What are the taxonomic and evolutionary relationships of the protozoa to the protista?

BioSystems, 14 (1981) 445--459 445 Elsevier/North-Holland Scientific Publishers Ltd.

WHAT ARE THE TAXONOMIC AND EVOLUTIONARY RELATIONSHIPS OF THE PROTOZOA TO THE PROTISTA?*,**

JOHN O. CORLISS

Department of Zoology, University of Maryland, College Park, MD, 20742, U.S,A.

(Received June 3rd, 1981)

In order to consider the problems of protist-protozoan interrelationships in proper pempective, a new "packaging" of phyla within the great kingdom Protista is proposed. Although it is based largely on hktorical groupings and is admittedly "unnatural" (nor are taxonomic names proposed for my five supraphyletic groupings), the arrangement may clarify some long-persisting problems, aspecially with regard to mixed algal-protozoan groups and/or phylogenies. Some three dozen phyla are recognized as comprising the kingdom, with the number that might be considered as "protozoan" ranging from 10 to 25, depending on one's viewpoint. No taxon should have the formal name "Protozoa", "Phytoflagellate" and "zooflagellate" are also misleading categories. Taxo- nomic and evolutionary relationships of phyla containing protozoa (with small "p") are inextricably intermeshed with those of other protist phyla, and thus no unified protozoan super-group exists.

I. Introduction

The seemingly innocent inquiry posed in the title of this paper actually involves a number of further questions of a difficult and largely unresolved nature, partly because they are usually neglected and partly because answering them wholly satisfactorily would require a much broader general knowledge as well as many more specific data of relevance than we now possess. Nevertheless, focusing some attention on such very questions is in order in light of the widespread renewed attention being given today to such highly significant and most fascinating problems as eukaryogenesis itself and the origin of complex multicellular organisms fxom an alleged unicellular ancestry,

*This paper is based on an invited presentation made at the Conference on Cellular Evolution (Fourth International Meeting of the Society for Evolutionary Protistology) held 31 May--3 June 1981 at the Uni- versity of Maryland's Donaldson Brown Conference Center, Port Deposit, Maryland, USA. **Support of National Science Foundation grant DEB 79-23440 is gratefully acknowledged.

problems not unrelated to the less studied ones to which I wish to call attention here.

There are two basic questions that must be addressed first of all, however briefly; they are these deceptively simple queries: (1) What do we mean by "Protista '~. and (2) What do we mean by "Protozoa"? Only then can we pursue the matters of possible taxonomic and evolutionary o~ phylogenetic affinities among groups of organisms represented by those labels.

In the past 3 or 4 years we have witnessed a truly phenomenal avalanche of papers, and even books and monographs, on topics at least indirectly relevant to the theme of this paper. That is, such works have been concerned with protist taxonomy, the place of protists in the biotic world, the evolution of cells, the origin of "cellular inclusions", or the fine structure or biochemistry of protists or of certain of their constituent parts. The stimulus for much of this out- pouring of new protistological literature may be attributed to a single publication of just a decade ago, the heuristic (first) book of Margulls (1970) on what F.J.R.

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Taylor later named the Serial Endosymbiosis Theory.

It seems unnecessary to cite a couple of hundred papers directly here, especially when a much smaller number of highly pertinent and excellent review works are easily available (indeed, several have appeared in recent numbers of this journal). And even from that reduced number, a cluster of half a dozen should suffice for any reader inter- ested in acquiring a background for the present overview or in delving into the mass of primary sources from the original scattered literature, starting with Haeckel (1866) and Hogg (1860). These bibliographically r i c h - and highly stimulating as well -- works are the following: Cox {1980), Dodge {1979}, Margulis {1981), Tappan (1980}, Taylor (1978), and Whittaker and Margulis (1978). Special mention should be made of Copeland's (1956) perceptive and illuminating contribu- tion to protist taxonomy: in fact, his book was practically the only "bright light" thrown on the subject throughout the first 65 years of the present century.

2. The kingdom Protista

For more than a century now, commencing with Ernst Haeckel, a taxonomic group called the Protista (sometimes, in an expanded form, the Protoctista, proposed still earlier by Hogg and noted for its not being restricted to unicellular forms) has been variously recognized, variously maligned, and variously defined. The most recent "thumbnail" characteriza- tion is that by Margulis (1981: see its Appendix). For my purpose, I propose the following brief description, recognizing -- along with many other workers -- the Protista as one of five major kingdoms of contemporary organisms.

