, and a few exhibit phagotrophy; monas, Hemiselmis, Pyrenomonas, Rhinomonas, many fossil forms. Rhodomonas http://rcin.org.pl 24 J. O. Corliss

Subkingdom (IV) CHLORARACHNIOPHYTA taxa of protists, the green algae s.l. (but excluding Hibberd & Norris, 1984 entirely the unrelated euglenoids of the kingdom Protozoa), are unicellular (generally biflagellated, Marine photosynthetic protists with amoeboid plas- without tubular mastigonemes), colonial, or filamen- modial vegetative stage, with individual cells linked tous (multicellular), many without motile vegetative by fine filopodia; uniflagellated zoospore (thus = an stages; all with starch-containing plastids bounded by amoeboflagellate?) with its flagellum, coiled helical- an envelope of two membranes; unmineralized scales ly around cell body, bearing delicate mastigonemes; on bodies or flagella of many species; found mitochondrial cristae tubular; chlorophyll a and b but predominantly in fresh-water habitats, but some en- no c nor phycobilins; outermost membrane around tire groups marine. Modern phycologists are of chloroplast lacking ribosomes on cytosolic face; diverse opinions concerning the exact num- complex extrusomes. bers/names of high-level taxa (phyla/divisions, clas- ses/subclasses) to be included here: four phyla are Phylum CHLORARACHNIOPHYTA endorsed below. As mentioned above, the non-protist Hibberd & Norris, 1984 phyla of the VIRIDIPLANTAE (i.e. the "higher" or "land" plants, bryophytes and tracheophytes) are With characters of subkingdom. Contains single beyond consideration in this paper. class, Chlorarachniophyceae Hibberd & Norris, 1984. Taxonomic position of the organism remains Phylum 1. PRASINOPHYTA Christensen, 1962 somewhat controversial, as well as the most ap- propriate name, authorship, and date for it at the The "grass-green scaly algae" (and close relatives), various supraordinal levels. Tentatively, I am using typically small biflagellated unicells, presumably the identical name for the subkingdom and phylum most primitive group among plant protists; organic here. Single species? And no closely related (other) scales, with rare exceptions, on body and/or flagella; genera? generally no cell walls; often unique extrusomes. Chlorarachnion Class (1) Pedinophyceae Moestrup, 1991 Phyla of Kingdom PLANTAE No scales; second flagellum represented by only its basal body. Two genera. The non-protist plant phyla (viz. BRYOPHYTA, Pedinomonas, Resultor PTERIDOPHYTA, SPERM ATOPHYTA) are beyond the scope of this paper, so they are not further Class (2) Prasinophyceae Christensen, 1962 considered here. The protists of the kingdom are (syn. Micromonadophyceae Mattox & Stewart, divided into two groups at the high level of sub- 1984) kingdom, the first - and much larger - assemblage Essentially with general characters of phylum s.s. containing the green algae of the literature (along Three orders recognized. In the past, some species with the "higher" plants proper, which clearly evolved have been considered members of the "old" Protozoa from them) and the second the taxonomically enig- by zoologists. matic red algae plus, possibly, the even more refrac- Bathycoccus, Dolichomastix, Mamiella, Mantoniella, tive glaucophytes. Further research may yield addi- Mesostigma, Micromonas, Nephroselmis, Pseudo- tional data that will make untenable these proposed scourfieldia, Pterosperma, Pyramimonas, Scourfiel- "taxonomic marriages"; in which case, appropriate dia, Tetraselmis classificational alterations can easily be made. Phylum 2. CHLOROPHYTA Pascher, 1914 Subkingdom (I) VIRIDIPLANTAE Cavalier-Smith, 1981 The "green algae" s.s. of the literature; many non- motile species; motile ones usually bi- or quadriflagel- Typically photosynthetic organisms with chloro- lated, walled or naked; morphological types include phylls a and b and flattened mitochondrial cristae; unicellular or colonial, tetrasporal, coccal, sarcinoid, cellulosic cell walls common. Species of included filamentous, and parenchymatous. Single class

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(Chlorophyceae Wille in Warming, 1884) with per- bers of this first class possess phragmoplast similar haps a dozen separate orders. Traditionally, zoologists to that of "higher" plants, and their cellulosic cell have claimed a number of motile species (outstanding walls sometimes heavily calcified. Species of second examples, Volvox and Chlamydomonas) as protozoa, class, with no flagellated stages in life cycle, show assigning them to the order Volvocida France, 1894 unique conjugation between cells (alone or of closely (replacing the highly inappropriate name appressed filaments), with fusion of amoeboid Phytomonadida Blochmann, 1895, since Phytomonas gametes; in the essentially mirror-image unicellular is in the protozoan class Kinetoplastidea). desmids, a pair of large, complex plastids are joined Aphanochaete, Botryococcus, Carteria, Chaeto- at an isthmus that contains a single shared nucleus; chloris, Chlamydomonas, Chlorella, Chlorococcum, cellulosic cell walls often slimy, organisms gliding Chlorogonium, Chloromonas, Coccomyxa, Coela- on the secreted mucilage. Evolutionarily, members strum, Dunaliella, Eudorina, Fritschiella, Gloeocys- of the first class are considered directly ancestral to tis, Gonium, Haematococcus, Hydrodictyon, Micro- "higher" plants. Some taxonomic phycologists have spora, Nanochlorum, Nautococcus, Palmodictyon, separated the two groups named below at phylum Pascherina, Pediastrum, Phacotus, Pleodorina, (division) rather than class level. Pleurastrum, Polytomella, Prasiola, Protosiphon, Scenedesmus, Schizomerus, Selenastrum, Sphaero- Class (1) Charophyceae Rabenhorst, 1863 plea, Stephanosphaera, Tetraspora, Tetrasporidium, With characters given above for the first class. Trebouxia, Trentepohlia, Treubaria, Trichophilus, Vol- Chaetosphaeridium, Chara, Chlorokybus, Coleo- vox, Yamagishiella chaete, Klebsormidium, Nitella, Nitellopsis, Raphido- nema, Stichococcus, Tolypella Phylum 3. ULVOPHYTA Stewart & Mattox, 1978 Class (2) Conjugatophyceae Engler, 1892 Most species macroscopic seaweeds (including "sea With characters given above for the second class. The lettuce") from tropical marine waters; sessile with larger group, mostly because of huge number o walled vegetative cells, thalli typically coenocytic or described desmids. Essentially synonymous names multicellular; bi- or quadriflagellated reproductive include "Conjugaphyceae", Gamophyceae, Zyg- cells common; morphology ranges from sarcinoid nematophyceae, and Zygophyceae. and blade-like to siphonous. Single class (Ul- Ancylonema,Arthrodesmus, Closterium, Cosmarium, vophyceae Stewart & Mattox, 1978) and five orders Cylindrocystis, Desmidium, Micrasterias, Oocar- recognized. dium, Sirogonium, Spirogyra, Staurastrum, Xan- Acetabularia, Acrosiphonia, Blidingia, Bryopsis, thidium, Zygnema Chaetosiphon, CladophoraCladophora, Codium, Cymopohlia, Dasycladus, Eugomontia, Halimeda, Subkingdom (II) BILIPHYTACavalier-Smith, 1981 Phaeophila, Rhizoclonium, Siphonocladus, Tricho- sarcina, Ulothrix, Ulva, Valonia Essentially the "red algae" of the literature. Unlike other members of the kingdom PLANTAE in many Phylum 4. CHAROPHYTA Rabenhorst, 1863 respects, their species also show little similarity to other taxa of protists. Whether they are "algal plants", Some species multicellular, macroscopic, and found as considered here, or better treated as an independent submerged in shallow fresh-water habitats, a few kingdom is a matter for the future when additional terrestrial, but majority (including the ubiquitous des- relevant data become available. Mostly marine mids) unicellular or filamentous in fresh waters protists, some unicellular, others of macroscopic size everywhere; the larger species, some commonly (length) - latter, like many brown (and a few green) known as stoneworts, have macroscopic thalli with algae, called seaweeds; particularly distinguished by main axis erect plus regular whorls of lateral total absence of centrioles and flagella and by branches, and with male and female sex organs presence of single thylakoids in their chlorophyll a reminiscent of those of land plants: these charophytes containing plastids with phycobilins as accessory have motile (flagellated) swarmers, never with photosynthetic pigments; mitochondria with flattened eyespot, typically covered with scales; many mem- cristae; starch stored in cytosol; often complex life http://rcin.org.pl 26 J. O. Corliss

histories. Some workers accept - as a second phylum parasitologists and medical clinicians without ques- of the BILIPHYTA, in addition to the RHODO- tion for over half a century. Recently, it has been PHYTA - the enigmatic and possibly non-mono- (re)classified as a sporozoon (Apicomplexa), a phyletic GLAUCOPHYTA Bohlin, 1901 (single lobosean amoeba (Rhizopoda), an "uncertain protist", class, Glaucophyceae Bohlin, 1901, with genera and a unique organism requiring a new phylum Cyanophora, Glaucocystis, Glaucosphaera, Gloeo- (named as a "protozoan subphylum": Blastocysta chaete). Glaucophytes are small, fresh-water, Jiang & He, 1993) of its own, but with some workers cyanelle-containing protists commonly with a pair of still considering it a fungus. See Belova (1992), flagella in their life cycle, cortical alveoli (curious- Boreham and Stenzel (1993), Garavelli and Libanore ly!), etc., sharing some characters with red algae (e.g. (1993), Jiang and He (1993), Johnson et al. (1989), possession of phycobiliproteins). The cyanelles are Zierdt (1988, 1993), and references within those presumably evolutionarily derived from blue-green papers. I favor assignment to, or near, the rhizopod algae (i.e. endosymbiotic cyanobacterial prokaryotes) class Lobosea (q.v.), at an undetermined rank, until on their way to becoming genuine plastids in more comparative data of phylogenetic significance glaucophytes and probably in several other taxa of are available on this taxonomically defiant organism. protists as well). Phylum CHYTRIDIOMYCOTA Sparrow, 1959 Phylum RHODOPHYTA Rabenhorst, 1863 Protists with definite fungal affinities: non-pigmented Essentially with characters of subkingdom, as given forms (some filamentous) with chitinous cell walls in above. Some workers recognize two principal clas- hyphal stage, flat mitochondrial cristae, absorptive ses: the more primitive and much smaller group, the mode of nutrition, symbionts or saprobes in soil or Bangiophyceae Wettstein, 1901; and the widespread, fresh-water habitats; atypical of (the majority of) the multicellular, much larger group, the kingdom, however, are such characteristics as their Florideophyceae Warming, 1884. Numerous orders motile stages in life cycle (most gametes and some have been described. asexual zoospores) with posteriorly directed single Audouinella, Bangia, Bangiopsis, Batrcichospermum, (rarely multiple) flagellum (without mastigonemes or Boldia, Callocolax, Capreolia, Chondrus, Com- scales), frequent unicellularity, and possession of psopogon, Cyanidium, Dilseci, Endocladia, Erythro- unusual cytoplasmic structures in many species (e.g. trichia, Gigartina, Goniotrichum, Gracilaria, distinctive flagellar root system and the curious rum- Halymenia, Heteroderma, Hildenbrandia, Iridaea, posome in members of two orders). The chytrids s.l. Eithophyllum, Mesophyllum, Minium, Naccaria, Pal- differ significantly from members of the phylum maria, Phragmonema, Phyllophora, Porolithon, Por- PSEUDOFUNGI (q.v.), heterokonts of the kingdom phyridium, Rhodella, Rhodochaete, Rhodophyllis, Chromista. Rhodospora, Sporolithon, Thorea, Zymurgia Class Chytridiomycetes Sparrow, 1959 Phyla of Kingdom FUNGI With characters of phylum. Four orders recognized. Allomyces, Blastocladiella, Callimastix, Catenaria, The non-protist fungal phyla (viz. ASCOMYCOTA, Chytridium, Chytriomyces, Coelomomyces, Karlin- BASIDIOMYCOTA, ZYGOMYCOTA) are gia, Monoblepharella, Neocallimastix, Olpidium, beyond scope of this paper, so are not treated here. Physoderma, Rhizophydium, Spizellomyces, Synchy- They embrace "typical" fungal forms, the Fungi Im- trium perfecta unicellular yeasts, and probably also the enigmatic "protozoon" Helicosporidium and the Phyla of Kingdom ANIMALIA taxonomically notorious Pneumocystis (but see note of caution by Frenkel et al. 1990). Blastocystis, a Since none of the many phyla of animals - in my common intestinal symbiont of many vertebrates in- opinion - contains any protist species, they are beyond cluding humans, was first discovered and described our consideration here. But, from time to time, spon- more than 75 years ago as a "vegetable organism" (= ges (if one classifies the choanozoa there) have rep- fungus), a taxonomic conclusion accepted by resented a possible exception. And, very recently, http://rcin.org.pl "User-friendly" Classification of the Protists 27

Cavalier-Smith (e.g. 1993c) has suggested that the considerably elevated over the years (especially in multicellular, ciliated MESOZOA, with (usually) recent decades), the numbers of their species have in- tubular mitochondrial cristae and lack of collagenous creased dramatically over time with advances in micros- connective tissue, should be removed from the copy, and the contents and boundaries of the assemblage Animalia to the protistan kingdom Protozoa. This have often changed with our increased understanding of taxonomic shift has not been endorsed, however, in them. the present paper. Some place the myxozoa here. Some 15-20 years ago (see historical account in Corliss 1986a), the "protist revolution" began to per- meate the thinking of the biological scientific com- DISCUSSION munity. In due time, it became unfashionable to retain a phylum or subkingdom (of "animals") called the As inferred in the INTRODUCTION and manifest Protozoa in light of our new appreciation of inter- throughout the preceding pages of classification, relationships among (former) algal and protozoan biologists can no longer think of protozoa or protists as groups, an intermingling that finally forced the break- conveniently divisible into separate taxa based on down of the old plant/animal barriers in taxonomy. A general characteristics such as modes of locomotion or neoHaeckelian kingdom Protista helds way, as it does types of nutrition. In other words, no longer can there be still today in many circles. Round (1980) perceptively named high-level taxonomic groups containing, for ex- realized that we were going too far in discarding genuine ample, only forms with pseudopodia or with flagella or differences between many algal and protozoan taxa, but with chloroplasts or with a totally symbiotic style of life. his warning was not heeded at the time. Our attempts to erect "natural" systems of classification With the emphasis on broad phylogenetic lines and have now moved far beyond that stage, thanks primarily the desire to break completely with the past, most protis- to the availability of more sophisticated ways of studying tologists failed to realize what we know today (but some the properties/characteristics of these generally unicel- still find difficult to accept), that the Protista are too lular and microscopic "lower" eukaryotes. diverse to remain as a single taxonomic entity and that There is no need (nor space!) to discuss all parts of some older concepts, properly refined, need not remain the preceding classification scheme in any detail here. discarded. The Protozoa represent an outstanding ex- It is clear that the general basis or rationale for arranging ample of this. As Cavalier-Smith (1993c, in particular) the taxa as I have done is the degree to which various has resurrected the group - as a kingdom PROTOZOA groups do, or do not, share key characters in common, - it deserves (re)acceptance, in my opinion (although a reflecting their phylogenetic affinities. Different ap- year ago I myself raised some objection to his choice of proaches or schools of thought have been mentioned in name for the new kingdom, while tacitly admitting that the INTRODUCTION; I consider myself an evolution- no better one came to mind: Corliss 1993). Its boun- ary biologist sensu Mayr (1990). Comments regarding daries have been sharpened by removal of several taxa various controversial taxonomic decisions have been formerly inappropriately assigned to it: for example, made in place on preceding pages. Here, I wish to focus groups that now reside, quite properly, in other attention on four matters that deserve additional ex- kingdoms. The ARCHEZOA represent a perfect haven planation or discussion: my choice of the names and for the primitive amitochondrial groups of certain concepts for the kingdoms PROTOZOA and amoebae, symbiotic flagellates, and the unique CHROMISTA; consideration of phylum and class microsporidians. The CHROMISTA embrace certain names in general (including authorships and dates); the algal protists (e.g. chrysophyceans s.l. and haptophytes) taxonomic category of "incertae sedis"; and my reasons totally different from the (former) algal groups of for supplying so many examples (so evident in the euglenoids and dinoflagellates (sensibly treated as INDEX as well as in the text) of included genera. protozoa now) but many of which were (also) once classified as protozoa. And the PLANTAE are the The Kingdom PROTOZOA proper place for the green algae, which harbor the ancestors of the "higher" plants but some of which were The Protozoa, united into a formal group of generally traditionally labeled, simultaneously, as protozoa (e.g. microscopic, unicellular, phagotrophic forms, have been Chlamydomonas, Volvox, and their close relatives: the around for 175 years. The rank accorded them has been "phytomonads" or, better, the volvocids).

