Acta Protozoologica (1994) 33: 1 - 51
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An Interim Utilitarian (MUser-friendlyM) Hierarchical Classification and Characterization of the Protists
John O. CORLISS
Albuquerque, N ew 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.
ÏNTRODUCTION 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 Souquerque, New Mexico 87153, USA. understanding with respect to the most "natural" scheme fiónos PaPer 1S dedicated to the memory of Zdzislaw Raabe of classification to employ for these ubiquitous and L r 1972) who, 30 years ago, perceptively foresaw the prob cosmopolitan eukaryotic - generally microscopic and us involved in constructing a macrosystem for the Protozoa ased on evolutionary principles (Raabe 1964a) and who, in the often unicellular - organisms. In recent years, with the *ne year, published a comprehensive protozoological textbook development of molecular Chronometrie techniques (e.g. . aabe 1964b) and, in the preceding year, had founded the ^national journal Acta Protozoologica. ribosomal RNA sequencing: see Christen 1992), com 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 fliy may not be identical with putative evolutionary lines of understanding of the composition and taxonomic boufi' the very recent literature; that is, they may not be daries of such groups: some of the major works amon? 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 (Harris^1 "User-friendly" Classification of the Protists 3 oni 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 Dyková ever (to save space), these individual specialist-contribu- (1992), Lynn (1981), Lynn and Corliss (1991), Margulis (jQijs - like many of the other numerous scattered (1970, 1981, 1993), Margulis et al. (1990), Margulis et ta x o n o m ic 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), Möhn (1984), Moss (1991), Müller (1992), Mylnikov FURTHER b a c k g r o u n d 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 Zölffel (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), Bárdele (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), Wainrightet 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: Bütschli (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-Kemeis (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 (1991),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), Hülsmann predominantly photosynthetic organisms, often non- (1992), Irvine and John (1984), Karpov (1990), Karpov mo tile, 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 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 w orks 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, Kützing, Lamouroux, Lemmermann, and numerous teachers and textbook writers around the Lister, Luther, Pascher, Rabenhorst, Smith, West, Wei world, have adopted this appealing way of viewing the tstem, 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). Bütschli, Calkins, Cash, Cépède, 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 Grassé, Haeckel, Hartmann, Hertwig, Kahl, Kent, posed purely of protists together in a single kingdom Kofoid, Kudo, Lankester, Laveran and Mesnil, Léger, (see the pioneering paper by Leedale 1974; Möhn 1984; Leuckart, O.F. and J. Müller, 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 sortie 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. "User-friendly" Classification of the Protists 5
ti 6 J. O. Corliss 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 Class (2) Opalinatea Wenyon, 1926 Goldfuss with the name and the general concept, as is 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 8. 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 9. 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 10. 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 Grassé, 1952 (= mostly Foraminiferea d’Orbigny, 1826) Class (1) Trepomonadea Cavalier-Smith, 1993 Class (5) Xenophyophorea Schulze, 1904 Class (2) Retortamonadea Grassé, 1952 Class (3) Oxymonadea Grassé, 1952 Phylum 11. 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 Subphylum - 1- ACANTHARIA Haeckel, 1881 Class (3) Lyromonadea Cavalier-Smith, 1993 Class Acantharea Haeckel, 1881 Class (4) Pseudociliatea Corliss & Lipscomb, 1982 Subphy\um-2- RADIOLARIA J. Müller, 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 Grassé, 1970 Phylum 3. EUGLENOZOA Cavalier-Smith, 1981 Class Myxosporea Bütschli, 1881 Class (1) Diplonematea Cavalier-Smith, 1993 Class (2) Euglenoidea Bütschli, 1884 Phylum 14. ASCETOSPORA Sprague, 1978 Class (3) Kinetoplastidea Honigberg, 1963 Class Haplosporidea Caullery & Mesnil, 1899 "User-friendly" Classification of the Protists 7
Kingdom m. CHROMISTA Cavalier-Smith, 1981 Phylum 4. CHAROPHYTA Rabenhorst, 1863 Class (1) Charophyceae Rabenhorst, 1863 5W¿kingdom (I) HETEROKONTA Luther, 1899 Class (2) Conjugatophyceae Engler, 1892 Phylum 1. BICOSOECAE Cavalier-Smith, 1989 Subkingdom (13) BILIPHYTA Cavalier-Smith, 1981 Class Bicosoecidea Grassé & Deflandre, 1952 Phylum 1. RHODOPHYTA Rabenhorst, 1863 Phylum 2. LABYRINTHOMORPHA Page in Levine Class (1) Bangiophyceae Wettstein, 1901 et ah, 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. RAPHEDOPHYTA Chadefaud, 1950 Class Chytridiomycetes Sparrow, 1959 Class Raphidomonadea Chadefaud, 1950 Kingdom VI. ANIMALIA Linnaeus, 1753 Phylum 5. PHAEOPHYTA Weitstem, 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 Subkingdom (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 Cavalier-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 (HI) 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
Subkingdom (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. PLANTAE Linnaeus, 1753 state. Included species that are capable of photosynthesis (some mixotrophic) typically have cytosolic Subkingdom (I) V IRIDIPLANTAE 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 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 0r 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 ß-giu^ 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 multicef Kingdom III. 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 s u c h a haploid and diploid generations. rank is appropriate for them) but in interrelating then1 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, feei a need "User-friendly" Classification of the Protists 9
to a s s e m b l e 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. or ; ¿so to subdivide them unmercifully at lower ranks, For a convenient summary of the classification ead) -j interposing between phyla and classes such ranks as sub- presented in this paper, the reader is referred to Table 1 •gla- and infraphyla and superclasses (not to mention inter and • mediate taxa at ordinal, familial, and generic levels as Phyla of Kingdom ARCHEZOA •s or well)* I can understand the rationale involved in the latter n of « practices, for they allow the user of the resulting In addition to the three quite disparate phyla tous) schemes to appreciate the clustering of certain taxa that described below, some workers have suggested the :icel- share key characters. Yet, for the general user, the inclusion here, also, of the parabasalan flagellates etely teach er and the student, and the person interested in (considered as the second phylum of the kingdom dany having a classification helpful in information retrieval, PROTOZOA in the present work) and/or of the i 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 losed quires new names, adding to the memory burden of the vatively feei 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. ARCHAMOEBAE Cavalier-Smith, 1983 longer works of Cavalier-Smith (e.g. 1993c). îago- Whenever possible, I have adopted phyletic names Amoeboid or amoeboflagellated (generally a poorly y or- familiar from the literature, as long as the composition motile single flagellum) protists with characteristics :issue and the rank of the taxon have not been too drastically of the kingdom (q.v.), although presumed presence Vlito- changed over time (see DISCUSSION). With respect to of 70s ribosomes not yet confirmed. Microaerobic, 3olgi the spelling of names of protist phyla, especially the with symbiotic bacteria; free-living, mostly fresh e tis- prefixes and suffixes, I have - once again - tried to water habitats. nplex maintain traditional forms of the words. In particular, I Com- have retained the phylum/di vision ending "-a" (excep Class Pelobiontea Page, 1976 ^ and tionally, -"ae" and one time "-i") so long used in both (syn. Karyoblastea Margulis, 1974 p.p.) mally 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 none 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. I "-ida"; but, in the interest of saving space, not many Mastigamoeba, Mastigella, Mastigina, Pelomyxa, j orders are included on the following pages. Phreatamoeba I As an aid to readers of various backgrounds with ase of I respect to protistological high-level systematics, names Phylum 2. METAMONADA Grassé, 1952 -level °f a goodly number of representative or common or dsys- familiar genera (plus some new within the past several Bi-, quadri-, octo- (or occasionally more) flagellated in the years) are given under the lowest-ranked taxa listed protists, mostly symbiotic species, with characters of 986a, within a specific phylum. The INDEX will serve as a the kingdom (q.v.), including 70s ribosomes and (e.g. phyla convenient guide to the page-locations of these generic Giardia) 16s rRNA. Some free-living, majority intes e, not names. tinal symbionts of various hosts. Parabasalans (see ogical 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. a, the would be of little value. On the other hand, to make up >t only f°r our ignorance of "true" evolutionary interrelation Class (1) Trepomonadea Cavalier-Smith, 1993 juch a ' s , a measure of "educated guess-work" (= healthy One or two karyomastigonts, each with 1-4 flagella; ¡ them speculation?) is required in quite a number of instances. contractile axostyle absent; cytostomal-cytopharyn- Some : Quite often, brief comments are offered in place in geal apparatus present; few cell-surface cortical i n eed c°ntroversial situations; otherwise, the reader is referred microtubules. Free-living or symbiotic. 10 J. O. Corliss