Primarily small, unicellular (but complete) organisms of the superkingdom EUKARYOTA, motile or non-motile, free- living in a great diversity of mainly aquatic (but also terrestrial) habitats or symbiotic

in or on numerous hosts. Some symbiotic species highly virulent, others have commen- salistic or even mutualistic relationship witk host organism. Commonly solitary but capable of exhibiting colonial {including filamentous) organization, occasionally reaching a level of syncytial or even multicellular composition, with the latter, however, typically limited to a single stage in the life cycle and/or of a relatively non- advanced nature. Diverse modes of nutrition: ingestive, absorptive, or photoautotrophic (the last when plastids, which may contain a variety of pigments, are present), or some combination of these three. Aerobic metabolism common, but anaerobic mechanisms used (even obligatorily) by some forms. Variation in reproductive cycles, but with mitosis (several kinds possible) occurring during methods of asexual fission and meiosis in whatever sexual phenomena may be exhibited. Nuclei may be single or multiple, homokaryotic or heterokaryotic {e.g., the dual nuclear apparatus of ciliates), and haploid, diploid, or polyploid with respect to numbers of sets of chromosomes. Life cycles may involve polymorphism; a stalked stage common in some groups. Most forms motile, possessing pseudopodia, flagella, or cilia (the latter two composed of tubulin microtubules in a characteristic "9 + 2" pattern), though some move by other means, in at least one (generally the trophic) stage of the life cycle. Pseudopodia may be of different kinds; flagella are often present as a single pair, but sometimes in abundance, typically arising from or near the anterior pole; cilia are characteristically numerous, as single or compound structures, and are associated with a complex infraciliature or kinetidal system. Spores or cysts may be produced, and extracellular thecae, shells, or loricae may be constructed.

In general, nuclear and other included organellar or cytoplasmic structures are not dissimilar (in ultrastructural composition, biochemical properties, etc.) from the alleged homologous structures of cells of the

so,ailed "higher" multiceUuiar organisms: the contrast is with the analogous features manifest by members of the more primitive superkingdom PROKARYOTA (exemplified by the bacteria sensu lato). On the other hand, advances of the other three eukaryotic kingdoms (Plantae, Fungi, Animalia) rarely shown by protists include a complicated multicellular organization with complex cell junctions, tissue and organ differentiation, and stages of a "true" embryological development.

Thus, by "Protista" I mean a kingdom of organisms that manifests a kind of evolutionary as well as taxonomic cohesiveness. It is not a "motley array of poorly understood microorganisms", an "unnatural 'rag-bag' of organisms", a ''taxonomic compromise of no value", a "phylogenetic wastebasket of little known microscopic forms" -- as some people have implied --by any means (the latest voice to be heard echoing such senti- ments is that of Round, 1980). Nor, in my opinion, is it quite cricket to consider it as merely a way station enroute to the Big Three Kingdoms That Really Matter, the multicellular Plantae, Fungi, and Animalia; or as only a Gap Bridger between prokaryotes and multicellular organisms.

We'll return shortly to discussion of the composition of this kingdom, but it is quite clear that it contains many distinct groups, mainly unicellular, some of which are much closer together phylogenetically than are others. Protozoa, algae, 'qower" fungi, and various mixes of these (see below) can be included. Perhaps a conservative splitter would recognize as many as three dozen phyla in taxonomic appreciation of their diversity, their deel>seated differences having arisen during many aeons of phylogenetic separation from one another.

3. The "Protozoa"

The answer to my original second question, what do we mean by the protozoa?, is far

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more difficult to deal with; but we can quickly say that they are a subset or subsets of the Pmtista taxonomically, in agreement with remarks in the preceding section of this paper. First of all, however, I strongly suggest -- nor am I the first to do so (e.g., see Kerkut, 1960, and recent works by various authors; see also Corliss, 1980, 1981)- that we officially drop "Protozoa", with a capital "P", as the name of any formal taxon at any level. I see no advantage in continuing to recognize a phylum Protozoa (although this will be carried on in biological textbooks for many decades into the future, I'm certain), a subkingdom Protozoa, or any other kind of evolutionary or taxonomic or classificational group called "Protozoa". The so-called teaching convenience is outweighed by the disadvantage of perpetuation of a grave mis- conception. That is, any single group "Protozoa" is so polyphyletic with respect to its origin(s) that it is criminally misleading to teach students that a uniformity-by-kinship exists within it. Fortunately, from a pedagogi- cal point of view, the abandonment of "Protozoa" does not require the dropping of "protozoa" (singular, "protozoon"), with a small "p", or "protozoan", "protozoology", "protozoologist", etc. as perfectly good descriptive terms for many of the organisms (or studies on them or students of them) included in certain groups contained within the kingdom Protista. In a general way, the same can be said for the vernacular term "algae". Nevertheless, such names should be used with caution. And, while we're on the topic, I recommend dropping --with capital or lower-case initial letter -- of such words as "plant protists" and "phyto-" or "zooflagellates", because they have highly misleading connotations (notably, pitting "pigmented" vs. "colorless" when often such is not the case).

I've implied above that the groups of organisms traditionally considered to comprise a single taxon named "Protozoa" are often either too distantly related to each other or more closely related to other

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"non-protozoan" taxa to be treated as a monophyletic unified "super-group". Yet critics will persist that this is not so, pointing out that textbooks and research monographs alike have always managed to define, characterize, or diagnose protozoa as possessing a number of significant traits in common. Two truths have been ignored, subconsciously or otherwise: some such characters (e.g., unicellular, eukaryotic, microscopic in size) are also typical of various non-protozoan groups; and others, general ones, such as the first and third just listed, or specific ones unique by virtue of their absence elsewhere in the biotic world, are not demonstrable throughout all groups that are treated as protozoa. Therefore, I prefer to recognize multiple "protozoan" phyla not assembled under a single heading, as discussed further below.