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Thus cleansed or purged, the Protozoa have become identical to most members of large assemblages given a much more homogeneous, if, admittedly, still possibly different names (and slightly different boundaries) in paraphyletic, assemblage. They certainly resemble the the literature. The classically known heterokonts (Pas- old "phylum Protozoa" sufficiently enough to be recog- cher 1937-1939) represent one such group, and this nizable as the protozoa; in fact, many of the included name has been used by me for the major subkingdom taxa of old remain intact in the new kingdom Protozoa, of the Chromista. The Chromophyta of Bourrelly which is clearly separated from the other five eukaryotic (1957), perhaps the basis for the recently appearing kingdoms. That the group is a large and genetically names Chromobionta and Chromobiota, also includes diverse one is no reason in itself to require that it must many of the same groups and has been popular as a be broken up. As the evolutionary proving ground from contrast to the Chlorobionta (see Christensen 1966), a which emerged the other eukaryotic kingdoms (except name applied essentially to the green algae. for the primitive Archezoa), the Protozoa might be ex- Recently, the "stramenopiles" (more properly spelled pected to show greater variety and even to be taxonomi- "straminopiles"? See V0rs 1993) of Patterson (1989a) cally unwieldy in some respects. Not surprisingly, new have become, in effect, a rival nomenclatural candidate data may in time oblige us to make substantial revisions for the chromists of Cavalier-Smith (1986, 1989b). In among a number of its numerous subtaxa, outstanding both men's cases, the same strong synapomorphic char- examples - in my view - being several of the classes and acter has been used: the tripartite rigid tubular hairs or orders of two of Cavalier-Smith's (1993a-c) newest mastigonemes found on (or postulated to have been lost phyla, viz. Percolozoa and Opalozoa. from) the flagella of allegedly all species assignable to A final argument in favor of (re)recognizing the the overall group. This phylogenetically important fea- Protozoa as a major high-level taxonomic unit among ture, however, is missing from species comprising the eukaryotes is the fact that the concept underlying it several (but different) taxa in both Cavalier-Smith's and continues to satisfy the needs of field and bench eco- Patterson's suggested classifications. I accept Cavalier- logists, who have long defined the Protozoa as basically Smith's arguments - explaining the absences from his comprised of primarily heterotrophic and colorless (with several included taxa that are without them - as the more a few exceptions), motile, unicellular, mostly free- cogent ones. Thus, in brief, I agree with the latter worker living, microscopic protists widespread in a variety of in excluding Patterson's proteromonads + opalinids (= habitats. This is essentially the same general - and useful the "slopalinids") and the heliozoan actinophryids from - definition found for the old phylum Protozoa in many the (mostly phototrophic, with plastids inside the rough textbooks. And, as Cavalier-Smith (1993c) has pointed endoplasmic reticulum) chromistic assemblage, while out, protozoologists need not restrict their studies, or including the haptophytes, cryptophytes, and several even their textbooks, to members of this kingdom alone. other chromist taxa left out of the "stramenopiles" in In fact, our knowledge concerning the archezoan groups, Patterson's circumscription of his informal group. and other more widely dispersed protists classically The CHROMISTA is an important non-protozoan, thought of as "protozoa" and sometimes - at the same non-plant kingdom of algal protists. In contrast to the bulk time - "algae", will benefit from attention by students of the PROTOZOA, its members are mostly autotrophic and researchers working in any field of the biological (although many are capable of mixotrophy), unicellular sciences. forms with unique mastigonemes and a unique placement Unresolved taxonomic problems within the Protozoa of their chloroplasts. The chromists represent a major exist mostly in areas involving groups of small-sized group of "the algae" of old; and their heterokontic moiety free-living and symbiotic heterotrophic flagellates, looms large among the seven distinct phylogenetic algal which abound in a great diversity of habitats (Patterson lineages described by Andersen (1992) as having arisen and Larsen 1991), and various amoeboid and plasmodial independently during geological time. protists, especially taxa of mycetozoa s.l. and amoeboflagellates s.l. Names and Authorships of Higher Taxa

The Kingdom CHROMISTA In general, the various codes of biological nomencla- ture do not have much control over the choice of names In a number of important characteristics, the protists for suprafamilial taxa (Corliss 1984, 1993; Jeffrey 1990; assignable to my kingdom Chromista are similar or even Ride and Younes 1986). This may be considered both

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"good" and "bad", but the unchecked promulgation of number of quite unusual organisms (e.g. a single family new ranks and names in recent years has led us nearly or even a single genus or species), then I especially have to the brink of chaos in protistology, nomenclaturally tended to use the original name and authority for the speaking (see extended discussions in Corliss 1984, group even if the rank (usually upward) may have 1990, 1991b, 1993; Patterson and Larsen 1992). Some changed drastically. The description, while refined in time ago, I stressed the need for "common sense and light of new knowledge, is basically concerned with the courtesy" in the area (Corliss 1972), and Silva (1980) same organism(s). However, there are a few defensible has urged that an overriding consideration should be exceptions to this. "effectiveness of communication". A reasonable degree 3. In the preceding and still other situations, I have of stability is another (overlapping) goal certainly wor- taken the liberty of altering prefixes and/or suffixes thy of achievement in these times of perhaps too much without necessarily changing the authorship/date infor- emphasis on constant change. mation. In the case of a number of former botanical In the classification of the 34 phyla formally offered classes, I have - along with other workers - felt free to in this paper, I have been confronted by the same dilem- elevate the group to phylum (= division) status, altering mas described in my earlier overview work (Corliss the suffix appropriately. Also, I have not been con- 1984), and have thus been obliged to make a number of strained by the lack of a Latin diagnosis in the first (or quite subjective decisions in choice of both names and subsequent) description to withhold credit from the authorities for the higher taxa included. Space does not original creator/proposer of a group or of its name. This permit a detailed discussion here. Suffice it to say, in latter decision has affected the date of authorship and keeping with my objectives to present a "user-friendly" occasionally the authorities themselves in the case of scheme of classification including all groups of protists, some botanically derived names, as will be apparent in I have adopted the guidelines given below, keeping in the text and in Table 1. mind the practical observation made by Raabe (1964a) 4. According to conventional practices, a number of some 30 years ago: "I am not an adherer of introducing group-names might well have been marked "emend", new names for old taxa, although they might stress better "sensu", "ex", "nom. nov.", or "stat. nov." (with or their properties. It introduces confusion..." And Silva without additional author/date data), but, for the sake of (1980) has sensibly suggested that a classification consistency and simplicity, I have not done this. I offer should be one that is "familiar and acceptable to the apologies to nomenclatural purists and any offended largest number of users". taxonomic specialists. Today, it is generally assumed 1. When possible/defensible, I have employed the by taxonomists that for descriptions of organisms or oldest and/or most familiar name for a more or less groups of organisms one must go to the more recent conventional group of protists. Although the concept, rather than the older literature; in some ways, however, boundaries, composition, and even the rank-level may their nomenclature may be considered to be a separate have changed somewhat over time, the name used may matter - primarily one more of historical interest. be credited to the original author, using date of his 5.1 am not automatically opposed to all "new" names! creation of the name. As might be expected, sometimes For instance, I have endorsed/accepted some 20 of exceptions to this principle are advisable. Incidentally, Cavalier - Smith's numerous high-level taxonomic / no- to save space, I have not regularly listed all synonyms menclatural creations of the past dozen years. For a few of the names selected for the various high-level taxa examples of these neologisms (some of them altered endorsed on preceding pages. In a number of cases, slightly in this paper in rank or in spelling of the name): however, I have included a few for the benefit of readers his kingdom Chromista and subkingdoms Viridiplantae who may have become more familiar with a name and Biliphyta; his phyla Archamoebae, Dinozoa, different from the one chosen here for a particular Euglenozoa, Opalozoa, Percolozoa, and Radiozoa; his (generally well-known) group, keeping in mind that classes Diplonematea, Entamoebidea, Protalveolatea, persons coming from a botanical background, for ex- and Proterozoea. I am not necessarily rejecting his large ample, will have had a nomenclatural exposure likely number of new names for intermediate ranks. As stated differing from that of students trained in zoological in my INTRODUCTION, most of these have been taxonomy. omitted primarily to reduce the size of my own clas- 2. When both an original group and its later recogni- sificatory framework, making it more easily usable for tion as a unique higher-level taxon involve a very small the many readers who are not taxonomic specialists and

http://rcin.org.pl 30 J. O. Corliss neither want nor need such details. But I am also not proper taxonomic homes. With respect to high-level always convinced that our evidence to date requires the lineages widely recognized as truly monophyletic, I have separation of so many genera at levels so far above that tried (on preceding pages) to show possible interrelated- of the family. ness at phyletic (and lower) ranks, even if this process has made demands on insight and intuition and involved some healthy speculation. On more than one occasion, The Category "Incertae Sedis" I have deliberately (though often in a tentative way) united paraphyletic groups under a single higher-level I have not placed any major (or minor) taxa in the rank (as generally explained in the text in place). convenient category of "uncertain status" for several reasons. It is obvious that, as our knowledge continues to grow, various species and higher groups as well will need to be shifted about taxonomically. Systematics is Listing of Multiple Genera within Classes and Phyla not a static science. Furthermore, from a puristic point of view, we are really uncertain about a great many of I have offered far more than the usual number one our ranks and group-interrelationships, frustrating sees of "representative genera" for each of the high-level though this may be. It seems to me superfluous to mark taxa named on preceding pages (notable also in the nearly everything as "incertae sedis" when we anticipate INDEX) because I should like to enable the readers - changes based on fresh data of high phylogenetic/evolu- no matter what their field of specialty - to find their tionary (and thus taxonomic) value every year or so. It "favorites" and thus be able to relate them to the ranks is to be expected that, at any given time, some groups above and to neighboring groups. All too often, it seems are better known than others; but all deserve some place to me, papers that are concerned with phyla and classes - even if it must be tenuous or tentative - in an overall fail to supply the reader with any clues as to the location hierarchical classification, as I see it. of familiar genera within a newly proposed or newly Patterson and colleagues (e.g. Brugerolle and Patter- rearranged protist macrosystem (or portion thereof). son 1990; Larsen and Patterson 1990; Patterson 1986a, Naturally, space restrictions preclude mention of all 1990; Patterson and Brugerolle 1988; Patterson and genera, which number in the thousands. But, among the Zolffel 1991; V0rs 1988, 1993) favor labeling many 1100 that are included in this paper, I hope that I have unique species as "incert. sed. protists," seemingly managed to select many of the better-known (as well as without much desire to give them a (or place them in "representative") names of protists from the modern as any preexisting) taxonomic rank above genus or family well as the classical literature. Perceptive (with rare exception). Scores of exciting new protists are phycologists/protozoologists will note that certain thus being more or less assigned to a vague "Anhangen" genera are no longer where they used to be in older, position. By the same token, the Patterson school (e.g. conventional classifications. Ultrastructural studies, per- see Patterson and Sogin 1993, and references therein), haps even more so than molecular biological data, have and some other laboratories as well, determine necessitated such reassignments of sometimes familiar monophyletic lineages of protists, excellent research to taxa. Consider cases of formerly (thought to be) "closely carry out, while/but making no overt effort to interrelate related" genera or groups the members of which are now these lines in a manner involving ranking and production so widely separated taxonomically from each other, such of some kind of hierarchical system useful to the many as the following: Amoeba, Dientamoeba, Entamoeba, people wanting and needing the overall classification and Pelomyxa\ Proteromonas and Trypanosoma; Giar- that would result. dia and Trichomonas', Acrasis and Dictyostelium\ Cavalier-Smith (e.g. 1993c, and references therein), Ciliophrys and Dimorpha; Stephanopogon or Opalina among others of us, has attempted to find at least tem- and the ciliates; microsporidians and myxosporidians; porary or tentative homes for many "uncertain" protist dinoflagellates, chrysophyceans, and volvocines (a trio genera (e.g. a number of those listed by Patterson and of taxa rather close in older zoological classifications); Zolffel 1991), thus stimulating future workers to confirm and oomycetes plus hyphochytriomycetes and the or disprove such allocations. Nevertheless, it is true that chytridiomycetes. More examples could be cited. often protists poorly described in the older literature It has not been appropriate, here, to become involved require rediscovery and restudy before they can be given in discussion/treatment of generic synonyms, http://rcin.org.pl "User-friendly" Classification of the Protists 31