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 , Endoreticulatu$ Caviomonas , Enteromonas, Trimitus Enterocytozoon , Glugea, Gurleya, Loma, MicrofilUrn Mrazekia, Nosema, Perezia, Pleistophora , Spraguea Class (2) Retortamonadea Grassé, 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 Grassé, 1952 Phylum 1. PERCOLOZOA Cavalier-Smith, 1991 Chilomastix , Retortamonas Unicellular, non-pigmented protozoa allegedly primi Class (3) Oxymonadea Grassé, 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 Grassé, 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, Pseudovahlkampfi& (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 microtubule^ 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 , P s alteromonas "User-friendly" Classification of the Protists 11
Class (4) Pseudociliatea Corliss & Lipscomb, 1982 with persistent nucleolus; many fresh-water free- IVlultiflagellated, 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 Bütschli, 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 ß-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 Bütschli, 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 dgotoides , Hoplonympha, Kofoidia , Macrospironym- Order 4. Heteronematida Leedale, 1967 pha, Spiro trichonympha, Teranympha, Trichonympha Entosiphon , Heteronema, Peranema, Petalomonas , Ploeotia , Sphenomonas Phylum 3. EUGLENOZOA Cavalier-Smith, 1981 Class (3) Kinetoplastidea Honigberg, 1963 nd no Forms with 1-4 flagella, with paraxial rods and non- Small, colorless flagellates with 1-2 flagella (arising bules; tubular mastigonemes; with peroxisomes and com from pocket and possessing paraxial rod) and y two 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 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 sy^. 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, ifer- is rather atypical of the phylum v.v. 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 Re dinomonas, 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 m cttpp) Class (2) Opalinatea Wenyon, 1926 (syns. Protociliata Metcalf, 1918, Paraflagellata Free-living, unicellular or syncytial p l a s m o d i ^ Corliss, 1955, Slopalinida Patterson, 1986 p.p.) forms, non-flagellated in their uni- or multinucleate "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. Cavaher-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 Thalassomyxa. 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, Iella, (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
Gass (1) Protostelea Olive & Stoianovitch, 1966 Single amoeboid cells, with filóse 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 liforme mitochondrial cristae, and peroxisomes; one flagellum typically with paraxial rod; ca. 50% of wna, Gass (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 : (but Echinostelium, Fuligo, Licea, Lycogala, Physarum, distinctive chromosomes consisting primarily of non icilia- Stemonitis, Trichia, Tubulina protein complexed DNA. Assemblage at one time ristae called the "Mesokaryota" because of its alleged pos ^mes; Class (3) Dictyostelea Lister, 1909 session of a combination of pro- and eukaryotic nplex Cellular slime molds from soil with triphasic life characters. First of three phyla known collectively as >rkers cycle: unicellular amoeboid microphage, pseudoplas the "Alveolata", a super-category designated a i, and modium (slug) formed by aligned aggregating parvkingdom by Cavalier-Smith (1993c). Possibly ) than 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).
% lum 6. CHOANOZOA Cavalier-Smith, 1989 Class (1) Protalveolatea Cavalier-Smith, 1991 Atypical dinozoa; closed mitosis, but mitotic spindle and Free-living, uniflagellated, colorless, unicellular or intranuclear; chromatin of normal eukaryotic form; tt. pp) 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 lodiai surrounded by collar of microvilli (aetin filaments (osmotrophic); typically unicellular and uninucleate, cleate internally) used in microphagous feeding; marine but symbiotic forms may be branched and multi- 14 J. O. Corliss
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 ÍNFUSORU ment. auctt. (a very old and vague term) or by the more ant Colponema, Ellobiopsis, Oxyrrhis, Thalassomyces name of HETEROKARYOTA Hickson, 1903, the cilioprotists comprise one of the largest protist phyia Class (2) Dinoflagellatea Bütschli, 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 planktonic. 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, Bütschli, 1889, in effect; and Postciliodes Rhizodinium, Roscoffia, 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 membranelies, 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). "User-friendly" Classification of the Protists 15
Subclass 1. H eterotrichia 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, FoZ- 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 Bütschli, 1889 Dendrocometes , Dendrosoma , Dysteria, Endos The classically known oligotrichs s.Z. (i.e. oligotrichs phaera, Ephelota, Hartmannula, Heliochona , Helio- s.s. + tintinnids s.Z. = today’s choreotrichs) and the phrya, Hypochona , Isochona , Lobochona , Lorico old hypotrichs s.Z. (i.e the pre-1980 stichotrichs and phrya, Lwoffia, Lynchella, Ophryodendron , Paraci sporadotrichs). neta,, Phalacrocleptes, Phascolodon , Podophrya , Amphisiella, Aspidisca, Australothrix, Bakuella, CZr- 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, Pseudo glaucoma, Sorogena , Thylaki- dium, Trihymena, Woodruffia Subclass 1. Hymenostomatia Delage & Hérouard, 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 T
16 J. O. Corliss
a unique watchglass organelle and a complex life Opercularia, Ophrydium, Opisthonema, Orboper cycle as obligate histophagous symbionts. cularia, Pallitrichodina, Platycola, Polycycia 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- (phoronis) on marine crustaceans. Three orders. nematids, and the totally symbiotic thigmotrichs. Ascophrys, Askoella, Chromidina, Collinia, Con- Ancistrum, Ancistrumina, Boveria, Cinetochilum, idiophrys, Cyrtocaryum, Foettingeria, Gym Cohnilembus, Conchophthirus, Cyclidium, Dexio- nodinioides, Hyalophysa, Opalinopsis Ophiurae- tricha, Dragescoa, Entodiscus, Fenchelia, Hemi spira, Phtorophrya, Vampyrophrya speira, Histiobalantium, Hysterocineta, Loxocepha lus, Miamiensis, Myxophthirus, Parauronema, Subclass 6. Peniculinia Fauré-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, Lem 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 a's 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 transversi "User-friendly" Classification of the Protists 17
jnicrotubular 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 , basal body of nine singlet instead of usual eukaryotic todinium, Gorillophilus , Isotricha , Lacrymaria, triplet micro tubules); zygotes undergo meiosis and Lagynophrya, Lepidotrachelophyllum, Litonotus , sporogony within gametocystic membrane; trophonis Loxophyllum , Mesodinium, Ophioscolex , 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 metophilus, Diplocystis, Doliospora , Gonospora , gum Gregarina, Lankesteria, Lecudina, Monocystis , Ophryocystis , Porospora , Rhynchocystis , Schizocys tis, Selenidioides , Selenidium, Siedleckia , Stepha- Phylum 9. APICOMPLEXA Levine, 1970 nospora, S tylocephalus, 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 cistemae (= 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 Léger, 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, Lrenkelia, of the "Alveolata" assemblage (others are the Goussia, Grellia, Haemogregarina , Hepatozoon , dinoflagellates and the ciliates: see above). Isospora, Karyolysus, Klossia, Klossiella, 18 J. O. Corliss