The very word, proto-zoa, with its inescapable connotation of "first animals", was -- from the vantage point of hindsight -- an unfortunate choice. Possibly certain protozoan species, perhaps from a group now extinct and without a fossil record, did give rise to early members of the kingdom Animalla; but the likelihcod of identifying such forms among contemporary groups is slim, to put it optimistically. The fact that zoologists were generally the first biologists to study protozoa -- and botanists the bacteria, algae, and fungi -- is today of historical interest only, amazingly influential though it has been in the drawing of taxonomic conclusions among researchers, as well as teachers and textbook writers, even up into the 1980's.

Anticipating the following sections, the title of this paper might better have read: what are the taxonomic and evolutionary relationships of so-called protozoan groups (or subgroups) to other groups assigned to the same kingdom, the Protista? I think that it will be instructive to consider that five major groups -- NOT to be given formal taxonomic ranks or names (especially since they admittedly may lack internal cohesiveness

and even be p o l y p h y l e t i c ) - comprise the Protista sensu lato and that these, in turn, contain various numbers of subgroups, which may well be representative of distinct taxonomic phyla (though no latinized names will be employed here, only vernacular terms: but practically all of them, I should add, do have perfectly good names -- at the level of phylum or lower -- available in the vast taxonomic literature on such assemblages of organisms). It will become frustratingly clear that so-called "protozoan" groups are inextricably comingled -- taxonomically as well as phylogenetically -- with other protist groups (as Taylor, 1978, and others have recognized but not emphasized).

4. The five major groupings of Protist Phyla

These may be labeled: Protozoan Group, Protozoalgal Group, Algal Group, Protozo- fungal Group, and Fungal Group. This is a unique "packaging" of the major protist taxa: the included groups under each heading are not, all told, particularly unique or originally conceived by me. This way of looking at or reviewing the total picture, however, may be of value.

I am greatly indebted to several modern workers for their very recent comprehensive taxonomic and evolutionary treatments of protist taxa, and I see no need in repeating their detailed characterizations, etc., here. Generally, I have no quarrel with their most helpful descriptions, unabashedly adopting (as well as endorsing) some of them directly (in abbreviated form) in parts of this paper. The dozen or so works serving as greatest primary or secondary sources of data are those of Corliss (1979a,b), Cox (1980), Dodge (1979), Heath (1980), Leedale (1974), Levine et al. (1980), Margulis (1981), Sleigh (1979), Stewart and Mattox (1980), Tappan (1980), Taylor (1976, 1978, 1980a,b), Whittaker (1977), and Whittaker and Margulis (1978).

Although the majority of detailed characteristics used comparatively in drawing my con-

cluaions are neither discussed nor listed anywhere in this paper, the principal categories f rom which they have been taken are the following: mitochondrial features, types of plastids, flagellar characteristics, kind of life style, modes of fission and locomotion, kinds of nutrition, cellular or supracellular organization, microtubular and fibrous and filamentous structures associated with flagellar basal bodies, plasma membrane and features of the cortex, Golgi characters, kinds of extrusomes, food storage products, and numerous characteristics of the nuclei (including mitotic figure, etc.). Using such multiple sources is in keeping with my Constellation of Characters Hypothesis (Corliss, 1976, 1979a), invaluable in comparative phylogenetic considerations. To at least partially counteract my largely "intuitive approach" -- which is a method- ology so heavily frowned on these days -- I've had available to me the results of a computer analysis involving some 136 such characters and 34 flagella-bearing protist taxa made by Ms. Diana Lipscomb (see Corliss and Lipscomb, 1982, in press). Although the objectives of that study -- determining the proper phylum to which to assign the enigmatic 8tephanopogon, ciliate- turned-flagellate -- were quite different, some of our findings there have, in turn, supported the arrangements of taxa proposed in the present paper. I have also been influenced by the coded features of culturable strains of protozoa published recently by Daggett et al. (1981).

A further word -- one of caution -- might be added concerning all writers' search for the phylogenetic markers that will produce the "best" tree for any groups under particular study: such sometimes elusive indicators of high evolutionary information content have been termed semes by Hanson (1977). The trend of the past decade has been to implicate ultrastructure, frequently at the expense of other sources of characteristics, and to concentrate on only a few organenes

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or systems, most notably the flagella or cilia (and their basal body complexes), the plastids and their pigments, the mitochondria, or the nuclei and their division figures. Examples of this may be found in various of the works cited elsewhere in this paper; even influential, well-meaning treatments (such as those by Casper, 1974; Dodge, 1973, 1979; Heath, 1980; Lynn, 1981; Pickett- Heaps, 1975; Stewart and Mattox, 1980; and Taylor, 1976) may sometimes tend to be at least partially guilty of this. I am not chiming that such approaches are without value - - the very opposi te is t r u e - but I am suggesting that the dangers and pitfalls of stressing "favorite systems", if done more or less in isolation, must be kept in mind. Finally, even in using multiple characteristics, the choice of method of handling one's data may signifi- cantly influence the shape of the phylogenetic tree produced. I am referring to the "big three" methodologies, the so ,a i led cladistic, phenetic, and synthetic approaches. Fortuna- tely, this topic is being covered elsewhere in depth by Lipscomb (pets. comm.), so no more need be said here about it.