homonyms, etc. But, in choosing representative genera, REFERENCES I have sometimes run across dual usage of the same name, generally in cases of "botanical" versus "zoologi- Alexopoulos C.J., Mims C.W. (1979) Introductory Mycology. 3 ed. cal" taxa of protists. Resolution of such duplication, John Wiley & Sons, New York Andersen R.A. (1989) The Synurophyceae and their relationship to somewhat like that of the particularly troublesome other golden algae. Beih. Nova Hedwigia 95: 1-26 problems arising from having two groups of protists (e.g. Andersen R.A. (1991) Algae. In: Encyclopaedia Britannica, 15 ed. 242-251 dinoflagellates and euglenoids) simultaneously under Andersen R.A. (1992) Diversity of eukaryotic algae. Biodiversity jurisdiction of two different codes of nomenclature, is and Conservation 1: 267-292 Andersen R.A., Saunders G.W., Paskind M.P., Sexton J.P. (1993) beyond consideration here. For the protists, cases of both Ultrastructure and 18S rRNA gene sequence for Pelagomonas an identical name for two taxonomically rather different calceolata gen. et sp. nov. and the description of a new algal organisms and different names for the same organism class, the Pelagophyceae classis nov. J. Phycol. 29: 701-716 Anderson O.R. (1983) Radiolaria. Springer-Verlag, New York all fall under Patterson's (1986b) broad nomenclatural Bardele C.F. (1987) Auf neuen Wegen zu alten Zielen-moderne concept of "ambiregnal" species (see discussion and Ansätze zur Verwandtschaftsanalyse der Ciliaten. Verh. Dtsch. Zool. Ges. 80: 59-75 additional relevant references in Corliss, 1993). I should Barnes R.S.K.(Ed.) (1984) A Synoptic Classification of Living like to mention one outstanding example of the former Organisms. Blackwell Scientific Publications, Oxford Baroin A., Perasso R., Qu L.-H., Brugerolle G., Bachellerie J.-P., situation. Urospora, a well-known genus and type of a Adoutte A. (1988) Partial phylogeny of the unicellular eukaryotes family in the class Gregarinidea of the protozoan phylum based on rapid sequencing of a portion of 28 S ribosomal RNA. Proc. natl. Acad. Sei. USA 85: 3474-3478 Apicomplexa, is also a familiar taxon in the class Ul- Baroin-Tourancheau A., Delgado P., Perasso R., Adoutte A. (1992) vophyceae of the phylum Ulvophyta (kingdom Plantae, A broad molecular phylogeny of ciliates: identification of major subkingdom Viridiplantae)! Deliberately, I have not evolutionary trends and radiations within the phylum. Proc. natl. Acad. Sei. USA 89: 9764-9768 listed the name in either place, since/although it would Barr D.J.S. (1992) Evolution and kingdoms of organisms from the be an excellent choice as a "representative" genus in perspective of a mycologist. Mycologia 84: 1-11 Belova L.M. (1992) World-fauna and morphofunctional organiza- both instances. tion of Blastocystis. Russian Acad. Sei., Proc. Zool. Inst. 244: Species, the taxonomic level most affected by the 1-53 (in Russian) Bold H.C., Wynne M.J. (1985) Introduction to the Algae: Structure codes of nomenclature (Corliss 1993), have received no and Reproduction. 2 ed. Prentice-Hall, Englewood Cliffs, New mention in the present classification of the protists. A Jersey Boreham P.F.L., Stenzel D.J. (1993) The current status of Blastocy- general idea of the numbers of them per phylum or class, stis hominis. Parasit. Today 9: 251 however, may be gained from information included in Bourrelly P. ( 1957) Recherches sur les Chrysophycées. Morphologie Corliss (1984): see also Andersen (1992), Sleigh et al. phylogénie, systématique. Rev. Algol., Mém. Hors-Sér. No. 1 Bovee E.C. (1991) Sarcodina. In: Microscopic Anatomy of Inverte- (1984), and Vickerman (1992). Annually, hundreds of brates, (Eds. F.W. Harrison, J.O. Corliss), Wiley-Liss, New York, protistan species have been described as new, even in 1: 161-259 Bowman B.H., Taylor J.W., Brownlee A.G., Lee J„ Lu S.-D., White most recent years. This fact alone stands as eloquent T.H. (1992) Molecular evolution of the fungi: relationship of the evidence that alpha taxonomy thrives still today. Basidiomycetes, Ascomycetes, and Chytridiomycetes. Mol. Biol. Evol. 9: 285-296 Bremer K. (1985) Summary of green plant phylogeny and classifi- cation. Cladistics 1: 369-385 Bremer K„ Humphries C.J., Mischler B.D., Churchill S.P. (1989) On cladistic relationships in green plants. Taxon 36: 339-349 Broers C.A.M., Stumm C.K., Vogels G.D., Brugerolle G. (1990) Psalteriomonas lanterna gen. nov., sp. nov., a free-living amoe- boflagellate isolated from freshwater anaerobic sediments. Eu- rop. J. Protistol. 25: 369-380 Brugerolle G. (1991a) Cell organization in free-living amitochon- driate heterotrophic flagellates. In: The Biology of Free-living Heterotrophic Flagellates, (Eds. D.J. Patterson, J. Larsen), Cla- Acknowledgments. Many colleagues have generously given me rendon Press, Oxford, 133-148 Brugerolle G. (1991b) Flagellar and cytoskeletal systems in amito- advice concerning possible ways to resolve at least some of the chondrial flagellates: Archamoeba, Metamonada and Parabasala. problems of classifying the protists in a way reflecting the latest Protoplasma 164: 70-90 information available. Among the numerous persons with whom I Brugerolle G., Patterson D.J. (1990) A cytological study of Aulaco- have worked over the years, I want to mention here, with deep feelings monas submarina Skuja 1939, a heterotrophic flagellate with a novel ultrastructural identity. Europ. J. Protistol. 25: 191-199 of gratitude, especially three: Robert A. Andersen, Thomas Cavalier- Bütschli O. (1880-1889) Protozoa. Abt. I. Sarkodina und Sporozoa, Smith, and David J. ("Paddy") Patterson. I should hasten to point out, Abt. II. Mastigophora, Abt. III. Infusoria und System der Radio- however, that counsel received has not always been followed. Thus, laria. In: Klassen und Ordnung des Thier-Reichs (Ed. no one but the author should be held responsible for the phylogenetic H.G.Bronn), C.F. Winter, Leipzig, 1: 1-616, 617-1097, 1098- 2035 and taxonomic conclusions drawn and offered in the present paper.

http://rcin.org.pl 32 J. O. Corliss

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http://rcin.org.pl 36 J. O. Corliss

INDEX of Taxonomic Names

Names of top-level taxa (empire, kingdoms, phyla) are printed in boldface CAPS; those of classes and subclasses, in boldface upper- and lowercase. Ordinal (always ending in "-ida") and informal or vernacular names and generally unused or discardable names (often in quotation marks) appear in roman type. Representative genera are shown in italics. Taxa that appear in Table 1. are so indicated by reference to that table following page number citations.

Ammodiscus 19 Ammonia 19 Acanthamoeba 18 Amoeba 18, 30 ACANTHAREA 19, Table 1 Amoeboflagellates 10, 12, 13, 28 ACANTHARIA 19, Table 1 Amoebophrya 14 Acanthochiasma 19 Amphiacantha 10 Acanthocystis 19 Amphidinium 14 Acanthoeca 13 Amphileptus 17 Acanthoecopsis 13 Amphilonche 19 Acantholithium 19 Amphipleura 22 Acanthometra 19 Amphisiella 15 "Acellular" slime molds 13 Amphitrema 19 Acetabularia 25 Amphora 22 Achlya 23 Amphorellopsis 18 Achnanthes 22 Ancistrocoma 15 Acineta 15 Ancistrum 16 Aconoidea 17 Ancistrumina 16 Acrasida 10 Ancora 17 Acrasis 10, 30 Ancylonema 25 Acrosiphonia 25 Ancyromonas 12 Actinobolina 17 Anigsteinia 15 Actinocephalus 17 ANIMALIA 4, 5, 8, 20, 26, Actinocoryne 19 Table 1 Actinomonads 21 Anisolpidium 23 Actinomonas 21 Anisomonas 12 Actinomyxidia 20 Anoplophrya 16 Actinophryidea 19, Table 1 Anthemosoma 18 Actinophryids 28 Anthophysa 22 Actinophrys 19 Aphanochaete 25 "Actinopoda" 19 APICOMPLEXA 17, 26, 31, Table 1 Actinosphaerium 19 Apiosoma 16 Acytostelium 13 Aplanochytrium 21 Adelea 17 Apostomatia 16 Adelphamoeba 10 Apusomonas 12 Aggregata 17 Arachnodinium 17 Alaria 22 Arachnula 19 Albugo 23 Arcella 18 Alexandrium 14 ARCHAMOEBAE 9, 29, Table 1 Allogromia 19 ARCHEZOA 5, 7,9, 11,18,20, Alloiozona 17 27, 28, Table 1 Allomyces 26 Aristerostoma 15 "Alveolata" 13, 14, 17 Arthrocladia 22 Arthrodesmus 25 Amastigomonas 12 http://rcin.org.pl "User-friendly" Classification of the Protists 37

ASCETOSPORA 20, Table 1 Blastocrithidia 12 Ascobius 15 Blastocysta 26 ASCOMYCOTA 26 Blastocystis 18, 26 Ascophrys 16 Blastodinium 14 Askenasia 17 Blepharisma 15 Askoella 16 Blepharocorys 17 Aspidisca 15 Blidingia 25 Astasia 11 Blue-green algae 26 Astomatia 16 Boderia 19 Astrolonche 19 Bodo 12 Astrolophus 19 Bodonida 12 Astylozoon 16 Bodonids 11 Athalamida 19 Boldia 26 Atlantic ella 20 Bolivina 19 Audouinella 26 Botrydiopsis 22 Aulacantha 20 Botryococcus 25 Aulosphaera 20 Boveria 16 Aulotractus 20 Brachonella 15 Auricula 22 Brachynema 22 Australothrix 15 Bresslaua 15 Avelia 15 Brevilegnia 23 Brooklynella 15 Brown algae 8, 22, 25 B Brugerolleia 10 Bryometopus 15 Babesia 18 Bryophrya 15 Bacillaria 22 Bryophyllum 17 Bacillariophyceae 22, Table 1 BRYOPHYTA 24 BACILLARIOPHYTA 22 Bryophytes 24 Bacteriastrum 22 Bryopsis 25 Badhamia 13 Buetschliella 16 Bakuella 15 Bullanympha 11 Balamuthia 18 Bumilleriopsis 22 Balantidium 17 Burkea 10 Bangia 26 Bursaria 15 Bangiophyceae 26, Table 1 Bursaridium 15 Bangiopsis 26 Bursellopsis 16 Barbulanympha 11 Bursostoma 16 BASIDIOMYCOTA 26 Buxtehudea 10 Bathycoccus 24 Batrachospermum 26 Besnoitia 17 Bicosoeca 21 BICOSOECAE 21, Table 1 Caenomorpha 15 Bicosoecidea 21, Table 1 Cafeteria 21 Bicosta 13 Calciosolenia 23 Biddulphia 22 Calliacantha 13 BILIPHYTA 25, 26, 29, Table 1 Callimastix 26 Biomyxa 19 Callocolax 26 Blastocladiella 26 http://rcin.org.plCalonympha 11 38 J. O. Corliss

19 Chlorobotrys 22 23 Chlorococcum 25 26 Chlorogonium 25 16 Chlorokybus 25 25 "Chloromonads" 21 19 Chloromonas 21, 25 17 Chloromyxum 20 18 Chlorophyceae 25, Table 1 20 CHLOROPHYTA 24, Table 1 26 "Choanociliata" 13 17 Choanoflagellatea 13, Table 1 10 Choanoflagellates 13 13 Choanoflagellida 13 13 Choanomonads 13 20 CHOANOZOA 13, Table 1 19, Table 1 Choanozoa 26 18 Chondrus 26 18 Chonotrichs 15 12 Chordaria 22 16 Choreotrichs 15 12 Chromidina 16 13 CHROMISTA 5, 8, 13, 19,: 14 26 - 29, Table 1 20 Chromobionta 28 12 Chromobiota 28 17 Chromophyta 28 25 Chromulina 22 25 Chroomonas 23 25 Chrysamoeba 22 20 Chrysidalis 23 20 Chrysocapsa 22 18 Chrysochromidina 23 25 Chrysococcus 22 18 Chrysodendron 22 25, Table 1 Chrysomonadida 22 25, Table 1 Chrysomonads 22 25 Chrysophyceae 22, Table 1 21 Chrysophyceans 27, 30 15 Chytridiomycetes 26, Table 1 15 Chytridiomycetes 31 10 CHYTRIDIOMYCOTA 26, Table 1 23 Chytridiopsis 10 15 Chytridium 26 25, 27 Chytrids 23, 26 18 Chytriodinium 14 24 Chytriomyces 26 24, Table 1 Cienkowskya 19 24, Table 1 Ciliates 17, 30 25 CILIOPHORA 14, Table 1 28 Ciliophryids 19 http://rcin.org.pl "User-friendly" Classification of the Protists 39

Ciliophrys 21, 30 Contophrya 16 Cilioprotists 14 Copromyxa ... 18 Cinetochilum 16 Corallomyxa 13 Cirrhogaster 15 Coscinodiscophyceae 22, Table 1 Cladophora 25 Coscinodiscus 22 Clathrostoma 16 Cosmarium 25 Clathrulina 19 Cosmetophilus 17 Clausilocola 16 Cosmocolpoda 15 Clevelandella 15 Costaria 22 Climacostomum 15 Cothurnia 16 Closterium 25 Craspedomonadophyceans 36 "Cnidosporidia" 20 Craspedomonads 13 Coccidea 17, Table 1 Craspedophyceae 13 Coccodiscus 20 Cribraria 13 COCCOLITHOPHORA 23 Crithidia 12 Coccolithophorida 23 Crypthecodinium 14 Coccolithus 23 Cryptobia 12 Coccomyxa 25 CRYPTOMONADA 23, Table 1 Cochliopodium 18 Cryptomonadea 23, Table 1 Codium 25 Cryptomonadida 23 Codonella 15 Cryptomonas 23 Codosiga 13 CRYPTOPHYTA 23, Table 1 Coelastrum 25 Cryptophytes 28 Coelodendrum 20 Cryptosporidium 17 Coelomomyces 26 Cucurbitella 18 Coelotropha 17 Culicospora 10 Cohnilembus 16 Curimostoma 16 Colacium 11 Cyanidium 26 Coleochaete 25 Cyanophora 26 Coleps 16 Cyathobodo 12 Collar flagellates 13 Cyathobodonida 12 Collinia 16 Cyathodinium 15 Collosphaera 20 Cyclidium 16 Collozoum 20 Cyclophora 22 Colpidium 16 Cycloposthium 17 Colpoda 15 Cyclospora 17 Colpodea 15, Table 1 Cyclotella 22 Colpodella 17 Cyclotrichium 17 Colponema 14 Cylindrocystis 25 Comatricha 13 Cylindrotheca 22 Compsopogon 26 Cymatopleura 22 Conchophthirus 16 Cymbella 22 Conchopsis 20 Cymopohlia 25 Condylostoma 15 Cyphoderia 18 Conidiophrys 16 Cyrtocaryum 16 Conion 13 Cyrtolophosis 15 Conjugaphyceae 25 Cyrtophorids 15 Conjugatophyceae 25, Table 1 Cyrtostrombidium 15 Conoidea 17 Cystodinium 14 Conradinema 11 Cystoseira 22 http://rcin.org.pl 40 J. O. Corliss

D Disematostoma Distigma Dactylosoma 18 Ditrichomonas Dasycladus 25 Dobellia Deltotrichonympha 11 Dolichomastix Dendrocometes 15 Doliospora Dendrosoma 15 Dorisiella Dermatochrysis 22 Dragescoa Desmidium 25 Duboscquella. Desmids 25 Dunaliella Desmothoracidea 19, Table 1 Durchoniella.. Desportesia 10 Dysteria Devescovina 11 Dexiotricha 16 Diadesmis 22 E Diaphanoeca 13 Diatoma 22 Ebria DIATOMAE 22, Table 1 Echinostelium Diatoms 22 Echinozoon.... Dictyocha 21 Ectocarpus DICTYOCHAE 19, 21, Table 1 Eimeria Dictyostelea 13, Table 1 Eimeriida Dictyostelium 13, 30 Ellobiophrya.. Dictyota 22 Ellobiopsis Didesmis 17 Elphidium Didinium 17 Emiliania Didymium 13 Encephalitozoon Dientamoeba 11, 18, 30 Enchelys Difflugia 18 Endamoeba Dileptus 17 Endocladia Dilsea 26 Endo Umax Dimorpha 12,30 Endoreticulatus Dimorphids 19 Endosphaera Dinobryon 22 Endotrypanum Dinoflagellatea 14, Table 1 Entamoeba Dinoflagellates 5, 17, 19, 27, 30 Entamoebidae Dinophyceae 14 Entamoebidea Dinophysis 14 Enterocytozoon DINOZOA 5, 13, 29, Table 1 Enteromonadida Diophryopsis 15 Enteromonas Diophrys 15 Entodiniomorphids Diphyllea 12 Entodinium Diplocystis 17 Entodiscus Diplomonadida 10 Entosiphon Diplonema 11 Epalxella Diplonematea 11, 29, Table 1 Ephelota Diplo spora 17 Epipyxis Discocelis 12 Epistylis Discocephalus 15 Erythropsidinium Discorbis 19 http://rcin.org.plErythrotrichia "User-friendly" Classification of the Protists 43