Lankesterelia, Legerella, Sarcocystis, Schellackia, belong here, as well as the baffling symbiotic Blas, Selysina, Toxoplasma, Tyzzeria, Wenyonella tocystis (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, Llabellula, Hartmannella, Hydra- or absent entirely; motile zygote (= ookinete) moeba, Leptomyxa, Lesquereusia, Mayorella penetrates vector-host’s gut wall, producing Nebela, Netzelia, Paramoeba, Platyamoeba, 0s- R numerous "naked" sporozoites which migrate to cuius, 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 pattem. 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, Iodamoeba) 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 apon 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 a m o e b o id , 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 of mycetozoa proving difficult to assign) might also more larger somatic nuclei and usually numerous >: til "User-friendly" Classification of the Protists 19
'¡as- small generative nuclei, a heterokaryotic condition ally placed here, have been removed: the dimorphids GD, ; 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 thia, 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 CllT- dra- composed of the foraminifers (Foraminiferea d’ Or certain members of the next phylum, RADIOZOA. ella, bigny, 1826: see genera below), with additionally Familiar name and conventional understanding of Ros - included separate, but dubiously distinct, orders "the Heliozoa" maintained, although considerably 'eba, Athalamida Haeckel, 1862 (e.g. Arachnula and refined over classical usage; still, some workers tfera Biomyxa) and Monothalamida Haeckel, 1862 (e.g. might prefer to elevate all or some of my classes to Amphitrema, Lieberkuehnia, Micro gromia). Several independent phyletic status. Classically, the heliozoa orders, numerous families, and many hundreds of s.I. and the radiozoa were combined under a super- > îÿt genera (a few with living species listed below) of taxon called the "Actinopoda", based on their com and forams. Does Komokia (still) belong here? mon possession of axopodial pseudopodia. Allogromia, Ammodiscus, Ammonia, Boderia, ; no Class (1) Actinophryidea Hartmann, 1913 Bolivina, Carterina, Discorbis, Elphidium, Glabra Jring Actinophrys, Actinosphaerium, Camptonema Ithat tella, Globigerinella, Guttulina, Hastigerina, »ebae Heterotheca, Iridia, Metarotaliella, Microglabratel Class (2) Centrohelidea Kühn, 1926 It is la, Myxotheca, Nonion, Ovammina , Patellinella, Acanthocystis, Actinocoryne, Cienkowskya, Gymnos En Planorbulina, Polystomella, Quinqueloculina, phaera, Hedraiophrys, Heterophrys, Raphidiophrys jeba) Rhizammina, Rosalina, Rotaliella, Saccammina, Class (3) Desmothoracidea Hertwig & Lesser, 1874 3ove. Schizammina, Schwagerina, Selenita, Sorites, Spiril Clathrulina, Hedriocystis, Orbulinella En- lina, Spiroloculina, Textularia, Triloculina, Uvigerina agel- Class (4) Taxopodea Fol, 1883 ylum 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, iched within agglutinated test; presumably with filóse or often of large body size, characteristically having aked, 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 lami rank of taxon and its placement among other protists either siliceous or of strontium sulfate, in latter case nero- remains uncertain. with radially arranged spicules; unicellular, oc ardin Galatheammina, Psammetta, Stannophyllum casionally colonial; single nucleus in early vegetative relia stage, organisms often becoming multinucleate sub sequently; some species produce biflagellated Phylum 11. HELIOZOA Haeckel, 1866 swarmer cells, not to be confused with symbiotic rming dinoflagellates often present. Based on numerous Lers in Unicellular phagotrophs with axopodia containing differences within the assemblage, phylum probably ithno rigid microtubular axonemes; micro tubules typically best divided into two subphyla, with two classes in i tests arrayed hexagonally, often nucleating on envelope of the second much larger and more familiar group. many nucleus; kinetocysts common; mitochondrial cristae aper- typically tubular; trophic stage usually without flagel Subphylum 1. Acantharia Haeckel, 1881 nation la; short filopodia in some species; several groups itions; with stalks, one with perforated shell or test; mostly Class Acantharea Haeckel, 1881 sboid; fresh-water, some marine. Controversial whether four Acanthochiasma, Acantholithium, Acanthometra, nation classes named below are closely enough interrelated Amphilonche, Astrolonche, Astrolophus, Haliom- one or to warrant being clustered into one phylum; two other matidium, Lithoptera, Pleuraspis, Pseudolithium, íerous taxa (of once-called "helioflagellates"), convention Xiphacantha T
20 J. O. Corliss
Subphylum 2. Radiolaria J. Müller, 1858 session of "spores" with polar filaments inside. ge cause of their pluricellular 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, 77za- lassophysa Class Myxosporea Bütschli, 1881 Ceratomyxa, Chloromyxum , Fabespora, G/ofo- Class (2) Phaeodarea Haeckel, 1879 spora, Henneguya, Hoferellus, Kudoa, Lomosporus Atlanticella, Aulacantha, Aulosphaera, Aulotractus, Myxidium, Myxobolus , Myxoproteus, Ortholinea Castanella, Challengeriae Challengeron , Coelo Parvicapsula, Sinuolinea, Sphaeromyxa, Sphaero dendrum, Conchopsis, Halocella , Medusetta, spora, Trilospora, Unicapsula, Unicauda, Ward/a Phaeodina Zschokkella
Phylum 13. MYXOZOA Grassé, 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 Bütschli, 1881 and Class Haplosporidea Caullery & Mesnil, 1899 Actinomyxidia Stoic, 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 arc 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. "User-friendly" Classification of the Protists 21
Subkingdom (I) HETEROKONTA Luther, 1899 Phylum 3. DICTYOCHAE Haeckel, 1894 ■ Be- anty Essentially with characters of the kingdom sensu Mixture of pigmented and non-pigmented with stricto: organisms with chloroplasts (unless secon heterokonts, free-swimming or stalked, marine and laced darily lost) located within rough endoplasmic fresh-water habitats; often with anteriorly directed ass. 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 lobo- thrust reversal. Bulk of the chromist species belong basal body; some species (silicoflagellates, mostly orus, to phyla of this well-established and nearly univer marine fossil forms) with complex basket-shaped inea, sally accepted major taxonomic assemblage of "the external siliceous skeleton. Two classes. The second, ciero- heterokonts": the name - in one form or another (e.g. whose members have long been studied by irdia, 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 Möhn (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 rates, "helioflagellates" (see Davidson 1982) of the litera cells Small, free-living, fresh-water or (few) marine, ture, may be polyphyletic; Cavalier-Smith (1993c) r fíla planktonic biflagellated (one flagellum with mas- has at least partially relieved that condition by remov mele; : tigonemes), heterotrophic non-pigmented forms typi nique ing Oikomonas to a separate class of its own, although cally living in loricae (attached by the second, smooth luded I have not done so here. Some workers vernacularly blage flagellum), and feeding on bacteria; some stalked, refer to (some or all of) the pedinelleans (or pedinel- dered some form colonies. lophyceans) as actinomonads. xidea Class (1) Silicoflagellatea Borgert, 1891 • Class Bicosoecidea Grassé & Deflandre, 1952 ís & Dictyocha (only genus with living species) laplo- j Bicosoeca , Cafeteria, Pseudobodo ecific Class (2) Pedinellea Kristiansen, 1990 993)? Actinomonas , Ciliophrys , Oikomonas , Parapedinel Phylum 2. LABYRINTHOMORPHA la, Pedinella, Pseudopedinella, Pteridomonas j Page in Levine et al., 1980 jmar- 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. recia- cristae; known zoospores biflagellated, one bearing Phylum is also known as "the chloromonads"; but this ers of mastigonemes, other naked; in marine, generally is inappropriate, because Chloromonas is a genus of com- coastal, waters, often associated with, or ectosym- green algal protists in the kingdom Plantae. pings, bionts of, aquatic angiosperms and certain algal id are protists. Class Raphidomonadea Chadefaud, 1950 least, Chattonella , Gonyostomum , Heterosigma , Mero o the Class (1) Labyrinthulea Cienkowski, 1867 tricha, Olisthodiscus , Vacuolaria data I Labyrinthula mship Phylum 5. PHAEOPHYTA Wettstein, 1901 terson Class (2) Thraustochytriacea Sparrow, 1943 cus- Aplanochytrium, Labyrinthuloides , Thraustochy Photosynthetic heterokonts predominantly with trium chlorophylls a plus c and leucosin and fat (or para- 1 22 J. O. Corliss
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 D 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, ]yja^ tive statospore; other groups almost entirely marine lodendron, Ophiocytium, Pleurochloris, Retículos (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 planktonic 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, Giffordia, Achnanthes, Amphipleura, Amphora, Auricula, Hormosira, 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 Triceratium 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 uniflagellated z o o s p o r e Chlorobotrys, Eustigmatos, Monodopsis, Nan stage; uninucleate or coenocytic walled protoplast in nochloropsis, Pseudocharaciopsis, Vischeria vegetative stage. Long conventionally considered a> 1