I. The Protozoan Group

Protists that have conventionally been assigned to "Protozoa", with at most mild murmurs of protest from a few phycologists or zoologists, seem to me to fall into some 10 subgroups each of which could stand as an independent taxon at perhaps as high as the phylum level. This grouping does not signify equal "closeness" of all contained taxa; nor does the arrangement, from first to last as listed below, indicate a single line of evolution from "simple" to "complex". Some groups contain many species (e.g., thare are many t h o u ~ n d s of "forams", counting both extinct and extant forms); others, relatively few (only one pelobiontid?! ). I believe that physiological, morphological, and ultrastructural information available in

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the literature justifies both the inner unity of these phyla and their outer high-level separation one from another. It remains to be seen if biochemical-molecular data will support the taxonomic conclusions proposed here for the groups involved (the review by Ragan and Chapman, 1978 has set the stage for research in this exciting area}. As mentioned earlier, only a brief comment or two is given for each entry in the list that follows: no at tempt has been made to offer full characterizations here.

(1) Pelobiontids. Pelomyxa palustris, a unique amoeba with no mitochondria, no Golgi bodies, no mitosis; but contains intriguing symbiotic prokaryotes and has a few basal bodies associated with some kind of flagellum. Sexless.

(2) Rhizopodians. Naked and shelled amoebae and close relatives, including amoeboflagellates, "lower sarcodinids" of the literature. Xenophyophorids may be placed here tentatively.

(3) Foraminiferans. The "forams", with their distinctive calcareous tests, etc. Many fossils, of use as biostratigraphic markers though of little value phylogenetically outside the group itself. A few of latter reach diameter of greater than six inches.

(4) Actinopodians. "Higher sarcodinids", comprised of four classes of quite distinct forms: the heliozoa, acantharids, poly- cystinids, and phaeodarids. Predominantly marine, with siliceous skeletons forming an ooze thousands of feet in depth over much of the ocean floor. Their common possession of axopodia represents their main unifying feature.

(5) Metamonads. The "higher zooflagellates" of the literature. Colorless, multi- flagellate forms. [Note the complete absence of "'lower zooflagellates" from this whole Protozoan Group! ].

(6) Opalinids. Probably closer to metamonads than any other group, on the basis of some salient features, but still largely enigmatic forms. Superficially resemble certain holotrichous ciliates.

(7) Ciliates. Large, diverse (from gymno- stomes to pelagic tintinnines and the ubiquitous hypotrichs), yet basically com- pact group, distinct from all others; kinetidal system and nuclear dualism unique.

(8) Sporozoa. Gregarines, coccidia (including the malarial parasites), and piroplasmids; recently unnecessarily renamed the "Apicom- plexa", based on their common possession of apically located unique ultrastructures. All included species symbiotic in some other organism.

(9) Microsporidians. Unique spores; minute obligate intracellular parasites of many other organisms. (Haplosporidians here or separate?)

(10) Myxosporidians. Unique spores, with a preceding multicellular stage in life cycle; all coelozoic or histozoic parasites of cold- blooded vertebrates. Renamed "Myxozoa" recently and considered by some to be a primitive group of Animalia.

Excluded from this Protozoan Group and from the entire kingdom Protista are the Parazoa {sponges), Mesozoa (curious acoelo- mate parasitic '~vorms"), and Placozoa (very simple, but diploblastic, multicellular fre~ living forms), groups that sometimes are considered protists (or "protoctists") sensu lato.

II. The Protozoalgal Group

By my presenting and naming this and the following group of phyla as I have, I hope that I am accomplishing more than just a happy compromise with our long-suffering phycological colleagues. The habit, over past decades, of separating taxa, sometimes even genera within a single family, at kingdom level simply on the basis of presence or absence of detectable chloroplasts (usually meaning whether the implicated organisms were being studied by a zoologist or a botanist, alas) has got to be branded as ridiculous and brought to a screeching halt. The forms included here, broadly known as the "phytoflagellates", are typically unicellular (solitary

or colonial), motile (usually biflagellate), and more often (but far from exclusively) contain photosynthetic pigments, though even colored species are not solely photoauto- trophs in their nutritional proclivities. In my view, these organisms can be thought of as either "algae" and/or "protozoa", underlining my earlier point of the inadvisability of recognizing Protozoa and Algae as independent formal taxonomic groups. What is significant is that they are all protists. Furthermore, the phyla included here may have phylogenetic affinities with various other protist phyla -- of this and/or the other four groups I recognize -- quite independently of each other. I wish to stress that my five categories, somewhat like ' ~ e y " characters, are for practical convenience and for historical continuity in discussion and do not represent distinct and separate taxonomic or evolutionary divisions. [As a "practicing protistologist", I should like to see some uniformity in taxonomic treatment of the subgroups within each of the phyla, some agreement on disputed nomenclatural matters, etc.; I believe that these goals may come to fruition in the near future, as more of us show a willingness to support them.]