Espejoia 16 Eudorina 25 11 Galatheammina 19 11 Gamophyceae 25 11 Gastrostyla 15 11 Geleia 15 11, Table 1 Giardia 9, 10, 30 5, 11,24,27,30 Giffordia 22 5, 11, 12, 29, Table 1 Gigartina 26 Euglypha 18 Glabratella 19 25 Glaucocystis 26 5, 7, Table 1 Glaucoma 16 12 Glaucophyceae 26, Table 1 23 GLAUCOPHYTA 17, 26, Table 1 15 Glaucophytes 24, 26 22, Table 1 Glaucosphaera 26 22 Glenodinium 14 ,22 Gleodinium 14 11 Globigerinella 19 Globospora 20 Gloeobotrys 22 Gloeochaete 26 Gloeocystis 25 20 Gloeopodium 22 15 Glugea 10 15 Golden-brown algae 22 16 Goniomonadea 23, Table 1 18, Table 1 Goniomonads 23 18 Goniomonas 23 26, Table 1 Goniotrichum 26 16 Gonium 25 15 Gonospora 17 10 Gonyaulax 14 19, Table 1 Gonyostomum 21 20 Gorillophilus 17 19 Goussia 17 19 Gracilaria 26 22 Grammatophora 22 22, Table 1 Grandoria 15 17 Granuloreticulosea 13, 18, Table 1 25 Grass-green scaly algae 24 16 Green algae 24 - 28 22 Gregarina 17 22 Gregarinidea 17, 31, Table 1 22 G re Ilia 17 Fuligo, 13 Gromia 18 5, 8, 18, 20, 23, 26 Grossglockneria 15 Table 1 Gruberella 10 26 Gurleya 10 15 http://rcin.org.plGuttulina 19 42 J. O. Corliss

Guttulinopsis 18 Hemiselmis 23 Gymnodinioides 16 Hemispeira 16 Gymnodinium 14 Henneguya 20 Gymnosphaera 19 Hepatocystis 18 Gyrodinium 14 Hepatozoon 17 Gyrosigma 22 Herpetomonas 12 Hessea 10 Heteramoeba 10 H Heterochloridea 22 Heteroderma 26 Haematococcus 25 Heterogloea 22 Haematozoea 18, Table 1 HETEROKARYOTA 14 Haemogregarina 17 Heterokont 22 Haemoproteus 18 HETEROKONTA 21, Table 1 Haemosporida 18 Heterokontophyta 21 Halimeda 25 Heterokonts 13, 21 -23, 26, Haliommatidium 19 Heterolobosea 10, Table 1 Halocella 20 Heteromita 12 Halosphaera 20 Heteromitida 12 Halteria 15 Heteronema 11 Halymenia 26 Heteronematida 11 Hanzschia 22 Heterophrys 19 Haplocaulus 16 Heterosigma 21 Haplosporidea 20, Table 1 Heterotheca 19 Haplosporidians 20 Heterotrichea 14, Table 1 Haplosporidium 20 Heterotrichia 15 Haplozoon 14 Heterotrichians 14 HAPTOMONADA 23, Table 1 Heterotrichs 14, 15 Haptophrya 16 Hexamastix 11 HAPTOPHYTA 23, Table 1 Hexamita 10 Haptophytes 8, 22, 27, 28 Hibberdia 22 Haptorids 17 Hildenbrandia 26 Hartmannella 18 Histiobalantium 16 Hartmannula 15 Histiona 12 Hastige rina 19 Histomonas 11 Hausmanniella 15 Hochbergia 13 Hedraiophrys 19 Hoferellus 20 Hedriocystis 19 Holomastigotoides 11 Hegneria 11 Holophrya 16 Helicoprorodon 16 Homosira 22 Helicosporidium 20, 26 Hoplitophrya 16 Heliochona 15 Hoplonympha 11 "Helioflagellates" 12, 19, 21 Hyalophysa 16 Heliomonas 12 Hydramoeba 18 Heliophrya 15 Hydrodictyon 25 HELIOZOA 19, Table 1 Hydrosilicon 22 Hemidiscus 22 Hymenostoma tia 15 Hemimastigida 12 Hypermastigotea 11, Table 1 Hemimastigophorea 11, 12, Table 1 Hyphochytriomycetes 23, Table 1 Hemimastix 12 http://rcin.org.plHyphochytriomycetes 30 "User-friendly" Classification of the Protists 43

Hyphochytrium 23 Kreyella 15 Hypochona 15 Kudoa 20 Hypotrichs 15 Hysterocineta 16

I Laboea 15 Ichthyobodo 12 LABYRINTHOMORPHA 21, Table 1 Ichthyophthirius 16 Labyrinthula 21 INFUSORIA 14 Labyrinthulea 21, Table 1 Intoshellina 16 Labyrinthuloides 21 Iodamoeba 18 Lacrymaria 17 Iridaea 26 Lagenidium 23 Iridia 19 Lagenophrys 16 Isochona 15 Lagotia 15 Isochrysis 23 Lagynophrya 17 Isonema 11 Lambornella 16 Isospora 17 Laminaria 22 Isotricha 17 Lamtostyla 15 Lankesterella 18 J Lankesteria 17 Lateromyxa 18 Jakoba 12 Lecudina 17 Jaocorlissia 16 Leegaardiella 15 Joenia 11 Legerella 18 Leishmania 12 K Lembadion 16 Lennoxia 22 Kahliella 15 Lepidotrachelophyllum 17 Karlingia 26 Leptomitus 23 Karotomorpha 12 Leptomonas 12 Karotomorphida 12 Leptomyxa 18 Karyoblastea 9 Leptothorax 15 Karyolysus 17 Lesquereusia 18 Karyorelictea 14, Table 1 Leucocryptos 12 Karyorelictians 14 Leucocytozoon 18 Karyorelictids 15 Leucodictyon 12 Kathablepharis 12 Licea 13 Kentrophoros 14 Licmophora 22 Kerona 15 Licnophora 15 Khawkinea 11 Lieberkuehnia 19 Kiitricha 15 Lithodesmium 22 Kinetomonadea 12, Table 1 Lithophyllum 26 Kinetoplastidea 11, 25, Table 1 Lithoptera 19 Klebsormidium 25 Litonotus 17 Klossia 17 Litosiphon 22 Klossiella 17 Litostomatea 16, Table 1 Kofoidia 11 Lobochona 15 Kofoidinium 14 Lobosea 13, 18, 26, Table 1 Komokia 19 http://rcin.org.plLohmanniella 15 44 J. O. Corliss

Loma 10 Metacysîis 16 Lomiella 16 METAMONADA 9, Table 1 Lomosporus 20 Metaroîaliella 19 Lophomonadida 11 Metchnikovella 10 Lophomonas 11 Metchnikovellida 10 Loricophrya 15 Metopus 15 Loxocephalus 16 Miamiensis 16 Loxodes 14 Micrasterias 25 Loxophyllum 17 Microfdum 10 Lujfisphaera 18 Microglabratella 19 Lwoffia 15 Microglena 22 Lycogala 13 Microgromia 19 Lynchella 15 Microjoenia 11 Ly relia 22 Micromonadophyceae 24 Lyromonadea 10, Table 1 Micromonas 24 Lyromonas 10 MICROSPORA 10, Table 1 Microspora 25 Microsporea 10, Table 1 M Microsporida 10 Microsporidians 20, 27, 30 Macrocystis 22 Microthorax 15 Macrospironympha 11 Minchinia 20 Mallodendron 22 Minisporida 10 Mallomonas 22 Minium 26 Mallomonopsis 22 Minutocellus 22 Mamiella 24 Monoblepharella 26 Mantoniella 24 Monocercomonas 11 Marituja 16 Monocercomonoides 10 Marteilia 20 Monochilum 16 Marteiliidea 20 Monochrysis 22 Maryna 15 Monocystis 17 Massisteria 12 Monodopsis 22 Mastigamoeba 9 Monosiga 13 Mastigamoebida 9 Monothalamida 19 Mastigella 9 Mrazekia 10 Masîigina 9 MYCETOZOA 12, Table 1 Maupasella 16 Mycetozoa 18, 28 Mayorella 18 Mycterothrix 15 Medusetîa 20 Mylestoma 15 Megamoebomyxa 13 Myrionema 22 Melanophyceae 22 Myxidium 20 Melosira 22 Myxobolus 20 Menoidium 11 Myxogastrea 13, Table 1 Merotricha 21 MYXOMYCETES 12 Mesodinium 17 MYXOMYCOTA 12 Mesojoenia 11 Myxophthirus 16 "Mesokaryota" 13 Myxoproteus 20 Mesophyllum 26 Myxosporea 20, Table 1 Mesostigma 24 Myxosporidia 20 MESOZOA 27 Myxosporidians 20, 30 http://rcin.org.pl "User-friendly" Classification of the Protists 45

Myxotheca 19 Onychodromus 15 MYXOZOA 20, Table 1 Oocardium 25 Myxozoa 27 Oodinium 14 Myzocytium 23 Oomycetes 23, Table 1 Oomycetes 30 N OOMYCOTA 23 Opalina 12, 30 Naccaria 26 Opalinatea 12, Table 1 Naegleria 10 Opalinida 12 Nannochloropsis 22 Opalinids 28 Nanochlorum 25 Opalinopsis 16 Nassophorea 15, 16, Table 1 OPALOZOA 11, 12, 19, 28, 29, Nassula 15 Table 1 Nassulopsis 15 Opercularia 16 Nautococcus 25 Ophiaster 23 Navicula 22 Ophiocytium 22 Nebela 18 Ophiuraespira 16 Neobursaridium 16 Ophrydium 16 Neocallimastix 26 Ophryocystis 17 Nephridiophaga 20 Ophryodendron 15 Nephromyces 12 Ophryoglena 16 Nephroselmis 24 Ophryoglenids 15 Netzelia 18 Ophryoscolex 17 Nitella 25 Opisthonecta 16 Nitellopsis 25 Orbopercularia 16 Nitzschia 22 Orbulinella 19 Noctiluca 14 Ortholinea 20 Nolaclusilis 15 Ovammina 19 Nolandia 16 Oxymonadea 10, Table 1 N onion 19 Oxymonadida 10 Nosema 10 Oxymonas 10 Notila 10 Oxyrrhis 14 Nuclearia 18 Oxytoxum 14 Nyctotheroides 15 Oxytricha 15 Nyctotherus 15 P O Pallitrichodina 16 Ochromonas 22 Palmaria 26 Octodendron 19 Palmodictyon 25 Octomitus 10 PARABASALA 11, 18, Table 1 Octomyxa 12 Parabasalans 7 Odontella 22 Parabundleia 17 Ogdeniella 18 Paracichlidotherus 15 Oikomonas 21 Paracineta 15 Oligohymenophorea 15, Table 1 Paradistigma 11 Oligotrichs 15 Paraflagellata 12 Olisthodiscus 21 Paraisotricha 17 Olpidiopsis 23 Paramarteilia 20 Olpidium 26 Paramecium 15, 16 http://rcin.org.pl 46 J. O. Corliss

18 Phacotus 25 20 Phacus 11 20 Phaeocystis 23 21 Phaeodarea 20 11 Phaeodina 20 10 Phaeophila 25 16 Phaeophyceae 22, Table 1 20 PHAEOPHYTA 21, Table 1 13 Phagodinium 12 25 Phagomyxa 12 23, Table 1 Phalacrocleptes 15 19 Phalansterium 12 18 Phascolodon 15 16 Phialinides 17 23 Philaster 16 23, Table 1 Philasterids 16 25 Phragmonema 26 21 Phreatamoeba 9 21, Table 1 Phreatamoebida 9 21 Phtorophrya 16 21 Phyllopharyngea 15, Table 1 21 Phyllophora 26 24 Physarum 13 24, Table 1 Physoderma 26 22 "Phytoflagellata" 5 15 Phytomonadida 25 22 "Phytomonads" 27 22, Table 1 Phytomonas 12, 25 15 Phytophthora 23 9, Table 1 Piroplasmida 18 9, 30 Placus 16 18 Plagiacantha 20 15 Plagiocampa 16 16 Plagiopyla 17 16 Plagiotoma 15 11 Planicoleps 16 10, Table 1 Planorbulina 19 10 PLANTAE 5, 8,10,21,24,25, 10, 11,28, 29, Table 1 27, 31, Table 1 10 Plasmodial slime molds 13 14 Plasmodiophora 12 Peritrichia 16 Plasmodiophorida 12 15 Plasmodium 18 17, Table 1 Platyamoeba 18 17 Platychilomonas 12 10 Platycola 16 23 Platyophrya 15 23 Pleistophora 10 11 Pleodorina 25 http://rcin.org.pl "User-friendly" Classification of the Protists 47

Pleuras pi s 19 Protoheterotrichs 15 Pleurastrum 25 Protoopalina 12 Pleurochloris 22 Protoperidinium 14 Pleurochrysis 23 Protosiphon 25 Pleurocoptes 16 Protostelea 13, Table 1 Pleuronema 16 Protostelium 13 Pleuronematids 16 Protozelleriella 12 Pleurosigma 22 PROTOZOA 5 - 7,9,10,22 - 28, Pleurostomes 17 Table 1 Ploeotia 11 PRYMNESIOPHYTA 23 Pneumocystis 26 Prymnesium 23 Pocheina 10 Psalteriomonas 10 Podophrya 15 Psammetta 19 Po do s ira 22 Pseudobalanion 16 Polycycla 16 Pseudobodo 21 Polycystinea 20, Table 1 Pseudocharaciopsis 22 Polyhymenophorea 14, Table 1 Pseudociliatea 11, Table 1 Polyhymenophoreans 15 Pseudodendromonas 12 Polykrikos 15 Pseudodifflugia 18 Polymyxa 12 PSEUDOFUNGI 23, 26, Table 1 Polysphondylium 13 Pseudoglaucoma 15 Polystomella 19 Pseudolithium 19 Polytomella 25 Pseudomicrothorax 15 Porolithon 26 PSEUDOMYCOTA 23 Porospora 17 Pseudopedinella 21 Porphyridium 26 Pseudoprorodon 16 Postciliodesmatophora 14 Pseudoscourfieldia 24 Poterioochromonas 22 Pseudospora 12 Prasinophyceae 24, Table 1 Pseudotrachelocerca 17 PRASINOPHYTA 24, Table 1 Pseudotrichomonas 11 Prasiola 24 Pseudovahlkampfia 10 Proboveria 16 Pteridomonas 21 Procryptobia 12 PTERIDOPHYTA 24 Promycetozoida 13 Pterosperma 24 Propyxidium 16 Ptychodiscus 14 Prorocentrum 14 Ptychostomum 16 Prorodon 16 Pycnothrix 17 Prorodontida 16 Pyramimonas 24 Prostomatea 16, 17, Table Pyrenomonas 23 Prostomatida 16 Pyrocystis 14 Protal veolatea 13, 29, Table Pyrophacus 14 Proteomyxids 12 Pyrrhophyta 14 Proteromonads 28 Pyrsonympha 10 Proteromonas 12, 30 Pythium 23 Proterospongia 13 Proterozoea 12, 29, Table PROTISTA 4, 5,27 Q Protociliata 12 Protocruzia 15 Quasillagilis 17 PROTOCTISTA 4 Quinqueloculina 19 http://rcin.org.pl 48 J. O. Corliss