"User-friendly" Classification of the Protists 23
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 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, SPERMATOPHYTA) 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 quadriflagd' 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 "User-friendly" Classification of the Protists 25
(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 Francé, 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, Vb/- Chaetosphaeridium, Chara, Chlorokybus, Coleo var, 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 swart, Chaetosiphon, CladophoraClaclophora, Codium, Cymopohlia , Dasycladus, Eugomontia, Halimeda, Subkingdom (II) BILIPHYTACavalier-Smith, 1981 Phaeophila, Rhizoclonium, Siphonocladus, Tricho sarcina, Ulothrix , [7/va, 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 / non- main axis erect plus regular whorls of lateral total absence of centrioles and flagella and by flagel- branches, and with male and female sex organs presence of single thylakoids in their chlorophyll a nclude reminiscent of those of land plants: these charophytes containing plastids with phycobilins as accessory cinoid, have motile (flagellated) swarmers, never with photosynthetic pigments; mitochondria with flattened class eyespot, typically covered with scales; many mem cristae; starch stored in cytosol; often complex life 1
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 phylurn 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, Batrachospermum, (rarely multiple) flagellum (without mastigonemes or Boldia , Callocolax , Capreolia, Chondrus , Com scales), frequent unicellularity, and possession of psopogon, Cyanidium, Dilsea, 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 sí Lithophyllum , Mesophyllum, Minium, Naccaria, P^/- differ significantly from members of the phylum maria, Phragmonema , Phyllophora , Porolithon , P 6 >r- 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 perfecti, 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, sporn 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* "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 crisiae 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 flames 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 in my The Kingdom PROTOZOA proper place for the green algae, which harbor the beyond ancestors of the "higher" plants but some of which were sporn The Protozoa, united into a formal group of generally traditionally labeled, simultaneously, as protozoa (e.g. ve rep' ^croscopic, unicellular, phagotrophic forms, have been Chlamydomonas , Volvox , and their close relatives: the îcently» ^ound for 175 years. The rank accorded them has been "phytomonads" or, better, the volvocids). 28 J. O. Corliss
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 Vprs 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 Cavaher-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 Younès 1986). This may be considered both "User-friendly" Classification of the Protists 29 livea "good" and "bad", but the unchecked promulgation of number of quite unusual organisms (e.g. a single family ■s) in new ranks and names in recent years has led us nearly or even a single genus or species), then I especially have (Pas-. ¡ t0 the brink of chaos in protistology, nomenclaturally tended to use the original name and authority for the this j peaking (see extended discussions in Corliss 1984, group even if the rank (usually upward) may have idem ¡99O, 1991b, 1993; Patterson and Larsen 1992). Some changed drastically. The description, while refined in 'relly , ¿mo ago, I stressed the need for "common sense and light of new knowledge, is basically concerned with the aring courtesy" in the area (Corliss 1972), and Silva (1980) same organism(s). However, there are a few defensible ludes has urged that an overriding consideration should be exceptions to this. as a "effectiveness of communication". A reasonable degree 3. In the preceding and still other situations, I have ’6 ), a 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 Jelled emphasis on constant change. mation. In the case of a number of former botanical 389a) In the classification of the 34 phyla formally offered classes, I have - along with other workers - felt free to lidate ' in this paper, I have been confronted by the same dilem elevate the group to phylum (= division) status, altering b). In mas described in my earlier overview work (Corliss the suffix appropriately. Also, I have not been con char- 1984), and have thus been obliged to make a number of strained by the lack of a Latin diagnosis in the first (or irs or auite subjective decisions in choice of both names and subsequent) description to withhold credit from the n lost authorities for the higher taxa included. Space does not original creator/proposer of a group or of its name. This ble to permit a detailed discussion here. Suffice it to say, in latter decision has affected the date of authorship and t fea- keeping with my objectives to present a "user-friendly" occasionally the authorities themselves in the case of rising scheme of classification including all groups of protists, some botanically derived names, as will be apparent in ’s and I have adopted the guidelines given below, keeping in the text and in Table 1. 'alier- mind the practical observation made by Raabe (1964a) 4. According to conventional practices, a number of m his some 30 years ago: "I am not an adherer of introducing group-names might well have been marked "emend", more new names for old taxa, although they might stress better "sensu", "ex", "nom. nov.", or "stat. nov." (with or 'orker i their properties. It introduces confusion..." And Silva without additional author/date data), but, for the sake of ids (= (1980) has sensibly suggested that a classification consistency and simplicity, I have not done this. I offer . from should be one that is "familiar and acceptable to the apologies to nomenclatural purists and any offended rough largest number of users". taxonomic specialists. Today, it is generally assumed while 1. When possible/defensible, I have employed the by taxonomists that for descriptions of organisms or everal oldest and/or most familiar name for a more or less groups of organisms one must go to the more recent es" in conventional group of protists. Although the concept, rather than the older literature; in some ways, however, i boundaries, composition, and even the rank-level may their nomenclature may be considered to be a separate rzoan, I have changed somewhat over time, the name used may matter - primarily one more of historical interest. e bulk be credited to the original author, using date of his 5 .1 am not automatically opposed to all "new" names! rophic creation of the name. As might be expected, sometimes For instance, I have endorsed/accepted some 20 of ellular exceptions to this principle are advisable. Incidentally, Cavalier - Smith’s numerous high-level taxonomic / no ement to save space, I have not regularly listed all synonyms menclatural creations of the past dozen years. For a few major : °f the names selected for the various high-level taxa examples of these neologisms (some of them altered noiety endorsed on preceding pages. In a number of cases, slightly in this paper in rank or in spelling of the name): ; algal however, I have included a few for the benefit of readers his kingdom Chromista and subkingdoms Viridiplantae arisen 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 aniple, will have had a nomenclatural exposure likely number of new names for intermediate ranks. As stated encla- differing from that of students trained in zoological in my INTRODUCTION, most of these have been nairies ^xonomy. omitted primarily to reduce the size of my own clas- 1990; 2- When both an original group and its later recogni- sificatory framework, making it more easily usable for d both ; tlQn as a unique higher-level taxon involve a very small the many readers who are not taxonomic specialists and 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 Zölffel 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 "Anhängen" 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 Dictyosteliutn', 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); Zölffel 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 synonym^ "User-friendly" Classification of the Protists 31 hom°nyms’ etc* ®ut’ m 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. John Wiley & Sons, New York c a l " taxa of protists. Resolution of such duplication, Andersen R.A. (1989) The Synurophyceae and their relationship to sornewhat like that of the particularly troublesome other golden algae. Beih. Nova Hedwigia 9 5 : 1-26 problems arising from having two groups of protists (e.g. Andersen R.A. (1991) Algae. 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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.