The first five taxa of my Protozoalgal Group comprise, in effect, what may be called " the Chlorophyte Series sensu stricto"; the second five, ' t h e Chromophyte Series sensu stricto". This is an adaptation of Christensen's {1966) lineages (expanded to series by Taylor, 1978, and also recognized by others), with the general omission of taxa of a rank below the level of division or phylum and the specific omission of the dinoflagellates and the assemblages included by me in other categories (see below). It is worth mentioning -- as Taylor (1978) and Stewart and Mattox (1980} have particularly pointed out -- that the latter Series, with its widespread possession of tubular mitochondrial criatae, chlorophylls a + c, etc., is alleged to have given rise to practically all other protist groups, particularly the "protozoan" phyla listed under "I" , above;

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whereas the former Series (with its lamellar- type cristae, chlorophylls a + b, etc.) pre- sumably has served primarily as ancestral material for members of the other three great eukAryotic kingdoms (Plantae, Fungi, Anima~a).

(1) Euglenids. Plastids, when present, grass- green; paramylon as distinctive storage product. Important non-pigmented forms that I assign here include the trypanosomes and relatives (former "lower zooflagellates"), possibly some other "zooflagellate" genera little studied to date with care, and, now, the enigmatic "ciliate" Stephanopogon (see especially Corliss and Lipscomb, 1982, and Lipscomb and Corliss, 1981: we have assigned Stephanopogon to an order of its own, the Pseudociliatida, which may have to be raised to status of class as more comparative research is carried out). First group of my "Chlorophyte Series". Sexuality not yet conclusively demonstrated.

(2) Cryptomonads. Plastids, when present, brown, red, olive-green, etc. (uniquely con- talning phycobilin pigments and chlorophylls a + c2). Unique ejectosomes. Sexless.

(3) Prasinomonads. Grass-green chloroplasts; scaly flagella, and body also often covered with (Golgi<ierived) scales. Sexual reproduction known.

(4) Phytomonads (Volvocids). The cele- brated Chlamydomonas -~ Volvox line so beloved of zoologists, who fiercely claim as protozoa these chlorophytan (in Margulis' class Chorales) " t rue" algae without recognizing (= ignoring!) their undeniable close relationship to the (other) major grass~q~een algal taxa (see Group III, below). Motile vege- tative cells. Sexual reproduction well known. [I include these organisms here because of their obvious "protozoalgal" features, including motility; but they belong with the (other) chlorophytes, perhaps as a taxon at only the ordinal level there.]

(5) ChoanoflageUates. Group of uncertain taxonomic and phylogenetic affinities; perhaps better maintained at a level well below phylum. Collared organisms; most

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species colorless, stalked or free-swimming, with characteristic basket-like "lorica" of siliceous costae.

(6) Chrysomonads. Golden-yellow or yellow-brown plastids, when present; unique arrangement of mastigonemes on flagella; other unique features. Sexual reproduction exhibited. First group of my "Chromophyte Series". Silicoflagellates may (or may not} belong here; also, perhaps the curious bicosoecids (whose name has been spelt at least four different ways! ).

(7) Haptomonads (Prymnesiomonads). Unique third appendage between two smooth flagella, the haptonema; body characteristically covered with patterned organic scales (when calcified = coccoliths, responsible for name of major subtaxon, the coccolitho- phorids). Sexual reproduction known.

(8) Eustigmatomonads. Lack chlorophyll c; number of other distinctive features, such as zoospores with eyespot reminiscent of that of euglenid protozoalgal species.

(9) Heterochlorids. Group formerly with the xanthophytes (see below), but possibly deserving of independent status at quite high taxonomic level; yellow-green plastids, but some chrysomonad features, etc.

(10) Chlorornonads. Like the heterochlorid situation, above, though just reversed: formerly with chrysomonads (yellow plastids, etc.), but recently shown to have some xanthophytan characteristics; possibly a high-level independent taxonomic status warranted.

(11) Dinoflagellates. Diverse assemblage of highly distinctive biflagellate unicellular forms, widespread, especially in plankton; both photoautotrophic and heterotrophic species known; also numerous symbiotic forms in diverse hosts; cellulose theca in some subtaxa; unique xanthophyll pigments as well as chlorophyll a and c and carotene {thus, variety of colors exhibited); "mesokaryotic" nuclei showing number of unusual features; pellicular alveoli as part of a ciliate-like cortex; numerous other specialized characteristics. All such traits support a separate phylum (at least!) status for these "phyto-

flagellates" that also show affinities with groups of the "Chromophyte Series". Their unique combination of very "primitive" and very "advanced" protist characters make most difficult a clear understanding of their phylogeny, though many investigators are working on the problem (e.g., see Loeblich, 1976; Tappan, 1980; Taylor, 1980b; and papers cited therein).