R Rotaliella Rudimicrosporea Raabella 15 Radiolaria 20, Table 1 S Radiolarians 20 Radiophrya 16 Saccammina RADIOZOA 19, 29, Table 1 Saccamoeba Raphidiophrys 19 Saccinobaculus Raphidomonadea 21, Table 1 Salpingoeca, Raphidonema 25 Saprodinium RAPHIDOPHYTA 21, Table 1 Saprolegnia.. Reclinomonas 12 Sarcinochrysis Red algae 24 - 26 Sarcocystis Reichenowella 15 "Sarcodina" Remanella 14 Sargassum Resultor 24 Saurocytozoon Reticulosphaera 22 Scaphidiodon Retortamonadea 10, Table 1 Scenedesmus Retortamonadida 10 Schellackia... Retortamonas 10 Schizammina Rhabdoaskenasia 17 Schizocalyptra Rhabdomonadida 11 Schizocystis Rhabdomonas 11 Schizomerus.... Rhabdophorids 16 Schizopyrenida Rhabdophrya 15 Schwagerina Rhabdostyla 16 Sclerospora.. Rhinomonas 23 Scourfieldia . Rhinozeta 17 Scuticociliatia Rhipidium 23 Scyphidia Rhizammina 19 Scytosiphon.. Rhizidiomyces 23 Sea lettuce ... Rhizochromulina 22 Sea weeds.... Rhizoclonium 25 Selenastrum . Rhizodinium 14 Selenidioides Rhizophydium 26 Selenidium ... RHIZOPODA 9, 10, 13, 18, 26, Selenita Table 1 Selysina Rhizosolenia 22 Semitrichodina Rhizosphaera 20 Sicuophora Rhodella 26 Siedleckia Rhodochaete 26 Silicoflagellatea Rhodomonas 23 Silicoflagellates Rhodophyllis 26 Singhamoeba RHODOPHYTA 26, Table 1 Sinuolinea Rhodospora 26 Siphonocladus Rhynchocystis 17 Sirogonium .. Rhynchomonas 12 Slopalinida... Rosalina 19 "Slopalinids" Ro scoffia 14 Snyde re I la.... Rosculus 18 http://rcin.org.plSonderia "User-friendly" Classification of the Protists 49

Sorites 19 Stichotrichs 15 Sorocarpus 22 Stilopsis 22 Sorodiscus 12 Stokesia 16 Sorogena 15 Stoneworts 25 Spathidiopsis 16 "Stramenopiles" 20, 28 Spathidium 17 "Straminopiles" 28 SPERMATOPHYTA 24 Streptophyllum 22 Sphaeromyxa 20 Strobilidium 15 Sphaeroplea 25 Strombidium 15 Sphaerospora 20 Stylocephalus 17 Sphenoderia 18 Stylochona 15 Sphenomonas 11 Stylonychia 15 Sphenophrya 15 Suctorians 15 Spirillina 19 Symbiodinium 14 Spirochona 15 Synchytrium 26 Spiro gyra 25 Syndinium 14 Spiroloculina 19 Synura 22 Spiromonas 17 Synurophyceae 22, Table 1 Spironema 12 Spironucleus 10 T Spirostomum 15 Spirotrichea 14, Table 1 Tachyblaston 15 Spirotrichia 15 Tardivesicula 10 Spirotrichonympha 11 Taxopodea 19, Table 1 Spizellomyces 26 Telomyxa 10 Spongodrymus 20 Teranympha 11 Spongomonas 12 Territricha 15 Spongospora 12 Tesselaria 22 Sporadotrichs 15 Tetractinomyxon 20 Sporochnus 22 Tetradimorpha 12 Sporolithon 26 Tetrahymena 16 SPOROZOA 17 Tetramastigamoeba 10 Sprague a 10 Tetramitus 10 Spumella 22 Tetramyxa 12 Stannophyllum 19 Tetraselmis 24 Staurastrum 25 Tetraspora 25 Steinella 16 Tetrasporidium 25 Stemonitis 13 Textularia 19 S tempe l lia 10 Thalassicolla 20 Stentor 15 Thalassionema 22 Stephanodiscus 22 Thalassiosira 22 Stephanoeca 13 Thalassomyces 14 Stephanopogon 11, 30 Thalassomyxa 13 Stephanosphaera 25 Thalassophysa 20 Stephanospora 17 Thaumatomastix 12 Stereomyxa 18 Thecacineta 15 Stereonema 12 Thecamoeba 18 Stichochrysis 22 Theileria 18 Stichococcus 25 Thelohania 10 Sticholonche 19 http://rcin.org.plThigmocoma 16 50 J. O. Corliss

Thigmophrya 16 Triloculina .... Thigmotrichs 16 Trilospora Thoracosphaera 14 Trimitus Thorea 26 Trinema Thraustochytriacea 21, Table 1 Triparma Thraustochytrium 21 Trochilia Thylakidium 15 Troglodytella Tiarina 16 Trypanosoma Tintinnids 15 Trypanosomatida Tintinnopsis 15 Trypanosomatids Tokophrya 15 Tubulina Tolypella 25 Turaniella Tontonia 15 Tuzetia Toxarium 22 Tyzzeria Toxoplasma 18 Trachelocerca 14 U Trachelomonas 11 Trachelonema 14 Ulothrix Tracheloraphis 14 Ulva Tracheophytes 24 Ulvophyceae Transitella 15 ULVOPHYTA Trebouxia 25 Umbilicosphaera Trentepohlia 25 Undella Trepomonadea 9, Table 1 Unicapsula... Trepomonas 10 Unicauda Treubaria 25 Unikaryon.... Triadinium 17 Uradiophora Tribonema 22 Urceolaria ... Tribophyceae 22 U rocentrum Trice ratium 22 U roglena Trichamoeba 18 U ronema Trichia 13 Uronychia.... Trichochona 15 Urosomoides Trichodina 16 U rospo ra Trichodinopsis 16 Urosporidium Trichomonadea 11, Table 1 Urostyla Trichomonadida 11 Urotricha Trichomonas 11, 30 Urozona Trichonympha 11 Utriculidium Trichonymphida 11 Uvigerina.... Trichophilus 25 Trichophrya 15 V Trichosarcina 25 Trichosphaerium 18 Vacuolaria .. Trichospira 17 Vaginicola... Trichostomes 17 Vahlkampfia Tricornia 10 Vairimorpha Tricoronella 15 Valonia Trigonomonas 10 Vampyrella.. Trihymena 15 http://rcin.org.plVampyrophrya "User-friendly" Classification of the Protists 53

Vannella 18 Xiphophora 22 Vasichona 15 Vasicola 16 Xystonellopsis 15 Vaucheria 22 Vegetabilia 6 Y Verrucalvus 23 Yamagishiella 25 Vestibül iferans 17 Yellow-green algae 22 Vestibulongum 17 Vexillifera 18 Yvonniellina 15 VIRIDIPLANTAE 24, 29, 31, Table 1 Vischeria 22 Z Volvocida 25 Volvocids 27 Zelleriella 12 Volvocines 30 Zonaria 22 Volvo)c 25, 27 Zooanthella 14 Vorticella 16 "Zoomastigophora" 5 Zoophagus 23 W Zoosporea 17 Zoothamnium 16 Wallackia 15 Zosterodasys 15 Wardia 20 Zschokkella 20 Wenrichia 16 Zygnema 25 Wenyonella 18 Zygnematophyceae 25 Woodrujfia 15 Zygocystis 17 Woronina 12 ZYGOMYCOTA 26 Zygophyceae 25 Zymurgia 26

Xanthidium 25 Xanthophyceae 22, Table 1 Xenophyophorea 19, Table 1 Xiphacantha 19 Received on 2nd November, 1993

http://rcin.org.pl http://rcin.org.pl ACTA Acta Protozoologica (1994) 33: 53 - 57 PROTOZOOLOGICA

Gravity-dependent Modulation of Swimming Rate in Ciliates

Hans MACHEMER

Arbeitsgruppe Zelluläre Erregungsphysiologie, Ruhr-Universität, Bochum, Germany

Eukaryotes including protists use gravity as a cue to sensitive receptor over a distance of 1 nm, the work done know "up" and "down". Research in Paramecium has 19 or energy exerted on the receptor is 10 J. This exceeds established that, for the induction of an orientational the energy of thermal noise by a factor of 50. Thus, from response to gravity, sensory transduction is not neces- the physicist's viewpoint, the energetic preconditions for sarily involved (see Machemerand Braucker 1992). For cellular gravitransduction are reasonable. instance, buoyancy of the cell body may produce nega- Where can gravity attack a ciliate cell? The visco- tive gravitaxis. A guiding principle of our research is to elastic properties of the cytoplasm may be modelled by search in the ciliates for evidence of a gravisensory a series of dashpots and springs. The lower membrane pathway, and if such pathway exists to elucidate its of a cell is the first candidate of outward deformation mechanisms. by gravity but, due to charging of the cytoplasmic An implication of gravisensation is that extrinsic "spring", also the upper membrane may be pulled inward energy is transduced to generate a cellular signal. For a after some delay. If gravity can induce mechanical defor- single cell, the most obvious way of transduction of the mations of the cell membrane, we are on less speculative gravity vector is pressure arising from local differences grounds because the distributions of mechanosensitivity in density. Independent measurements have shown that in ciliates such as Paramecium, Stylonychia and the density of the Paramecium cytoplasm exceeds the Didinium are comparatively well studied. Figure 1 density of freshwater by 4% (Koehler 1922, Fetter 1926, shows the pattern of distributions of depolarizing Taneda 1987, Kuroda and Kamiya 1989). This cor- mechanosensitivity, as mediated by somatic Ca channel responds to a force of 10"10 N and a pressure gradient conductances, and hyperpolarizing mechanosensitivity, across the lower membrane of slightly below 0.1 Pa. as mediated by somatic K channel conductances (Ogura Gravitropism in plant roots employs forces and pressure and Machemer 1980). If we assume that this pattern gradients of this magnitude (Volkmann 1974). If we applies to static loads as well as to pulse stimulation, we assume tentatively that the force of 10"10 N deforms a can predict that a downward swimming Paramecium is depolarized due to activation of Ca-mechanoreceptor Paper presented at the Symposium: Motility, Behaviour and channels. When Paramecium swims upward, it is hy- Orientation at the IXth International Congress of Protozoology, July 25th - August 1st, 1993, Berlin, Germany. perpolarized because of K-mechanoreceptor channel ac- tivation. For horizontally swimming paramecia this Address for correspondence: H. Machemer, Arbeitsgruppe Zelluläre Erregungsphysiologie, Ruhr-Universität, D-44780 Bochum, scheme predicts a full cancelling of depolarizing and Germany. hyperpolarizing gravisensory input because the summed http://rcin.org.pl 54 H. Machemer mechanoreceptor conductances give a Ca-K conduc- tance ratio equivalent to that of the Paramecium resting post. potential. Unfortunately, it is difficult to directly measure per- sistent gravity- and position-dependent small potential offsets in single cells. We employ an indirect method of assessing gravireceptor potentials: the velocity of free swimming cells. It is established that small positive shifts from the resting potential depress ciliary frequen- cy and the rate of forward swimming in Paramecium; small negative shifts from the resting potential raise the ciliary frequency so that the forward swimming velocity goes up (see Machemer 1986). In other words, the electrophysiological hypothesis of gravireception Fig. 1. Paramecium mechanoreceptor conductances of the cell soma predicts that active ciliary propulsion in upward swim- as revealed by topographically defined pulse stimulation (modified after Ogura and Machemer 19^0). Along the antero-posterior axis of ming paramecia exceeds propulsion in horizontal cells, the cell two gradients of Ca~+-dependent depolarizing mechano- + whereas ciliary propulsion in downward swimming cells sensitivity and K -dependent hyperpolarizing mechanosensitivity overlap. A mechanically induced conductance ratio, AgCa/AgK, deter- is reduced as compared to horizontal swimmers mines the polarity and amplitude of the resulting mechanoreceptor (Machemer et al. 1991). We call this gravity-induced potential (conductance ratio of resting potential: near 2.3). Behaviou- ral data suggest that overall static deformation of the "lower" soma modulation of the rate of locomotion gravikinesis. membrane by gravitational pressure affects a similar or even the same In a world of gravitational pull, it is not easy to system of mechanically sensitive channels measure the rate of active propulsion of a cell. A Para- mecium that adds an increment (Ay) to the propulsion horizontal vertical rate (P) during upward swimming from activation of K n = 1003 n • 1277 channels, settles at the same time at the rate of sedimen- tation (S). The vector sum of these velocities (Vy) gives the observable swimming velocity. In vertically moving cells, the equation is:

Vy = P S + Au (1)

The same reasoning applies to vertically downward swimmers, where Ca channel activation induces a sub- traction from P by the amount A, and S adds to that 573 tj? Mm/s difference:

VD = P + S -Ae (2) In order to assess the gravikinetic response, A, we need to determine three variables: the observed swim- ( (hC\ v^ n ming velocity, the sedimentation rate and the rate of \ Ivt& J intrinsic propulsion, as being unaffected by gravity. For convenience in experimentation, we have, as a first 8% attempt, ignored the value of the propulsion rate using r = 0.059 r = 0.200 the difference of the equations of vertically downward swimming and vertically upward swimming cells. In the resulting simple equation, P has been eliminated, and Fig. 2. Swimming velocities (upper panel) and orientations (lower panel) of Paramecium in horizontally and vertically oriented volumes the value of A equals the arithmetic mean of A during of the experimental chamber (30 x 18 x 1.6 mm). The polar histograms downward (VD) and upward swimming (Vy): suggest a downward velocity bias and upward orientation bias of cells swimming in the vertical plane. Note scaling of velocity (|im/s) and orientation (% of total cell count, n). r - direction coefficient (Bat- (VD - Vu)/2 = S - A (3) schelet 1981). Modified after Machemer et al. 1993 http://rcin.org.pl Gravity-dependent Swimming Rate in Ciliates 55

swimming rate [pm/s] are 2 to 4 seconds. Linear calibration of the field, and time of swimming, give the velocity. Fields were evaluated quantitatively by hand. This allows us to distinguish between continuously swimming cells and those, which perform reversals. Swimming velocities were represented by polar his- tograms. In Fig. 2 the upper panel shows polar distribu- tions of velocities of the same population of cells recorded horizontally (left) and vertically at 1 g (right). There was no preferred direction in horizontal swim- ming rates. On the other hand, the upward swimmers vertical 1g Mg (1.5-3 s) Mg (3-4.5 s) horizontal 1g were slower, and the downward swimmers faster than 708 503 836 6179 at horizontal orientation. In the same population, Fig. 3. Relaxation of differences in vertical velocities of Paramecium velocity medians of all vertical rates differed from the following transition from normal gravity (lg) to weightlessness (|ig) medians of all horizontal rates suggesting in vertically in the drop tower (light shading: upward swimmers; heavy shading: downward swimmers). Median velocities within "upward" and oriented cells the existence of a gravikinetic response "downward" 90° sectors were determined during two periods (1.5-3 superimposed on sedimentation. s; 3-4.5 s) after start of free fall. Comparison with horizontal velocity of same population within same sectors shows that velocity under A quantitative determination of the graviresponse is weightlessness corresponds to horizontal velocity at lg. Note inter- possible defining sectors of more or less vertical orien- ruption of velocity scale (Machemer et al. 1992) tation. Figure 3 gives the evaluation of a free-fall ex-