A 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 A chlya ...... 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 A delea...... 17 Apostomatia ...... 16 Adelphamoeba...... 10 Apusomonas...... 12 Aggregata ...... 17 Arachnodinium ...... 17 A laria...... 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 Amastigomonas ...... 12 Arthrodesmus ...... 25 "User-friendly" Classification of the Protists 37
ascetospora ...... 20, Table 1 Blastocrithidia ...... 12 Ascobius ...... 15 Blastocysta...... 26 a Sc o m y c o t a ...... 26 -Blastocystis...... 18, :
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
Atlanticella...... 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,
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 C
, Bicosoeca ...... 21
BlCOSOECAE...... 21, Table 1 Caenomorpha ...... 15
Bicosoecidea ...... 21, Table 1 Cafeteria...... 21
Bicosta...... 13 Calciosolenia ...... 23
Biddulphia...... 22 Calliacantha...... 13
b il ip h y t a ...... 25, 26, 29, Table 1 Callimastix...... 26
Biom yxa ...... 19 Callocolax ...... 26
Biastocladiella...... 26 Calonympha...... 11 38 J. O. Corliss
Camptonema...... 19 Chlorobotrys ...... 22 Canistrolithus...... 23 Chlorococcum ...... 25 Capreolia...... 26 Chlorogonium ...... 25 Carchesium...... 16 Chlorokybus ...... 25 Carteria...... 25 "Chloromonads" ...... 21 Carterina...... 19 Chloromonas ...... 21, 25 Caryospora...... 17 Chloromyxum ...... 20 Cashia...... 18 Chlorophyceae ...... 25, Table 1 Castanella...... 20 CHLOROPHYTA...... 24, Table 1 Catenaria...... 26 "Choanociliata" ...... 13 Caulleryella...... 17 Choanoflagellatea ...... 13, Table 1 Caviomonas ...... 10 Choanoflagellates...... 13 Cavostelium...... 13 Choanoflagellida ...... 13 Cellular slime molds ...... 13 Choanomonads ...... 13 Cenosphaera...... 20 CHOANOZOA...... 13, Table 1 Centrohelidea ...... 19, Table 1 Choanozoa ...... 26 Centropyxiella...... 18 Chondrus ...... 26 Centropyxis...... 18 Chonotrichs ...... 15 Cepedea...... 12 Chordaria ...... 22 Cepedietta...... 16 Choreotrichs...... 15 Cephalothamnium...... 12 Chromidina ...... 16 Ceratiomyxa...... 13 CHROMISTA...... 5, 8,13,19,20,23, Ceratium...... 14 26 - 29, Table 1 Ceratomyxa...... 20 Chromobionta ...... 28 Cercomonas ...... 12 Chromobiota...... 28 Chaenea...... 17 Chromophy ta ...... 28 Chaetochloris ...... 25 Chromulina...... 22 Chaetosiphon ...... 25 Chroomonas ...... 23 Chaetosphaeridium...... 25 Chrysamoeba ...... 22 Challengeria ...... 20 Chrysidalis ...... 23 Challengeron ...... 20 Chrysocapsa...... 22 Chaos ...... 18 Chrysochromulina ...... 23 Chara...... 25 Chrysococcus ...... 22 Chardezia...... 18 Chrysodendron ...... 22 Charophyceae ...... 25, Table 1 Chrysomonadida ...... 22 CHAROPHYTA ...... 25, Table 1 Chrysomonads ...... 22 Charophytes...... 25 Chrysophyceae ...... 22, Table 1 Chattonella ...... 21 Chrysophyceans ...... 27, 30 Chilodochona ...... 15 Chytridiomycetes ...... 26, Table 1 Chilodonella ...... 15 Chytridiomycetes ...... 31 Chilomastix ...... 10 CHYTRIDIOMYCOTA 26, Table 1 Chilomonas ...... 23 Chytridiopsis ...... 10 Chlamydodon ...... 15 Chytridium ...... 26 Chlamydomonas ...... 25, 27 Chytrids ...... 23, 26 Chlamydophrys ...... 18 Chytriodinium ...... 14 Chlorarachnion ...... 24 Chytriomyces ...... 26 Chlorarachniophyceae ...... 24, Table 1 Cienkowskya...... 19 CHLORARACHNIOPHYTA . 24, Table 1 Ciliates...... 17, 30 Chlorella ...... 25 CILIOPHORA...... 14, Table 1 Chlorobionta ...... 28 Ciliophryids ...... 19 "User-friendly" Classification of the Protists 39
Ciliophrys ...... 21, 30 Contophrya ...... 16 Cilioprotists...... 14 Copromyxa...... 18 Cinetochilum ...... 16 Corallomyxa ...... 13 Cirrogaster ...... 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 Coelodiscus ...... 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 Anoidea ...... 17 Cystodinium...... 14 Conradinema...... 11 Cystoseira...... 22 40 J. O. Corliss
D Disematostoma ...... 16 Distigma ...... 11 Dactylosoma ...... 18 Ditrichomonas ...... 11 Dasycladus...... 25 Dobellia ...... 17 Deltotrichonympha ...... 11 Dolichomastix ...... 24 Dendrocometes ...... 15 Doliospora ...... 17 Dendrosoma ...... 15 Dorisiella...... 17 Dermatochrysis ...... 22 Dragescoa ...... 16 Desmidium...... 25 Duboscquella...... 14 Desmids ...... 25 Dunaliella...... 25 Desmothoracidea ...... 19, Table 1 Durchoniella...... 16 Desportesia...... 10 Dysteria...... 15 Devescovina ...... 11 Dexiotricha ...... 16 Diadesmis...... 22 E Diaphanoeca...... 13 Diatoma...... 22 Ebria...... 12 DIATOMAE...... 22, Table 1 Echinostelium ...... 13 Diatoms...... 22 Echinozoon ...... 18 Dictyocha ...... 21 Ectocarpus...... 22 DICTYOCHAE...... 19, 21, Table 1 Eimeria...... 17 Dictyostelea...... 13, Table 1 Eimeriida ...... 17 Dictyostelium...... 13, 30 Ellobiophrya ...... 16 Dictyota...... 22 Ellobiopsis ...... 14 Didesmis ...... 17 Elphidium...... 19 D idinium...... 17 Emiliania...... 23 Didymium...... 13 Encephalitozoon ...... 10 Dientamoeba...... 11, 18, 30 Enchelys ...... 17 Difflugia...... 18 Endamoeba...... 18 Dileptus...... 17 Endocladia ...... 26 D ilsea...... 26 Endo limax ...... 18 Dimorpha...... 12, 30 Endoreticulatus...... 10 Dimorphids ...... 19 Endosphaera...... 15 Dinobryon ...... 22 Endotrypanum...... 12 Dinoflagellatea ...... 14, Table 1 Entamoeba...... 18, 30 Dinoflagellates...... 5, 17, 19, 27, 30 Entamoebidae ...... 9, 18 Dinophyceae ...... 14 Entamoebidea ...... 18, 29, Table Dinophysis ...... 14 Enterocytozoon ...... 10 DINOZOA ...... 5, 13, 29, Table 1 Enteromonadida ...... 10 Diophryopsis ...... 15 Enteromonas ...... 10 Diophrys ...... 15 Entodiniomorphids ...... 17 Diphyllea...... 12 Entodinium ...... 17 Diplocystis...... 17 Entodiscus...... 16 Diplomonadida ...... 10 Entosiphon ...... 11 Diplonema...... 11 Epalxella...... 15 Diplonematea ...... 11, 29, Table 1 Ephelota...... 15 Diplospora...... 17 Epipyxis...... 22 Discocelis ...... 12 Epistylis...... 16 Discocephalus...... 15 Erythropsidinium...... 14 Discorbis ...... 19 Erythrotrichia ...... 26 ▼