As mentioned under the euglenids (No. 1, above), some peculiar non-pigmented forms, including a couple of marine symbiotic species, need to be more extensively studied (ultrastructurally, etc.) before their taxonomic or phylogenetic relationships can be positively determined. Very likely, however, they should be assigned somewhere within my Protozoalgal Group. These include Colponema, Cyanophora, Cyathobodo, Isonema, Pseudodendromonas, Rhipidoden- dron, Spiromonas, and Spongomonas, genera usually considered to be "lower zooflagellates" in the literature. Until very recently, as mentioned above, Stephanopogon -- as a homokaryotic gynmostome ciliate -- would have graced this list as well.

III. Algal Group

I include six of the major "classical" taxa of algae here, ranging from clearly unicellular groups to the multicellular red and brown algae. Pigmented species are the rule; and/but motility by means of flagella is rare except in heterochlorids and phytomonads (volvocids), which -- interestingly enough -- I have already treated in the preceding Group.

(1) Xanthophytes. Yellow-green algae; none of the accessory pigment fucoxanthin present; many filamentous species. Considered members of or arising from the "Chromo- phyte Series", as described in the preceding section. Heterochlorids often included here have been treated separately in the Proto- zoalgal Group.

(2) Chlorophytes. Grass-green or the green algae; associable with the "Chlorophyte Series". Chlamydomonas, Volvox, and closely

related "phytomonad" genera have already been covered as part of the Protozoalgal Group (above), whether advisedly or not. Some filamentous and syncytial (siphonous or coenocytic construction) forms- often macroscopic in size -- occur in this large phylum (or division) that includes such diverse genera as Acetabularia, NiteUa, and Ulva. Perhaps more than one phylum should be recognized here?

(3) BaciUariophytes. Diatoms. Typically golden brown; a few species colorless. Wide- spread group of symmetrical forms with numerous species, all essentially unicellular. Unique gliding motility possessed by vegeta- tive stage; some species have uniflegellate male gsmetes. Classification based almost entirely on the often intricate structure and ornamentation of the frustule (cell wall), which is composed largely of silicon.

(4) Zygnematophytes (Conjugatophytes--. Generally unicellular green forms, exclusively from fresh-water habitats; particularly noted for their exhibition of conjugation as part of their sexual reproduction; gametes amoeboid, non-flagellated. Spirogyra species numerous and well known; desmids represent a large part of the taxon, here considered a phylun~

(5) Rhodophytes. Red algae or "seaweeds", some several feet in length; unicellular (a few) to multicellular; mostly marine. No flagellated stages in life cycle, but sexual reproduction widespread. Phycobilins as accessory photosynthetic pigments. Serve as commercial source of agar. Thylakoids occur singly within the chloroplasts. Other specialized features also exhibited by many species. Considered by some workers as possibly very primitive group, phylogenetically, within the Protista; according to Taylor (1978), they may have arisen near (but before) the base of the "Chlorophyte Series" branch of the protist tree.

(6) Phaeophytes. Brown algae or "seaweeds", including kelps that reach length of 200 feet or more; almost exclusively marine and widespread (giving name, for example, to the Sargasso Sea). Even microscopic

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~implest species are multicellular, with composition of bodies ranging from filaments, generally branched, to huge n ~ i v e l y constructed thalli. Zoospores biflsgellate. Fucoxanthin important accessory pigment in photosynthesis; major food reserve is laminarin. Serve as commercial sources of algln and potash. Chloroplasts and reproductive structures characteristic of the phylum. Generally considered as comir~g off the "Chromophyte Series" branch (e.g., see Taylor, 1978).

Definitely excluded from my Algal Group are the "blue-green algae" (prokaryotic cyanobacteria) and the prochlorophytes (prokaryotic chloroxybacteria). Neither of these groups can be protists as defined in this paper.

IV. Pro tozo fungal Group

Somewhat as in the case of preceding Groups II and III, where I attempted to allay the fears of phycologists that the protozo- ologiats were "stealing away" many of their algal taY~, in this and the following section I hope to assure mycologists that some protists are either "proto animals" and "lower fungi", at one and the same time, or, better, that some protists are better left as protists (but) open to study by any school of professional biologists. The same kinds of chance tradition that made bacteria and algae into "plants" (because botanists were among the first to study them most extensively) have been instrumental in making fungi "plants" and then making certain more~r-less amoeboid protists into ("lower") fungi.*

*It is only fair, however, to acknowledge that algae (and bacteria, early on, especially) were/are also considered "plants" because of their widespread Immeasion of photosynthetic pigments and/or cell walls and/or frequent lack of independent motility. Fungi have been treated as "co lo r l~ plants" with simply a different kind of "root system", '~tem", etc. And certain amoebae sensu lato, though microscopic in size, are not only similarly non-pigmented but also exhibit the absorptive ("saprophytic", "saprozoic") mode of nutrition characteristic of "true" fungi.