With equation 3, it takes measurements of easily accessible parameters to determine gravikinesis: the ve- locities of downward and upward swimming, and the Gravikinesis [pm/s] sedimentation rate. Note that with the electrophysiologi- cal hypothesis, the sign of gravikinesis in Paramecium is inverse to sedimentation. We have used both the simple difference equation (3) and the more specific original equations (1,2). The propulsion rate, P, can be determined in the absence of gravity such as during free fall in the vacuum tube of a drop tower. The sedimen- tation rate can be modulated using, for instance, hyper- gravity conditions in a centrifuge. We have performed these types of experiments in different ciliates. I will now briefly summarize some of our experiments and conclusions. 2 3 4 5 6 How is the sedimentation rate determined? We im- Acceleration [g] mobilize cells using up to 1 mM NiCl2 in experimental solution. Individual variations of sedimentation rates of Fig. 4. Gravikinesis in Paramecium as a function of acceleration. Paramecium caudatum are quite large, but mean values Swimming and sedimentation velocities at 5 different values of are near 90 jim/s at 1 g. Applying hypergravity of up to hypergravity between 1.5g and 5.4g were used to calculate graviki- 5.4 g, the sedimentation rate of Paramecium rose in a nesis (A; equation 3). The intersection near Og of linear regressions of upward (corr. coeff. 0.99) and downward velocity (corr. coeff. quasilinear fashion beyond 300 |jm/s (correlation coef- 0.96) were employed for approximation of the intrinsic propulsion ficient 0.995). We cannot infer the sedimentation rates velocity (P) and gravikinesis of upward (AU) and downward swim- ming cells (AD; equations 1, 2). The data suggest that A grows with below 1 g because a linear regression of data points did rising acceleration because the increase in gravikinesis of downward not intersect with zero velocity and zero gravity. swimmers outweighs the decrease in gravikinesis of upward swim- mers (Braucker et al. unpublished). Note that (1) the sign of graviki- How are the velocities of cells measured? Several nesis is negative in the full range of hypergravity tested and (2) strategies exist. We record on video tape fields including regressions do not tend to intersect with the origin of the diagram. Gravikinesis of Paramecium at lg is between -20 |im/s and -90 p.m/s 100 to 300 cells and evaluate by hand tracks from according to the published literature (see Machemer and Braucker digitized, superimposed fields. Typical tracking times 1992)

http://rcin.org.pl 56 H. Machemer

periment of Paramecium, which we have done in the ant. 140m-drop tower of Bremen. A significant difference in rates of upward and downward swimmers at 1 g decayed JAU with the beginning of the free fall and was absent after about 5 s. This would be expected for conditions under fyu Nu weightlessness, where intrinsic propulsion alone deter- mines the swimming rate. Interestingly, the swimming rates during free fall coincided with the rates of horizon- tal swimmers at normal gravity. Our conclusion is that K - corresponding to predictions from the distribution of w mechanically sensitive receptors in Paramecium - horizontal swimming rates at normal gravity are equal Vh to the value of P. With the rates of swimming under weightlessness (P), sedimentation (S) and vertical up and down swimming at 1 g (Vy, V ) given, the B D O Ca-Channel gravikinetic responses can be determined in detail. In all / \ II K-Channe( experiments Ajj and AD had a negative sign, and their absolute values differed from each other. The mean gravikinetic response (A) in Paramecium was small, ranging near 50 |J.m/s which is about 5% of the active |Vd jvd propulsion rate. \ I will now briefly summarize experiments using artificially raised gravity. We have mentioned a (Ad tAd sedimentation rate growing with the g-vector. With Paramecium Didinium gravity rising more than fivefold, the downward swim- ming rates of 3 days old Paramecium increased, and the Fig. 5. Paramecium and Didinium gravikinesis compared diagram- upward swimming rates strongly declined. Interestingly, matically. Cells are depicted as swimming upward (A), horizontally (B) and downward (C; ant. = anterior cell end). Two classes of the horizontal swimming velocities were virtually un- gravireceptor channels are included in the membrane with gradient- changed even at raised gravity. Using the intersection type distributions: Ca-channels (0) and K-channels (II). Heavy arrows give presumed area of membrane deformation due to inside-outside of linear regressions of downward and upward swim- density differences. Light arrows: forward swimming rates (Vu, Vh, ming rates for approximation of the gravity-free propul- Vd) and inferred gravikinetic components (Ay, Ah, Ad) incorporated in the observed velocities. Note that a gravikinetic response can add sion (P), and the regression lines of sedimentation, to or subtract from the intrinsic cell propulsion. In Paramecium upward and downward swimming, we calculate the gravikinesis always acts to reduce effects of sedimentation. Data in Didinium suggest that hyperpolarizing gravireceptor channels are gravity-dependent kinetic responses of Paramecium absent; therefore, propulsion is slightly depressed under gravity irre- (Fig. 4). It is seen that negative values of gravikinesis, spective of orientation (Braucker et al. unpublished) that is an active motor response antagonizing sedimen- tation, persisted or even grew well beyond 150 |nm/s that we cannot expect a gravikinesis from hyperpolari- with 5-fold gravity. zation-dependent ciliary activation. Is the gravikinetic behaviour of Paramecium repre- The swimming rates of Didinium at normal gravity, sentative of many or even all ciliates? In order to answer horizontal and vertical rates, and the swimming rates this question, we investigate the electrophysiology and during weightlessness were investigated. Horizontal behaviour in different ciliates. Here, I will briefly men- swimmers of opposite field sectors swam at the same tion the graviresponses in Didinium, which is a well rate at 1 g. After about 5 s of weightlessness during free known predator of Paramecium. Didinium differs from fall in the drop tower, the vertical velocity differences Paramecium in that it does not generate hyperpolarizing subsided as expected. However, the swimming rates receptor potentials with posterior mechanostimulation during the free fall were significantly higher than the (Pernberg, unpublished observations), and its cilia do horizontal swimming rates. This suggests, in agreement not respond to hyperpolarization under voltage clamp with the electrophysiological hypothesis of gravikinesis, (Mogami et al. 1990). An implication of this finding is that in horizontally swimming Didinium at normal gravity, the excitatory motor component of gravistimula-

http://rcin.org.pl Gravity-dependent Swimming Rate in Ciliates 57

tion, hyperpolarization, is missing, whereas the in- REFERENCES hibitory motor component, depolarization, persists. Removal of the inhibitory depolarization under weight- Batschelet E. (1981) Circular statistics in Biology. In: Mathematics lessness conditions, therefore, speeded up Didinium. in Biology, (Eds. R. Sibson, J. E. Cohen). Academic Press, I close this short presentation with a scheme which London, New York Fetter D. (1926) Determination of the protoplasmic viscosity of attempts to explain the observed gravikinetic behaviour Paramecium by the centrifuge method. J. Exp. Zool. 44: 279-283 of Paramecium and Didinium at the level of membrane Koehler O. (1922) Uber die Geotaxis von Paramecium. Arch. Proti- stenkd. 45: 1-94 channels (Fig. 5). In upward swimming Paramecium, Kuroda K., Kamiya N. (1989) Propulsive force of Paramecium as gravity acts to open gravireceptor K channels at the revealed by the video centrifuge microscope. Exp. Cell Res. 184: posterior cell end, the cell hyperpolarizes and the cilia, 268-272 Machemer H. (1986) Electromotor coupling in cilia. In: Membrane by raising the frequency of their beating, generate an control of cellular activity, (Ed. H. C. Liittgau). Fortschr. Zool. increment in upward swimming rate, Ay, which an- 33: 205-250 Machemer H., Braucker R. (1992) Gravireception and graviresponses tagonizes sedimentation. In horizontally swimming in ciliates. Acta Protozool. 31: 185-214 Paramecium, both gravireceptor K and Ca channels are Machemer H., Braucker R., Takahashi K., Murakami A. (1992) Short-term microgravity to isolate graviperception in cells. activated with a conductance ratio which corresponds to Proceedings of a workshop "Drop Tower Days 1992", Bremen. that of the resting potential. Hence, no change in ciliary Microgravity Sci. Technol. 5: 119-123 Machemer H., Braucker R., Murakami A., Yoshimura K. (1993) frequency occurs. In downward swimming Para- Graviperception in unicellular organisms: a comparative beha- mecium, anterior gravireceptor Ca channels activate; the vioural study under short-term microgravity. Microgravity Sci. membrane depolarizes depressing the rate of ciliary Technol. 5:221-231 Machemer H., Machemer-Rohnisch S., Braucker R., Takahashi K. beating. This decrement in downward swimming rate, (1991) Gravikinesis in Paramecium: Theory and isolation of a physiological response to the natural gravity vector. J. Comp. AD, antagonizes sedimentation. Physiol. A 168: 1-12 Our data in Didinium agree with the general scheme Mogami Y., Pernberg J., Machemer H. (1990) Messenger role of of Paramecium with two exceptions: (1) there exist no calcium in ciliary electromotor coupling: a reassessment. Cell Calcium 11: 665-673 hyperpolarizing gravireceptor channels; (2) gravity-in- Ogura A., Machemer H. (1980) Distribution of mechanoreceptor duced inward as well as outward deformation of the channels in the Paramecium surface membrane. J. Comp. Physiol. 135: 233-242 membrane can generate depolarizing gravireceptor Taneda K. (1987) Geotactic behavior in Paramecium caudatum. I. potentials. Thus, with the pull of gravity, swimming in Geotaxis assay of individual specimen. Zool. Science 4: 781-788 any direction is slightly inhibited. Only under conditions Volkmann D. (1974) Amyloplasten und Endomembranen: Das Geoperzeptionssystem der Primarwurzel. Protoplasma 79: 159- of weightlessness is this inhibition of ciliary activity 183 removed so that the Didinium cell swims faster than at Received on 21 st October, 1993 terrestrial gravity.

http://rcin.org.pl http://rcin.org.pl ACTA Acta Protozoologica (1993) 33: 59 - 65 PROTOZOOLOGICA

Effects of Solar Radiation on Motility, Orientation, Pigmentation and Photosynthesis in a Green Dinoflagellate Gymnodinium

Jochen SCHÂFER, Claudia SEBASTIAN and Donat-P. HÀDER

Institut fiir Botanik und Pharmazeutische Biologie, Friedrich-Alexander-Universitàt, Erlangen, Germany

Summary. The effects of solar radiation on motility, orientation to light and gravity as well as pigmentation and photosynthetic and respiratory oxygen exchange have been analyzed in the dinoflagellate, Gymnodinium, Y-100. Exposure to unfiltered solar irradiation impaired motility (percentage of motile cells) within 130 min while the average swimming velocity of the remaining motile cells was hardly affected. The cells show exclusive positive phototaxis, the precision of which decreases strongly with exposure time to solar radiation. In a vertical cuvette the cells show positive gravitaxis which soon becomes random after short exposure times; longer exposure causes the cells to switch to positive gravitaxis, which may be an escape mechanism from excessive radiation. The photosynthetic pigments are gradually bleached by solar radiation. Photosynthetic oxygen production is impaired even on a shorter time scale, while respiration is not as much affected.

Key words. Dinoflagellate, gravitaxis, Gymnodinium, photosynthesis, phototaxis, solar radiation, swimming velocity.

INTRODUCTION Thus, they optimize their position, finding a compromise between optimal photosynthesis and pigment bleaching. Dinoflagellates are among the most important Some freshwater and marine organisms use positive biomass producers in the oceans (Taylor 1987). Most phototaxis at low fluency rates to move upward in the photosynthetic dinoflagellates are capable of active water column (Eggersdorfer and Hader 1991a, b). Often movement and optimize their position in the water the upward movement by positive phototaxis is sup- column by orienting with respect to external factors. ported by negative gravitaxis (Hader and Liu 1990a, b). Many phytoplankton organisms cannot tolerate bright In some cases the upward movement is balanced by a solar radiation encountered at the surface and their downward movement mediated by negative phototaxis pigments are bleached within hours or days (Nultsch and at high fluence rates (Rhiel et al. 1988). In contrast, Agel 1986, Hader et al. 1988). On the other hand, they several freshwater and marine dinoflagellates have been cannot move too far down in the water column because found to show diaphototaxis (movement perpendicular of their dependence on sunlight for energetic reasons. to the incident light beam) at higher fluence rates which is an effective means to stay at a selected level (Liu et al. 1990, Eggersdorfer and Hader 1991a). On top of Address for correspondence: D.-P. Häder, Institut für Botanik these orientation mechanisms many phytoplankton or- und Pharmazeutische Biologie, Friedrich-Alexander-Universität, Staudtstr. 5, D-91058 Erlangen, Germany. ganisms undergo vertical diurnal migrations, and

http://rcin.org.pl 60 J. Schafer et al. dinoflagellates have been found to move up to 15 m up Any inhibition of motility and orientation of and down the water column (Burns and Rosa 1980). phytoplankton organisms by solar ultraviolet radiation In addition to phototaxis (orientation with respect to is bound to be detrimental for growth and survival of the light direction, Diehn et al. 1977) some organisms the population in its habitat. Furthermore, any increase use photokinesis (dependence of the swimming velocity in solar UV-B radiation due to a partial reduction of the on the steady state light intensity, Wolken and Shin 1958) stratospheric ozone layer caused by the production and and/or both step-up and step-down photophobic respon- emission of anthropogenic gaseous pollutants such as ses (transient directional changes upon sudden changes CFCs (Madronich et al. 1991) bears the risk of reducing in the fluence rate, Doughty and Diehn 1983, 1984). In the biomass production of phytoplankton. addition to light, other organisms have been found to The aim of this paper is to characterize the effects of utilize different physical and chemical external stimuli solar ultraviolet radiation on motility and the orientation to orient within their microhabitat such as chemical and strategies with respect to light and gravity in the marine thermal gradients (MacNab 1985, Poff 1985), the mag- dinoflagellate, Y-100. Furthermore, the effects of solar netic field of the earth (Esquivel and de Barros 1986) radiation on pigmentation and photosynthesis are studied. and even electric currents (Mast 1911). Enhanced solar radiation has been shown to impair MATERIALS AND METHODS motility and swimming velocity in a number of flagel- lates and also gliding organisms. In addition, the orien- Organism and culture tation mechanisms with respect to light are affected (Hader and Worrest 1991). The degree of inhibition is The dinoflagellate, Gymnodinium Y-100, was a gift lower, when the short wavelength radiation is removed from Dr. Elbrachter and used for all experiments by cut-off filters or by inserting an artificial layer of described in this article. The cells were inoculated into ozone. Furthermore, artificial ultraviolet radiation has 40 ml of a medium described recently (Guillard and been found to induce similar effects (Hader and Hader Ryther 1962) kept in 100 ml Erlenmeyer flasks. The 1990a, Hader et al. 1990), indicating that the ultraviolet cultures were grown for about 1-2 weeks under con- component is a major stress factor for phytoplankton tinuous light of about 2.5 W m " from mixed cool white organisms. Similarly, gravitaxis was affected in a num- and warm tone fluorescent lamps at about 23° C. Cell ber of flagellates (Hader and Liu 1990a, b), indicating suspensions were removed from the cultures and sub- that the orientation is mediated by an active physiologi- jected to solar irradiation in their growth medium. cal receptor organelle rather than by a passive physical process (Brinkmann 1968). Solar irradiation Many UV-B effects are caused by DNA absorption (Yamamoto et al. 1983), leading to the formation of Cell suspensions were exposed to solar radiation in thymine dimers. However, for some responses DNA could open plastic Petri dishes at the research station Quinta be ruled out as a primary UV-B target and also de Sao Pedro, Monte de Caparica, south of Lisbon (38° photodynamic reactions were found not to be involved North) on sunny days between 20.07. and 1.08.1992 (Hirosawa and Miyachi 1983, Hader et al. 1986), suggest- between 10.30 and 15.00 h local time. The organisms ing that specific proteins of the photoreceptor and motor were placed inside a temperature controlled growth organelles were affected by increased ultraviolet radia- chamber, the Plexiglas roof of which transmitted >92% tion. And indeed, spectroscopic and biochemical studies of solar radiation between 280 and 750 nm. The spectral have revealed that specific proteins were destroyed under distribution and the fluence rates of solar radiation were the influence of ultraviolet radiation (Hader and Brodhun measured by the group of Prof. Tevini with a double 1991, Zundorf and Hader 1991, Haberlein and Hader monochromator spectroradiometer (model 742, 1992). In addition, the chromophoric groups of the pig- Optronic, Orlando, Fla.). ments are bleached as shown by spectroscopic investiga- tions. Pigment bleaching and other damages of the Image analysis of motility and orientation photosynthetic apparatus result in reduced photosynthetic oxygen production (Zundorf and Hader 1991). Especially Samples were taken at regular time intervals during sites in photosystem II have been identified as primary exposure to solar radiation for motility and orientation UV-B targets (Renger et al. 1989). measurements. Gravitaxis of the flagellates was meas-