"User-friendly" Classification of the Protists 41
16 G 25 Euglena. 11 -Galatheammina...... 19 11 Gamophyceae ...... 25 11 Gastrostyla...... 15 11 Geleia...... 15 11, Table 1 Giardia...... 9, 10, 30 Euglenoids .. 5, 11, 24, 27, 30 Giffordia ...... 22 e u g l e n o ; 5, 11, 12, 29, Table 1 Gigartina...... 26 Euglypha...... 18 Glabratella...... 19 Eugomontia. .25 Glaucocystis...... 26 5, 7, Table 1 Glaucoma...... 16 .12 Glaucophyceae ...... 26, Table 1 "Eumycota" ...... 23 GLAUCOPHYTA...... 17, 26, Table 1 Euplotes...... 15 Glaucophytes ...... 24, 26 Eustigmatophyce: .22, Table 1 Glaucosphaera...... 26 Eustigmatophytes. .22 Glenodinium ...... 14 .22 Gleodinium ...... 14 .11 Globigerinella ...... 19 Globospora ...... 20 Gloeobotrys ...... 22 Gloeochaete ...... 26 Gloeocystis ...... 25 .20 Gloeopodium ...... 22 Fabrea...... 15 Glugea...... 10 Favella...... 15 Golden-brown algae ...... 22 Fenchelia , ..16 Goniomonadea ...... 23, Table 1 .. 18, Table 1 Goniomonads ...... 23 ..18 Goniomonas ...... 23 ..26, Table 1 Goniotrichum ...... 26 Foettingeria ..16 Gonium...... 25 Folliculina... ..15 Gonospora ...... 17 ..10 Gonyaulax...... 14 ..19, Table 1 Gonyostomum ...... 21 Foraminifereans. ..20 Gorillophilus ...... 17 ..19 Goussia...... 17 Foram s...... 19 Gracilaria...... 26 Fragilaria. ..22 Grammatophora...... 22 ..22, Table 1 Grandoria...... 15 ..17 Granuloreticulosea ...... 13, 18, Table 1 Fritschiella. ...25 Grass-green scaly algae...... 24 Frontonia ... ..16 Green algae...... 24 - 28 Frustulia...... 22 Gregarina...... 17 ...22 Gregarinidea...... 17, 31, Table 1 Fucus.... 22 Grellia...... 17 Fuligo...... 13 Gromia ...... 18 f u n g i . ... 5. 8, 18, ?0, 23, 26 Gross glockneria ...... 15 Table 1 Gruberella...... 10 ...26 Gurleya...... 10 p Urgasonia. ...15 Guttulina...... 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 H essea...... 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, 28 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 Hastigerina...... 19 Histomonas ...... 11 Hausmanniella...... 15 Hochbergia ...... 13 Hedraiophrys ...... 19 Hoferellus...... 20 Hedriocystis ...... 19 Holomastigotoides ...... 11 H egneria ...... 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 Hymenostomatia ...... 15 Hemimastigida...... 12 Hypermastigotea ...... 11, Table 1 Hemimastigophorea...... 11, 12, Table 1 Hyphochytriomycetes ...... 23, Table 1 Hemimastix...... 12 Hyphochytriomycetes ...... 30 "User-friendly" Classification of the Protists 43
¡{yphochytrium ...... 23 Kreyella...... 15 Uypochona ...... 15 Kudoa...... 20 jfypotrichs...... 15 Hysterocineta ...... 16
I Laboea...... 15 Ichthyobodo ...... 12 LABYRINTHOMORPHA 21, Table 1 Ichthyophthirius. 16 Labyrinthula...... 21 in f u s o r ia ..... 14 Labyrinthulea ...... 21, Table 1 Intoshellina ...... 16 Labyrinthuloides ...... 21 lodamoeba ...... 18 Lacrymaria...... 17 Iridaea...... 26 Lagenidium...... 23 Iridia...... 19 Lagenophrys ...... 16 Isochona ...... 15 Lagotia ...... 15 Isochrysis ...... 23 Lagynophrya...... 17 Isonema...... 11 Lambornella...... 16 Iso spora...... 17 Laminaria...... 22 17 Lamtostyla...... 15 Lankesterella...... 18 Lankesteria...... 17 Lateromyxa...... 18 Jakoba...... 12 Lecudina...... 17 Jaocorlissia. 16 Leegaardiella...... 15 11 Legere Ila...... 18 Leishmania...... 12 K Lembadion ...... 16 Lennoxia ...... 22 Kahliella...... 15 Lepidotrachelophyllum...... 17 Karlingia...... 26 Leptomitus...... 23 Karotomorpha. 12 Leptomonas...... 12 12 Leptomyxa...... 18 9 Leptothorax ...... 15 Karyolysus 17 Lesquereusia...... 18 14, Table 1 Leucocryptos...... 12 14 Leucocytozoon ...... 18 15 Leucodictyon ...... 12 Kathablepharis. 12 Licea...... 13 Kentrophoros ... 14 Licmophora ...... 22 Kerona . 15 Licnophora ...... 15 Khaw kinea...... 11 Lieberkuehnia...... 19 Kiitricha ...... 15 Lithodesmium ...... 22 12, Table 1 Lithophyllum ...... 26 11, 25, Table 1 Lithoptera...... 19 Klebsormidium. 25 Litonotus ...... 17 Klossia . 17 Litosiphon ...... 22 17 Litostomatea...... 16, Table 1 11 Lobochona ...... 15 14 Lobosea...... 13, 18, 26, Table 1 Komokia 19 Lohmanniella ...... 15 1
44 J. O. Corliss
Lom a ...... 10 Metacystis...... 16 Lomiella ...... 16 METAMONADA 9, Table 1 Lomosporus ...... 20 Metarotaliella...... 19 Lophomonadida ...... 11 Metchnikovella ...... 10 Lophomonas ...... 11 Metchnikovellida ...... 10 Loricophrya ...... 15 M etopus...... 15 Loxocephalus...... 16 Miamiensis...... 16 Loxodes ...... 14 Micrasterias...... 25 Loxophyllum ...... 17 Microfilum...... 10 Luffisphaera...... 18 Microglabratella...... 19 Lw offia ...... 15 M icroglena ...... 22 Ly cogala ...... 13 Micro gromia ...... 19 Lynchella...... 15 Microjoenia ...... 11 Lyrella...... 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 M allomonas ...... 22 Minium...... 26 Mallomonopsis ...... 22 Minutocellus...... 22 M amiella...... 24 Monoblepharella ...... 26 Mantoniella...... 24 Monocercomonas ...... 11 M arituja...... 16 Monocercomonoides ...... 10 M arteilia...... 20 Monochilum ...... 16 Marteiliidea...... 20 Monochiysis ...... 22 Maryna...... 15 Monocystis ...... 17 Massisteria...... 12 Monodopsis ...... 22 Mastigamoeba...... 9 Monosiga ...... 13 Mastigamoebida...... 9 Monothal amida ...... 19 M astigella...... 9 Mrazekia...... 10 M astigina...... 9 MYCETOZOA...... 12, Table 1 Maupasella...... 16 M ycetozoa...... 18, 28 Mayorella...... 18 Mycterothrix ...... 15 Medusetta...... 20 M ylestoma ...... 15 Megamoebomyxa ...... 13 Myrionema...... 22 Melanophyceae ...... 22 Myxidium...... 20 M elosira ...... 22 M yxobolus ...... 20 M enoidium ...... 11 Myxogastrea ...... 13, Table 1 M erotricha ...... 21 MYXOMYCETES...... 12 Mesodinium...... 17 MYXOMYCOTA 12 Mesojoenia ...... 11 Myxophthirus ...... 16 "Mesokaryota"...... 13 Myxoproteus...... 20 Mesophyllum...... 26 Myxosporea ...... 20, Table 1 M esostigma ...... 24 Myxosporidia ...... 20 MESOZOA...... 27 Myxosporidians ...... 20, 30 T