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Four "classes" of organisms claimed and classified by both protozoologists and mycologists comprise my Protozofungal Group. I believe that they may each warrant phylum standing, especially in view of the fact that such a rank has been accorded numerous taxa, of roughly parallel distinctiveness, treated on preceding pages.

(1) Acrasids. Cellular slime molds. Uni- nucleate amoebae (with lobopodia) aggregating to form pseudoplasmodium that gives rise to so,ailed fruiting body lacking a tubed stalk.

(2) Eumycetozoa. True slime molds (and some other forms), some several feet in length. Amoeboid stage (with filopodia) giving rise to multicellular pseudoplasmodium with multispored fruiting body on tubed stalk. In some subtaxa, organisms biflageftate (no mastigonemes) at unicellular stage. Many species, belonging to the class Myxogastria (= Myxornycetes), have multinucleate syncytial (coenocytic) plasmodia.

(3) Labyrinthulids. Net slime molds. Curious forms, parasitic on aquatic plants (e.g., eel-grass) and marine algae; numerous specialized characters, including organelles called bothrosomes that produce the "slime-ways". Zoospores biflagellate. Group includes the thraustochytrids, separated out by some workers.

(4) Plasmodiophorids. Endoparasitic slime molds. Minute multinucleate plasmodia develop in cells and tissues of land plants (e.g., in roots of cabbage) following invasion by biflagellate zoospores that become uni- nucleate "myxamoebae" that, in turn, become the plasmodia (which in due time produce the infective spores that start the cycle again).

Sexuality has been noted in scattered species from all taxa listed above except the acrasids. Much more research with modern techniques needs to be carried out on these protozofungal forms of such potential importance in protist phylogeny. Olive's (1975) review is the latest comprehensive report on the "phyla" listed above.

V. Fungal Group

I am aware of the continuing dispute over the place of the fungi sensu lato which respect to kingdoms of the Superkingdom EUKA- RYOTA: apparently arguments can be enlisted in support of all four options. They may be considered "plants", "fungi", or "protists" ("protoctists"), or split between Fungi sensu stricto and Protista sensu lato (as I am doing, with little explanation, here). Further comparative studies should help resolve the vexatious problem. Unicellular, some flagellated, or simple mycelial stages seem to predominate in the life cycles of the three taxa (deserving to be ranked as separate phyla?) listed below; mycologists separate the first (considered more highly evolved) from the other two at a high taxonomic level.

(1) Chytrids. Mostly aquatic, some parasitic, microscopic in size. Zoospores (piano- gametes) typified by possession of single posteriorly located smooth flagellum. No cellulose in cell walls; mitochondrial cristae flattened.

(2) Hyphochytrids. Aquatic, some parasitic; motility by anteriorly located flagellum bearing mastigonemes. Cellulose in cell walls; mitochondrial cristae tubular.

(3) Oomycetes. Major group of water molds; some parasitic, a few also in soft; zoospores biflagellate, with anteriorly located flagellum with mastigonemes and posterior one smooth. Most species produce multinucleate syncytial mycelia. Cellulose in cell walls; mitochondrial cristae tubular.

The phyla that I assign to the kingdom Fungi proper [not treated here] are flagella- less (amastigote), often macroscopic with septate mycelia, exhibit dikaryosis, and manifest other special characteristics.

5. Discussion and concluding thoughts

My deliberate arrangement of protist phyla

into five sometimes admittedly unnatural and polyphyletic groupings, done primarily to preserve a kind of historical approach while stzessing the breadth and diversity encom- passed by the kingdom Protiata sensu lato, does allow me to return to the major question used as the title of this paper.

Even for the taxonomic~lassification query, it is not enough to reply simply that protozoa (with a small "p") are microorganisms assignable here and there within the larger protist taxon. Rather, how are the phyla containing them related to other protist phyla? Unfortu- nately, there are at least two or three problems associated with identifying and interrelating "protozoan" phyla -- better, phyla containing (at least some) protozoa -- as is evident in the composition of the Groups described on preceding pages. These new questions deserve brief discussion.

(1) What, exactly, constitutes a protozoan phylum? There is no exact reply! I suggest that the 10 taTa listed under my section labeled Protozoan Group would qualify without much debate, except for the myxosporidians. Yet some workers would say that the list is too long; others, that it is too short. But the 11 subsections of the Protozoaigal Group, plus the four of the Protozofungal Group, ought to be counted, too: at least, this would be the feeling of many protozoologists. A lot of discussion would be needed to bring about a meeting of the minds in most of those cases; on the other hand, my proposal that both adjectives be allowed or allowable as modi- tiers of these phyla or divisions -- that is, protozoan and/or algal -- might be acceptable. (But doesn~ the adjective "protiat" represent the best solution of all?) The recent Levine Report (Levine et al., 1980) lists seven phyla - - recall that Kudo (1966), a most authoritative textbook for years, had only one -- for the traditionally accepted high.level groups of protozoan species; in the present paper the number runs from 10 to 25. Even for t i~ same general groups (Levine's and mine), a couple are quite different; and the

4 5 5

characterizations will differ considerably in several cases (e.g., recall my dropping the clsmes of "phytoflagellates" and "zooflagel. lates" per se). One can thus appreciate the real dffficul~y of recognizing a formal supra. category (under kingdom Protista) for such a dispersed assemblage of diverse species that we are in the habit of calling " the protozoa".