http://rcin.org.pl UV Effects in a Dinoflagellate 61 ured in darkness in a flat glass cuvette (60x8x0.17 mm closed with lids and parafilm to avoid evaporation and inner dimensions) placed on the stage of a horizontally thus volume changes. A baseline was determined with a oriented microscope (Olympus BH2) with a 2.5x objec- cuvette each in the sample and reference compartment, tive. A dark field condensor was used to enhance the respectively, to abolish all possible optical differences contrast and the microscope light beam was filtered between the two. Subsequently the sample cuvette was through an infrared cut-off filter (RG 715, Schott & exposed to solar radiation and difference spectra were Gen., Mainz, FRG) to be used as an IR measuring beam. recorded at regular time intervals. By this method the Infrared monitoring of the cells allowed to avoid orien- bleached pigments appear as negative peaks. Another tation of the cells with respect to the measurement beam; advantage of this method is that exclusively real absorp- furthermore, the cells in the microscope focus did not tion changes are detected while differences in scattering produce oxygen photosynthetically which otherwise are excluded. might have attracted cells from the outside due to their pronounced aerotaxis. The image of the moving cells Photosynthetic oxygen production was recorded by an infrared sensitive CCD b/w camera (LHD 0600, Philips, The Netherlands) mounted on top Photosynthetic oxygen production was measured in a of the microscope. The video signal was digitized on Plexiglas cylinder with 20 mm inner diameter thermally line in real time by a framegrabber (Matrox, PIP 1024, stabilized by a water jacket connected to a thermostat Quebec, Canada) accommodated in an IBM AT com- (25 °C, RMT6, Dr. Wobser GmbH, Lauda-Königshofen, patible microcomputer (Deskpro 386/25, Compaq, Scot- Germany). The sample compartment held 5 ml cell land). Digitization was performed with a spatial suspension agitated by a magnetic stirrer and was sealed resolution of 512x512 pixels at 256 possible grey levels. with a Clark electrode (Yellow Springs Instruments, Yel- The software package has been written in the computer low Springs, Ohio, USA) (Dubinsky et al. 1987). The language C (Hader and Vogel 1991) but time critical electrode was connected via a custom-made polarizer calculations such as the determination of position and (Estabrook 1967) with a recorder (PM 8262, Philips). outline of the organisms were performed in Assembly Calibration was done with 10 mM sodium dithionite for language using the chain code algorithm (Freeman 1974, the 0% oxygen saturation and the 100% value was 1980). The raw data were stored in form of movement measured after bubbling air through the medium. vectors of the cells reflecting the individual swimming Photosynthesis was induced by white light produced from speed and the deviation from the stimulus direction. a 250 W slide projector with a 24 V quartz halogen bulb Subsequent programs were developed for statistical and (Kindermann Universal). mathematical analysis to quantify the precision of orien- All experiments were repeated at least four times on tation. The computer program also recorded the percent- different days. However, as in ecological experiments age of motile cells. day-to-day changes in visible and specifically ultraviolet Phototaxis was measured with the same hardware and radiation levels are unavoidable the data were not software system as gravitaxis in a horizontal cuvette averaged and the standard error calculated but rather placed on the stage of a vertically oriented microscope. representative single experiments are shown. The actinic light beam was produced from a 250 W slide projector equipped with a 24 V quartz halogen bulb RESULTS (Kindermann Universal, Wetzlar, Germany) and entered the cuvette at an angle of 12° above the surface. The In the horizonal cuvette the cells showed a high irradiance was measured with a Mavolux radiometer precision of phototactic orientation when irradiated (Gossen, Erlangen, FRG). laterally at an irriadiance of 50 W m" (Fig. la). The Rayleigh test (Batschelet 1965, 1981) gave an r-value Absorption spectroscopy of 0.70. When exposed to unfiltered solar radiation this high precision of orientation was maintained for about In vivo absorption spectra were measured with a dual 40 min. After 75 min the r-value of phototactic orienta- beam spectrophotometer (UV240, Shimadzu, tion had decreased to 0.51 (Fig. lb) and after 105 min Düsseldorf, Germany). The cells were immobilized in a to 0.25 (Fig. lc). After 125 min the motile cells moved 0.7% agar prepared from medium. Two quartz cuvettes completely randomly as indicated by the standard were filled bubble free with the same suspension and Rayleigh test for directionality (Fig. Id). Quantification

http://rcin.org.pl 62 J. Schafer et al.

least the same time (data not shown). The percentage of motile cells decreased steadily with increasing exposure time (Fig. 3), while the average swimming velocity of the motile fraction was not as much affected (Fig. 4). When the UV component of solar radiation is removed by a GG 400 cut-off filter the effect of solar radiation on orientation and motility is less dramatic even though also visible radiation affects these processes (data not 270' 90' shown). When the cells were exposed to a point that their motility had decreased to zero there was no 270° regeneration even when the cells were kept for 24 h in

180° 180" darkness or dim white light indicating that there is no reversibility after UV exposure. After short term ex- posure (10 min) there was a partial recovery after 24 h.

In a vertical cuvette the cells showed negative gravitaxis (upward movement in the water column) with an r-value of about 0.35. Even after short exposure to unfiltered solar radiation the precision of gravitactic orientation declined (Fig. 5) and the cells moved ran- domly. Visual inspection of the moving track indicated that the cells actually moved in a random fashion as opposed to half of the cells moving upward and half 270° downward. After about 100 min the cells started moving downward in the water column (positive gravitaxis) with 180° 180 increasing r-values until after 160 min no motile cell was 2 Fig. 1. Histograms of positive phototaxis to 50 W m " in Gymnodi- found. The downward movement is mediated by active nium after 0 (a), 75 (b), 105 (c) and 125 (d) min of unfiltered solar swimming and not by passive sedimentation. Control radiation populations kept in darkness continued to show negative 0.9 -| gravitaxis with a high degree of precision for several 0.8 - hours (data not shown). Absorption difference spectra showed a gradual ZJ 0.7 - 0.6 - | in the absorption range of the carotenoids and the 0.5 - chlorophylls (Fig. 6). Furthermore there is a gradual

http://rcin.org.pl UV Effects in a Dinoflagellate 63

100 300

250 -

200 - E a. ~ 150 -

o £ 100 - >

50

t r 25 50 75 100 125 150

Exposure time [min] Exposure time [min] Fig. 3. Effects of unfiltered solar radiation on the percentage of motile Fig. 4. Effects of unfiltered solar radiation on the average swimming cells in Gymnodinium velocity of motile cells in Gymnodinium less affected by solar radiation when the UV component was removed. After short term exposure there was some recovery: oxygen production commenced within about 30 min. After long term exposure no recovery could be observed within the next few hours.

DISCUSSION

In the water column, the dinoflagellate, Gym- nodinium Y-100, moves upward by using light as an 100 150 200 external stimulus (positive phototaxis). The precision of orientation increases with light intensity (Tirlapur et al. Exposure time [min] 1993). In contrast to other flagellates, which show posi- Fig. 5. Effects of unfiltered solar radiation on the direction and precision (r-value) of gravitactic orientation in Gymnodinium. Nega- tive phototaxis at low fluence rates and negative one at tive gravitaxis (circles) is plotted above zero and positive gravitaxis higher (Hader et al. 1988), this organism shows ex- (squares) below (although, mathematically speaking, the r-value is always positive) clusively positive phototaxis. Other dinoflagellates, both marine and freshwater, use a different strategy of orien- tation and show a positive phototaxis at low fluence rates but diaphototaxis (movement perpendicular to the inci- dent light beam) at higher, which effectively keeps the cells at a level of suitable light intensities (Liu et al. 1990, Eggersdorfer and Hader 1991a). Gravitactic orien- tation is similar to that of many other flagellates being negative in unstressed cells (Hader and Liu 1990a, b). The orientation pattern of this organism is surprising, 1 1—1 1 1 1 T since both phototaxis and gravitaxis will take the cells 350 400 450 500 550 600 650 700 750 to the surface, where they are exposed to the bright Wavelength [nm] unfiltered solar radiation, which is known to bleach and eventually kill many phytoplankton organisms (Hader Fig. 6. Absorption difference spectra calculated by subtracting the spectrum of an unexposed sample from the spectra of samples expo- and Hader 1990b, Hader and Worrest 1991). However, sed to solar radiation after increasing times

http://rcin.org.pl 64 J. Schafer et al.

" 0.008 excessive UV-A and visible radiation exert inhibitory c E 0.006 effects on motility, orientation and photosynthesis in this and other phytoplankton organisms (Hader and Worrest = 0.004 a> 1991). o _ 0.002 In summary, the inhibition of motility, swimming o velocity and orientation mechanisms by enhanced levels a. 0.000 of solar radiation diminishes the ability of the popula- O -0.002 tions to grow and survive under stress conditions. Any increase in solar UV-B radiation caused by a reduction •=o -0.004 o of the ozone layer due to the emission of anthropogenic £ -0.006 gaseous pollutants (Madronich et al. 1991) will affect the productivity and thus adversely affect the whole o -0.008 0 5 10 15 20 25 biological food web (El Sayed 1988). This is in accord- Exposure time [mini ance with the findings that in situ photosynthetic produc- Fig. 7. Effects of unfiltered solar radiation (squares) and solar tivity of natural phytoplankton populations is drastically radiation from which the ultraviolet radiation has been removed decreased under the Antarctic ozone hole (Smith et al. (circles) on photosynthetic oxygen production (open symbols) eli- cited by a test light at 333 W m"2 and respiration (closed symbols) 1992, Vosjan et al. 1990, Karentz et al. 1991). in Gymnodinium Acknowledgements. This work was supported by financial support from the Bundesminister fur Forschung und Technologie (project KBF a similar behavior has been found in another dinoflagel- 57), the European Community (EV5V-CT91-0026) and the State of late, Gyrodinium, which exclusively moves upwards in Bavaria (BayFORKLIM, Dili 1) to D.-P. Hader. The authors grate- the water column (Ekelund and Hader 1988) and which fully acknowledge the skilful technical assistance of B. Kiihl, indeed is bleached by light at higher fluence rates. M. Peschke and V. Zuniga-Ostwald and the friendly help of A. Pircher, This orientation mechanism is difficult to understand manager of the research station Quinta de Sao Pedro, Sobreda in on an ecological basis since the current results indicate Portugal. that motility and orientation mechanisms with respect to light and gravity are strongly affected by even moderate REFERENCES exposure to unfiltered solar radiation. This leads to the Batschelet E. (1965) Statistical methods for the analysis of problems question of how the cells escape detrimental radiation in animal orientation and certain biological rhythms. In: Animal at the surface. Some dinoflagellates have been observed Orientation and Navigation (Eds. S.R. Galles, K. Schmidt-Koe- nig, G.J. Jacobs, R.F. Belleville), NASA, Washington, 61-91 to passively sediment when exposed to excessive Batschelet E. (1981) Circular Statistics in Biology. Academic Press, ultraviolet radiation (Hader and Liu 1990a). In contrast, London Gymnodinium Y-100 seems to utilize an active escape Brinkmann K. (1968) Keine Geotaxis bei Euglena. Z. Pflanzenphy- siol. 59: 12-16 mechanism by downward swimming (positive gravi- Burns N. M., Rosa F. (1980) In situ measurements of the settling taxis). velocity of organic carbon particles and ten species of phytoplank- ton. Limnol. Oceanogr. 2: 855-864 This escape behavior is probably ecologically sig- Diehn B„ Feinleib M., Haupt W„ Hildebrand E., Lenci F„ Nultsch, nificant since photosynthesis is strongly affected by W. (1977) Terminology of behavioral responses of motile micro- organisms. Photochem. Photobiol. 26: 559-560 solar radiation. This inhibition is even more rapid than Doughty M. J., Diehn B. (1983) Photosensory transduction in the the effect on motility and orientation. Since the absorp- flagellated alga, Euglena gracilis. IV. Long term effects of ions and pH on the expression of step-down photobehavior. Arch. tion difference spectra show massive bleaching only Microbiol. 134: 204-207 after longer exposure times it can be assumed that Doughty M. J., Diehn B. (1984) Anion sensitivity of motility and photosynthesis is affected by structural changes in the step-down photophobic responses of Euglena gracilis. Arch. Mi- crobiol. 138:329-332 photosynthetic apparatus as has been detected also in Dubinsky Z., Falkowski P. G., Post A.F., van Hes U.M. (1987) A higher plants (Renger et al. 1989, Tevini et al. 1989). system for measuring phytoplankton photosynthesis in a defined light field with an oxygen electrode. J. Plankton Res. 9: 607-612 The decrease in absorption at shorter wavelength may Eggersdorfer B., Hader D.-P. (1991a) Phototaxis, gravitaxis and reflect a loss in scattering indicating a partial lysis of vertical migrations in the marine dinoflagellates, Peridiniumfae- roense and Amphidinium caterii. Acta Protozool. 30: 63-71 cells after extended periods of solar exposure. UV-B Eggersdorfer B., Hader D.-P. (1991b) Phototaxis, gravitaxis and radiation is responsible for part of the inhibition by solar vertical migrations in the marine dinoflagellate, Prorocentrum radiation as indicated by a study which used artificial micans. Eur. J. Biophys. 85: 319-326 Ekelund N., Hader D.-P. (1988) Photomovement and photobleaching ultraviolet radiation (Tirlapur et al. 1993). However, also in two Gyrodinium species. Plant Cell Physiol. 29: 1109-1114