"User-friendly" Classification of the Protists 45
Myxotheca ...... 19 Onychodromus ...... 15 MYXOZOA...... 20, Table 1 Oocardium...... 25 ¡yfyxozoa ...... 27 Oodinium ...... 14 yiyzocytium...... 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 Nonion ...... 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 Paraíso tri cha...... 17 Olpidiopsis...... 23 Paramarteilia ...... 20 Olpidium...... 26 Paramecium...... 15, 16 46 J. O. Corliss
Paramoeba...... 18 Phacotus...... 25 Paramyxa...... 20 Phacus...... 11 Param yxidea...... 20 Phaeocystis ...... 23 Parapedinella...... 21 Phaeodarea ...... 20 Parastasia...... 11 Phaeodina ...... 20 Paratetramitus...... 10 Phaeophila...... 25 Parauronema...... 16 Phaeophyceae ...... 22, Table 1 Parvicapsula...... 20 PHAEOPHYTA...... 21, Table 1 Parvicorbicula...... 13 Phagodinium ...... 12 Pascherina...... 25 Phagomyxa ...... 12 Patelliferea...... 23, Table 1 Phalacrocleptes...... 15 Patellinella...... 19 Phalansterium...... 12 Paulinella...... 18 Phascolodon ...... 15 Paurotricha...... 16 Phialinides ...... 17 Pavlova...... 23 Philaster...... 16 Pavlovea...... 23, Table 1 Philasterids ...... 16 Pediastrum...... 25 Phragmonema ...... 26 Pedinella...... 21 Phreatamoeba...... 9 Pedinellea ...... 21, Table 1 Phreatamoebida...... 9 Pedinelleans ...... 21 Phtorophrya ...... 16 Pedinellids ...... 21 Phyllopharyngea ...... 15, Table 1 Pedinellophyceans ...... 21 Phyllophora ...... 26 Pedinomonas ...... 24 Physarum...... 13 Pedinophyceae ...... 24, Table 1 Phvsoderma ...... 26 Pelagococcus ...... 22 "Phytoflagellata"...... 5 Pelagohalteria ...... 15 Phytomonadida ...... 25 Pelagomonas ...... 22 "Phytomonads" ...... 27 Pelagophyceae...... 22, Table 1 Phytomonas ...... 12, 25 Pelagostrombidium ...... 15 Phytophthora ...... 23 Pelobiontea ...... 9, Table 1 Piroplasmida ...... 18 Pelomyxa...... 9,30 Placus...... 16 Penardia...... 18 Plagiacantha...... 20 Peniculines ...... 15 Plagiocampa...... 16 Peniculinia ...... 16 Plagiopyla...... 17 Peniculistoma...... 16 Plagiotoma ...... 15 Peranema...... 11 Planicoleps...... 16 Percolomonadea ...... 10, Table 1 Planorbulina...... 19 Percolomonas ...... 10 PLANTAE...... 5, 8, 10, 21, PERCOLOZOA ...... 10, 11,28, 29, Table 1 27, 31, Table 1 Perezia...... 10 Plasmodial slime molds ...... 13 Peridinium...... 14 Plasmodiophora ...... 12 Peritrichia...... 16 Plasmodiophorida ...... 12 Peritromus...... 15 Plasmodium...... 18 Perkinsidea ...... 17, Table 1 Platyamoeba...... 18 Perkinsus...... 17 Platychilomonas ...... 12 Pernina...... 10 Platycola...... 16 Peronosclerospora ...... 23 Platyophrya...... 15 Peronospora ...... 23 Pleistophora ...... 10 Petalomonas ...... 11 Pleodorina ...... 25 Phacodinium ...... 15 Pleurasiga...... 13 "User-friendly" Classification of the Protists 47
¡¡¡¿uraspis...... 19 Protoheterotrichs...... 15 pleurastrum...... 25 Protoopalina...... 12 porochloris ...... 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, ; pieurostomes ...... 17 Table 1 ploeotia...... 11 PRYMNESIOPHYTA...... 23 Pneumocystis...... 26 Prymnesium...... 23 Pocheina ...... 10 Psalteriomonas ...... 10 j Podophrya ...... 15 Psammetta...... 19 Podosira ...... 22 Pseudobalanion...... 16 Polycycla...... 16 Pseudobodo ...... 21 Polycystinea ...... 20, Table 1 Pseudocharaciopsis...... 22 ] Polyhymenophora ...... 14, Table 1 Pseudociliatea ...... 11, Table 1 i Polyhymenophoreans ...... 15 Pseudodendromonas ...... 12 Polykrikos ...... 15 Pseudodifflugia...... 18 Polvmyxa...... 12 PSEUDOFUNGI...... 23, 26, Table 1 Polysphondylium ...... 13 Pseudo glaucoma...... 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 1 Prostomatea ...... 16, 17, Table 1 Pyrenomonas ...... 23 Prostomatida ...... 16 Pyrocystis ...... 14 Protalveolatea ...... 13, 29, Table 1 Pyrophacus...... 14 1 Proteomyxids ...... 12 Pyrrhophy ta ...... 14 I Pfoteromonads ...... 28 Pyrsonympha...... 10 Pteromonas ...... 12, 30 Pythium...... 23 Pterospongia ...... 13 Proterozoea ...... 12, 29, Table 1 i p r o t is t a ...... 4, 5,27 Q ’ Protociliata ...... 12 ïr°tocruzia...... 15 Quasillagilis...... 17 ^O T O C T IST A ...... 4 Quinqueloculina...... 19 1
48 J. O. Corliss