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Surv. 6: 57-97 surface. Environmental Effects Panel Report, United Nations, Freeman H. (1980) Analysis and Manipulation of Lineal Map Data. Environmental Program, 1-13 Map Data Processing. Academic Press, 151-168 Mast S. O. (1911) Light and Behavior of Organisms. John Wiley & Guillard R. R. L., Ryther J. H. (1962) Studies of marine planktonic Sons, New York diatoms. I Cyclotella nana Hustedt and Detonula confervacea Nultsch W., Agel G. (1986) Fluence rate and wavelength dependence (Cleve) Gran. Can. J. Microbiol. 8: 229-239 of photobleaching in the cyanobacterium Anabaena variabilis. Haberlein A., Hàder D.-P. (1992) UV effects on photosynthetic Arch. Microbiol. 144: 268-271 oxygen production and chromoprotein composition in a freshwa- Poff K. L. (1985) Temperature sensing in microorganisms. In: Sen- ter flagellate Cryptomonas. Acta Protozool. 31: 85-92 sory Perception and Transduction in Aneural Organisms (Eds. G. Hàder D.-P., Brodhun B. ( 1991 ) Effects of ultraviolet radiation on the Colombetti, F. Lenci, P.-S. Song). Plenum Press, New York, photoreceptor proteins and pigments in the paraflagellar body of London, 299-307 the flagellate, Euglena gracilis. J. Plant Phys. 137: 641-646 Renger G., Völker M., Eckert H. J., Fromme R., Hohm-Veit S., Hàder D.-P., Hàder M. (1990a) Effects of UV radiation on motility, Gräber P. (1989) On the mechanisms of photosystem II deterio- photo-orientation and pigmentation in a freshwater Cryptomonas. ration by UV-B irradiation. Photochem. Photobiol. 49: 97-105 J. Photochem. Photobiol. B: Biol. 5: 105-114 Rhiel E„ Häder D.-P., Wehrmeyer W. (1988) Photoorientation in a Hàder D.-P., Hàder M. (1990b) Effects of solar radiation on motility, freshwater Cryptomonas species. J. Photochem. Photobiol. B.- photomovement and pigmentation in two strains of the cyanobac- Biol. 2: 123-132 terium, Phormidiutn uncinatum. Acta Protozool. 29: 291-303 Smith R. C„ Prezelin B. B„ Baker K. S., Bidigare R. R„ Boucher N. Hàder D.-P., Liu S.-M. (1990a) Effects of artificial and solar UV-B P., Coley T., Karentz D., Maclntyre S., Matlick H. A., Menzies radiation on the gravitactic orientation of the dinoflagellate, Peri- D„ Ondrusek M., Wan Z„ Waters K. J. (1992) Ozone depletion: dinium gatunense. F EMS Microbiol. Ecol. 73: 331-338 Ultraviolet radiation and phytoplankton biology in Antarctic wa- Hàder D.-P., Liu S.-M. (1990b) Motility and gravitactic orientation ters. Science 255: 952-959 of the flagellate, Euglena gracilis, impaired by artificial and solar Taylor F. J. R. (Ed.) (1987) The biology of dinoflagellates. Blackwell UV-B radiation. Curr. Microbiol. 21: 161-168 Scientific Publications, Oxford, UK. Hàder D.-P., Vogel K. ( 1991 ) Simultaneous tracking of flagellates in Tevini M., Teramura A. H., Kulandaivelu G., Caldwell M. M., Björn real time by image analysis. J. Math. Biol. 30: 63-72 L. O. (1989) Terrestrial Plants. UNEP Environmental Effects Hàder D.-P., Worrest R.C. (1991) Effects of enhanced solar ultravio- Panel Report, 25-37 let radiation on aquatic ecosystems. Photochem. Photobiol. 53: Tirlapur, U., Scheuerlein, R„ Häder D.-P. (1993) Motility and orien- 717-725 tation of a dinoflagellate, Gymnodinium, impaired by solar and Hàder D.-P., Rhiel E., Wehrmeyer W. ( 1988) Ecological consequen- ultraviolet radiation. FEMS Microbiol. Ecol. 102: 167-174 ces of photomovement, photobleaching in the marine flagellate Vosjan J. H„ Döhler G„ Nieuwland G. (1990) Effect of UV-B Cryptomonas maculata. FEMS Microbiol. Ecol. 53: 9-18 irradiance on the ATP content of microorganisms of the Weddell Hàder D.-P., Watanabe M., Furuya M. (1986) Inhibition of motility Sea Antarctica. Neth. J. Sea Res. 25: 391-394 in the cyanobacterium, Phormidium uncinatum, by solar and Wolken J. J., Shin E. (1958) Photomotion in Euglena gracilis. I monochromatic UV irradiation. Plant Cell Physiol. 27: 887-894 Photokinesis II Phototaxis. J. Protozool. 5: 39-46 Hàder D.-P., Liu S.-M., Hàder M., Ullrich W. (1990) Photoorienta- Yamamoto K. M., Satake M., Shinagawa H., Fujiwara, Y. (1983) tion, motility and pigmentation in a freshwater Peridinium affec- Amelioration of the ultraviolet sensitivity of an Escherichia coli ted by ultraviolet radiation. Gen. Physiol. Biophys. 9: 361-371 recA mutant in the dark by photoreactivating enzyme. Mol. Gen. Hirosawa T., Miyachi S. (1983) Inactivation of Hill reaction by Genet. 190:511-515 long-wavelength ultraviolet radiation (UV-A) and its photoreac- Zündorf I., Häder D.-P. (1991) Biochemical and spectroscopic ana- tivation by visible light in the cyanobacterium, Anacystis nidu- lysis of UV effects in the marine flagellate Cryptomonas macula- lans. Arch. Microbiol. 135: 98-102 ta. Arch. Microbiol. 156: 405-411 Karentz D„ Cleaver J. E„ Mitchell D. L. (1991) DNA damage in the Antarctic. Nature 350: 28 Received on 12th July, 1993; accepted 30th September, 1993

http://rcin.org.pl ANNOUNCEMENT

DIRECTORY OF PARASITOLOGISTS

Electronic communications provide a rapid means of obtaining information from or sending information to colleagues involved in parasitological research. However, there is currently no centralized "directory" that provides the e-mail addresses and FAX numbers of parasitologists. I believe that such a directory would benefit parasitologists, and I am therefore beginning to put together such a directory. I invite aii those individuals involved in parasitological research to communicate with me so your names can be included in this new directory.

In addition to e-mail addresses and FAX numbers, this new directory will also include mailing addresses, telephone numbers, research interests, etc. As the directory grows and is updated, it will be sent electronically to everyone whose name appears in it (and who has provided an e-mail address), thus providing parasitologists with the most current information available. For those individuals not currently using electronic mail, I plan to make the directory available on disk at a later date.

Interested readers can contact me via e-mail, and I will forward additional information (a questionnairel to them. Readers who do not currently have an email address but wish to be included in the directory can contact me via mail or FAX.

Sincerely,

Peter W. Pappas The Ohio State University Department of Zoology 1735 Neil Avenue Columbus, OH 43210-1293 USA

E-mail: [email protected] FAX: 614-292-2030

http://rcin.org.pl ACTA Acta Protozoologica (1993) 32: 67 - 70 PROTOZOOLOGICA

In Vitro Excystation of Gregarina blattarum Oocysts

Kazumi HOSHIDE*, Hiroyuki NAKAMURA* and Kenneth S. TODD, Jr.**

^Biological Institute, Faculty of Education, Yamaguchi University, Yamaguchi, Japan; **Department of Veterinary Pathobiology, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA

Summary. Excystation of sporozoites from Gregarina blattarum oocysts was observed with light and scanning electron microscopy. When digestive tracts extracts were added to oocysts, the sporozoites became activated and emerged. Two or three holes surrounded by projections were observed in the surface of oocyst walls just after sporozoites had excysted. Oocysts were able to excyst for at least 10 days after being desiccated.

Key words. Gregarina blattarum, gametocyst, oocyst, sporozoite, excystation, SEM.

INTRODUCTION Ten B. germanica were decapitated and dissected. The digestive tracts were removed, placed in 1 ml of Ringer's solution and homo- genized with a glass microhomogenizer. The mixture was centrifuged It has been reported that the sporozoites of some at 2000 x g for 2 min and filtered with a Millipore filter with 0.45 m gregarines excyst from oocysts after the addition of the pores. The filtrate was used as the extract of digestive tracts. host's digestive fluids (Canning 1956; Janardanan and Gametocysts of G. blattarum were collected from the feces of B. Ramachandran 1979, 1982). We investigated the process germanica and placed in distilled water on a glass slide which was of sporozoite excystation from the oocysts of Gregarina kept in a moist chamber for 2 or 3 days. The oocysts on the slide were blattarum with light and scanning electron microscopy divided. Each half was transferred to a different slide and two drops of Ringers's solution was added to one half and two drops of the after adding the extracts from the digestive tract. The digestive tract extract was added to the other half. The slides were resistance of the oocysts to desiccation was also studied. covered with a cover-glass which was sealed around the edges with a Terminology used was that proposed by Levine (1971). balsam-paraffin resin. The samples were examined with a light mic- roscope every 20 min. MATERIALS AND METHODS The oocyst from which the sporozoites had excysted were exami- ned with a scanning electron microscope. The specimens were prefi- xed in a 5% glutaraldehyde solution, rinsed several times with The cockroach, Blattella germanica used in this experiment came cacodylate buffer and dehydrated with an ethanol series. They were from a culture that has been maintained in our laboratory and origina- then placed in isoamylacetate and further dehydrated by the critical ted from Fumakilla Inc., Japan. point method using CCh as the transition liquid. Dried samples were attached to aluminum stubs and sputtered with gold using a JEOL 40 unit. Specimens were observed with a JEOL T-300 scanning electron microscope. Address for correspondence: K. Hoshide, Biological Institute, Faculty of Education, Yamaguchi University, Yamaguchi 753, The resistance of the oocysts to desiccation was examined. Oocysts Japan. were transferred to 3 slides and each slide was dried for 1,5 and 10

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100H171

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Figs. 1-4. Gregarina blattarum gametocyst. 1 - immature with a constriction, 2 - mature, 3 - mature with sporoducts inside the wall, 4 sporoducts extended

Figs. 5-6. Gregarina blattarum oocyst. 5 - chains of oocyst just after extrusion, 6 - individual oocyst several hours after extrusion http://rcin.org.pl Excytation of Gregarina blattarum 69

Figs. 7-8. Gregarina blattarum oocyst. 7 - vibrating oocyst 2 h after adding the digestive tract extract, 8 - rotational or spiral movement of oocyst 5 h after adding the extract. Sporozoites partially emerged from the oocyst days. After desiccation the digestive tract extract was added and the oocysts were examined for excystation with light microscopy. The experiment was done in room temperature, approximately at 25°C.

Figs. 9-10. Gregarina blattarum oocyst. 9 - oocyst with protuberance RESULTS (SEM), 10 - oocyst with several holes (SEM)

Gametocyst were spherical to slightly ellipsoidal and had thick gelatinous walls. Immediately after passing in the feces of B. germanica, a constriction was clearly visible at the center of the gametocysts (Fig. 1). The stricture usually disappeared and the endoplasm became homogeneous within 5 h (Fig. 2). Oocysts and sporoducts were formed inside the gametocysts (Fig. 3). After 2-4 days of storage in a moist chamber the gametocysts formed 6-12 external sporoducts and the oocysts were extruded through them (Fig. 4). The oocysts were initially in chains but became separated within a few hours (Figs. 5, 6). When Ringer's solution was added, oocysts remained unchanged for several hours. Two hours after the addi- tion of digestive tract extract many oocysts began to move (Fig. 7). At that time the thread-like sporozoites were observed inside vibrating oocysts. After 5 h several oocysts began to rotate or spin. At that time, the . Excysted sporozoites (SEM) sporozoites were partially outside the oocysts and violent movement of sporozoites caused a rotational or and appeared transparent with light microscopy. The spiral movement of the oocysts (Fig. 8). The sporozoites protuberances were observed with a scanning electron were elongated cylinders and constricted at the middle microscope (Fig. 9), and two or three holes were ob- (Fig. 11). Free sporozoites moved rapidly away from the served on the surface of the oocyst walls. The holes were oocysts. Oocysts from which the sporozoites had ex- irregularly distributed with some at the middle of the cysted had one or two protuberances on their surface oocysts and others at the tips (Fig. 10).

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The tolerance of the oocyst for desiccation was ex- tivate the sporozoites or weaken the wall of the oocyst. amined by adding digestive tract extracts. When the The property of activation by the extract of the digestive extract was added to the oocysts which were dried for tract may be connected with host specificity. 1, 5 or 10 days, the sporozoites excysted from the One or two protuberances were observed on the oocysts. It took a longer time compared to nondesiccated surface of the oocyst shortly after excystation. The oocysts but they hatched normally. The oocysts which projections protruded from the inside and was the part were dried for 5 or 10 days took 7 to 10 h to excyst. of endoplasm of the oocyst which emerged with the sporozoites. The sporozoites were elongate cylinders and had constrictions at the middle of the bodies. The DISCUSSION shape of the sporozoite of G. blattarum is similar to that of Schneideria schneidrae described by Da Cunha and Gregarina blattarum is a typical cephaline gregarine Jurand (1978). (Siebold 1839, Watson 1916). It has a complex life cycle which includes sporozoites, cephalines, gamonts, gametocysts and oocysts. The different stages show REFERENCES structural changes which are adapted to an endogenous Canning E. U.(1956) A new eugregarine of locusts. Gregarina garn- or exogenous environment. The gametocyst and oocyst hami n.sp., parasite in Schistocerca gregaria ForskJ. Protozool. stages are exogenous and produce multiple sporozoites. 3: 50-62 Da Cunha A. B., Jurand A. (1978) Ultrastructural study of the Maturation of gametocysts and oocysts was observed relationships between the gregarine Schneideria schneiderae Da with light microscopy. Oocysts of G. korogi have thick Cunha et al. 1975 and the cells of the host Trichosia pubescens Morgante 1969 (Sciaridae, Diptra). Arch. Protistenk. 120: 233- and homogeneous walls (Hoshide and Todd 1993) as 254 does G. blattarum. The oocyst wall of G. blattarum was Hoshide K., Todd K. S., Jr. (1993) Morphology of Gregarina korogi Hoshide, 1952 (Apicomplexa, Eugregarinorida) gametocysts and thick and protected sporozoites from external environ- oocyst. Acta Protozool. 32: 17-26 mental conditions. Oocysts retained the ability to excyst Janardanan K. P., Ramachandran P. (1979) Observations on a new after 10 days of desiccation. Janardanan and species of cephaline gregarine from the millepede, Carlogonus palmatus Demange, 1977. Zool. Anz.(Jena) 203: 392-400 Ramachandran (1979, 1982, 1983) reported that the Janardanan K. P., Ramachandran P. (1982) On a new cephaline digestive fluids released the sporozoites from the oocyst gregarine, Stenoductusxenoboli n.sp. (Protozoa: Cephalina) from the gut of the millipedes Xenobolus acuticonus attems and Auca- on the gregarines that parasitized millipedes. The diges- cobolus graveleyi sivestri. Proc. Indian Acad. Parasit. 2: 57-61 tive tract extract affected the excystation of sporozoites, Janardanan K. P., Ramachandran P. (1983) On a new septate grega- rine, Stenoductuspolydesmi sp.n. (Sporozoa: Cephalina) from the but we did not attempt to identify the active component. millipede, Polydesmus sp. with the millipedes in Kerala, India. Some substance in digestive tracts activate sporozoites. Acta Protozool. 22: 87-94 Levine N. D. (1971) Uniform terminology for the protozoan subphy- The activated sporozoites bored holes in the wall of the lum apicomplexa. J. Protozool. 18: 352-355 oocyst and emerged through the holes. We found three Siebold C. T. (1839) Beitrage zur Naturgeschichte der wirbellosen breaks in the oocyst wall of Gregarina korogi and were Thiere. N. Schrift. Naturf. Ges. Danzig 3: 56-71 Watson M. E. (1916) Studies on gregarines. III. Biol. Monogr. 2: of the opinion that the wall is split along the lines at the 1-258 time of sporozoite excystation (Hoshide and Todd 1993). Sporozoites G. blattarum formed holes and emerged through the oocyst wall. The extract solution may ac- Received on 10th August, 1993; accepted on 9th November, 1993

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http://rcin.org.pl Corliss J. O.: An interim utilitarian ("user-friendly") hie- rarchical classification and characterization of the Protists 1 Machemer H.: Gravity-dependent modulation of swim- ming rate in Ciliates 53 Schäfer J., Sebastian C. and Hader D.-P.: Effects of solar radiation on motility, orientation, pigmentation and photosynthesis in green dinoflagellate Gymnodi- nium 59 Hoshide K., Nakamura H. and Todd K. S., jr.: In vitro excystation of Gregarina blattarum oocysts 67

1994FEBRUARY

VOLUME 33 NUMBER 1

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