R Rotaliella...... 19 Rudimicrosporea ...... 10, Table 1 Raabella...... 15 Radiolaria ...... 20, Table 1 S Radiolarians ...... 20 Radiophrya...... 16 Saccammina...... 19 RADIOZOA...... 19, 29, Table 1 Saccamoeba...... 18 Raphidiophrys...... 19 Saccinobaculus...... 10 Raphidomonadea ...... 21, Table 1 Salpingoeca...... 13 Raphidonema...... 25 Saprodinium...... 15 RAPHIDOPHYTA...... 21, Table 1 Saprolegnia...... 23 Reclinomonas ...... 12 Sarcinochrysis ...... 22 Red algae...... 24-26 Sarcocystis ...... 18 Reichenowella ...... 15 "Sarcodina" ...... 18 Remanella ...... 14 Sargassum...... 22 Resultor...... 24 Saurocytozoon ...... 18 Reticulosphaera...... 22 Scaphidiodon ...... 15 Retortamonadea ...... 10, Table 1 Scenedesmus...... 24 Retortamonadida ...... 10 Schellackia ...... 18 Retortamonas ...... 10 Schizammina ...... 19 Rhabdoaskenasia...... 17 Schizocalyptra...... 16 Rhabdomonadida ...... 11 Schizocystis ...... 17 Rhabdomonas ...... 11 Schizomerus ...... 25 Rhabdophorids ...... 16 Schizopyrenida ...... 10 Rhabdophrya ...... 15 Schwagerina ...... 19 Rhabdostyla ...... 16 Sclerospora ...... 23 Rhinomonas ...... 23 Scourfieldia ...... 24 Rhinozeta ...... 17 Scuticociliatia ...... 16 Rhipidium...... 23 Scyphidia ...... 16 Rhizammina...... 19 Scytosiphon ...... 22 Rhizidiomyces ...... 23 Sea lettuce ...... 25 Rhizochromulina ...... 22 Sea weeds ...... 22, 25, 26 Rhizoclonium ...... 25 Selenastrum...... 25 Rhizodinium ...... 14 Selenidioides ...... 17 Rhizophydium ...... 26 Selenidium ...... 17 RHIZOPODA...... 9, 10, 13, 18, 26, Selenita ...... 19 Table 1 Selysina...... 18 Rhizosolenia ...... 22 Semitrichodina ...... 16 Rhizosphaera...... 20 Sicuophora ...... 15 Rhodella ...... 26 Siedleckia ...... 17 Rhodochaete ...... 26 Silicoflagellatea ...... 21, Table 1 Rhodomonas ...... 23 Silicoflagellates...... 21, 22 Rhodophyllis ...... 26 Singhamoeba ...... 10 RHODOPHYTA...... 26, Table 1 Sinuolinea...... 20 Rhodospora ...... 26 Siphonocladus ...... 25 Rhynchocystis ...... 17 Sirogonium ...... 25 Rhynchomonas ...... 12 Slopalinida ...... 12 Rosalina...... 19 "Slopalinids"...... 28 Roscoffia ...... 14 Sny de relia ...... 11 Rosculus...... 18 Sonderia ...... 17 "User-friendly" Classification of the Protists 49
Sorites ...... 19 Stichotricha...... 15 Sorocarpus...... 22 Stilopsis ...... 22 Sorodiscus ...... 12 - Stokesia ...... 16 Sorogena ...... 15 Stoneworts ...... 25 j 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 , Spirogyra ...... 25 Syndinium ...... 14 Spiroloculina...... 19 Synura...... 22 Spiromonas ...... 17 Synurophyceae ...... 22, Table 1 Spironema...... 12 Spironucleus...... 10 T Spirostomum ...... 15 j 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 Spraguea ...... 10 Tetramitus...... 10 Spumella...... 22 Tetramyxa ...... 12 ^ Stannophyllum...... 19 Tetraselmis...... 24 Staurastrum...... 25 Tetraspora...... 25 Steinella...... 16 Tetrasporidium...... 25 Stemonitis ...... 13 Textularia ...... 19 Stempellia...... 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 Thigmocoma ...... 16 50 J. O. Corliss
Thigmophrya ...... 16 Triloculina...... 19 Thigmotrichs...... 16 Trilospora...... 20 Thoracosphaera ...... 14 Trimitus...... 10 Thorea ...... 26 Trinema...... 18 Thraustochytriacea ...... 21, Table 1 Triparma...... 22 Thraustochytrium...... 21 Trochilia ...... 15 Thylakidium...... 15 Troglodytella ...... 17 Tiarina...... 16 Trypanosoma...... 12, 30 Tintinnids ...... 15 Trypanosomatida ...... 12 Tintinnopsis...... 15 Trypanosomatids ...... 11 Tokophrya ...... 15 Tubulina...... 13 Tolypella...... 25 Turaniella...... 16 Tontonia ...... 15 Tuzetia...... 10 Toxarium...... 22 Tyzzeria...... 18 Toxoplasma...... 18 Trachelocerca ...... 14 U Trachelomonas ...... 11 Trache Ionema ...... 14 Ulothrix ...... 25 Tracheloraphis...... 14 U lva...... 25 Tracheophytes...... 24 Ulvophyceae ...... 25, 31, Table 1 Transitella...... 15 ULVOPHYTA...... 25, 31, Table 1 Trebouxia...... 25 Umbilicosphaera...... 23 Trentepohlia...... 25 Undella...... 15 Trepomonadea ...... 9, Table 1 Unicapsula...... 20 Trepomonas...... 10 Unicauda...... 20 Treubaria...... 25 Unikaryon...... 10 Triadinium...... 17 Uradiophora ...... 17 Tribonema ...... 22 Urceolaria...... 16 Tribophyceae ...... 22 Urocentrum...... 16 Triceratium...... 22 Uroglena ...... 22 Trichamoeba ...... 18 Uronema...... 16 Trichia...... 13 Uronychia ...... 15 Trichochona ...... 15 Urosomoides ...... 15 Trichodina ...... 16 Urospora...... 31 Trichodinopsis ...... 16 Urosporidium...... 20 Trichomonadea ...... 11, Table 1 Urostyla...... 15 Trichomonadida ...... 11 Urotricha ...... 16 Trichomonas ...... 11, 30 Uro zona ...... 16 Trichonympha ...... 11 Utriculidium...... 22 Trichonymphida ...... 11 Uvigerina...... 19 Trichophilus ...... 25 Trichophrya ...... 15 V Trichosarcina ...... 25 Trichosphaerium...... 18 Vacuolaria...... 21 Trichospira ...... 17 Vaginicola ...... 16 Trichostomes...... 17 Vahlkampfia...... 10 Tricornia ...... 10 Vairimorpha...... 10 Tricoronella ...... 15 Valonia...... 25 Trigonomonas ...... 10 Vampyrella...... 18 Trihymena...... 15 Vampyrophrya...... 16 "User-friendly" Classification of the Protists 51
^annella...... 18 Xiphophora ...... 22 Vasichona...... 15 Xystonellopsis...... 15 Vasicola...... 16 Vaucheria...... 22 Y Vegetabilia...... 6 Verrue alvus...... 23 Yamagishiella...... 25 Vestibuliferans ...... 17 Yellow-green algae...... 22 Vestibulongum...... 17 Yvonniellina...... 15 Vexillifera...... 18 VIRIDIPLANTAE...... 24, 29, 31, Table 1 Z Vischeria...... 22 Volvocida...... 25 Zelleriella...... 12 Volvocids...... 27 Zonaria...... 22 Volvocines...... 30 Zooanthella ...... 14 Volvox ...... 25, 27 "Zoomastigophora"...... 5 Vorticella...... 16 Zoophagus ...... 23 Zoosporea...... 17 W Zoothamnium ...... 16 Zosterodasys ...... 15 Wallackia...... 15 Zschokkella ...... 20 Wardia...... 20 Zygnema ...... 25 Wenrichia...... 16 Zygnematophyceae ...... 25 Wenyonella...... 18 Zygocystis ...... 17 Woodruffia...... 15 ZYGOMYCOTA ...... 26 Woronina ...... 12 Zygophyceae ...... 25 Zymurgia...... 26
Xanthidium...... 25 Xanthophyceae ...... 22, Table 1 Xenophyophorea ...... 19, Table 1 Xiphacantha...... 19 Received on 2nd November, 1993