(2) What are the closest neighbors of such "protozoan" phyla? With which other protist groups do they show the greatest evolutionary affinities? These questions are even more difficult to answer. Depending on the particular phylum under study, the nearest neighbor phylogenetically may be anywhere else in the whole kingdom! Some of the "first 10" referred to above may be closer to phyla in other Groups than they are to each other (e.g., rhizopodians closer to the protozofungal acrasids than to ciliates). And certainly some members of the "other 11 + 4" are much more likely closer to phyla in Groups HI or V than they are to each other (e.g., the phytomonads much nearer evolutionarily to the algal chlorophytes than to their fellow protozoalgal chrysomonads). In a work in press on 8tephanopogon, euglenid flagellate formerly ch~if ied as a gymnostome ciliate, in which Ms. Lipscomb and I have compared numerous protist taxa using over 100 characters, we have found many other examples of the "mismatching" illustrated above (Corlis8 and Lipscomb, 1982). This does not mean that my five proclaimed non- taxonomic Groups are '°oad" per se; it does emphasize the genuine difficulty (= impossi- bility!) of trying to label phyla as "purely protozoan" or "purely algal". They are, as stated some pages earlier, inextricably co- m led.

(3) Which came first, protozoan or algal phyla? Again, not important; it doesn't matter. Whether the "eoprot is t" was photosynthetic or phagotrophic, however, may be significant (I favor the latter hypothesis myself). In either case, the organism itself can be called an alga or a protozoon; it

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should be classified simply as an early protist. / f (note the italics please) it is reasonable

to divide the Protista into about three dozen constituent phyla, as supported in this paper, then - - by the arrangements I have sugges- ted -- from one-third to two-thirds to th ree fourths of the phyla might be considered protozoan in the broadest sense, with from one-fifth to one-half algal and from one-tenth to one-fifth fungal. As a protozoologist, I guess I've shown my bias by having the figures "come out" that way; as a protistologist, I prefer that the phyla involved be called simply 100% protist, and let it go at that.

A d d e n d u m

Comments received from a respected and perceptive reviewer after my manuscript had been accepted for publication deserve con- sideration, so I have requested permission from the Editor to add a page or two, preceding the bibliography, to make proper response. Essentially asked for was further clarification of my objectives and of my concluding recommendations. I am happy to reply here, since the extensiveness called for by the reviewer would require considerable expansion or redrafting of scattered parts of my paper as originally presented on the preceding pages; however, nothing said below contradicts any statements made in earlier sections.

Objectives

The underlying aims of my paper - -which may be thought of as an overview presented by a generalist in protistology -- have covered a rather broad range of topics. Incompletely expressed before, perhaps, they may be listed briefly here as follows:

(1) To call to the attention of protozoologists that the protozoa have evolutionarily close relatives among other unicellular groups of organisms and that these should no longer

be as neglected as they have been in the past, especially in light of present-day k n o w l e d g e that some such relatives have closer affimties to certain protozoan groups than some of the conventional protozoan taxa do to each other. Protozoa are simply (some of the) members of the kingdom Protista (see below).

(2) To similarly remind phycologists and mycologists that some algae and "lower fungi" are also inseparable from certain groups traditionally put aside as being solely protozoan.

(3) To urge a "new look" at the putative kingdom Protista and to accept it more or less as delimited and characterized in this paper, recognizing it as the most appropriate single highest-level taxon to include the diverse and numerous phyla of (mainly) unicellular and microscopic eukaryotic organisms. It may also be recognized as the group containing the ancestors of the three multicellular and more highly organized eukaryotic kingdoms, the Plantae, Fungi, and Animalia.

(4) To group what I identify as protist phyla into five "packages" (named for historical associations admittedly not entirely natural in their composition) that deliberately emphasize certain intermixed relationships and unabashedly indicate the inadvisability of accepting such groupings as formally repre- senting natural taxonomic units at any supraphyletic level.

(5) To point out several ways by which my five sometimes polyphyletic groupings (called Groups with a capital "G") could be better "naturalized", while nevertheless simultane- ously insisting that their persisting "defects" render them forever inappropriate as formal taxonomic units. In short, their very weaknes- ses strongly support my central theme that it is preferable to recognize a single unifying taxon into which many phyla, interrelated to various and varying degrees, can safely be assigned rather than to endorse separate polyphyletic high-level groups. This taxon is the kingdom Protista, as I have redefined it. I hope, then, to show that the three dozen or so phyla united under it by me should

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not -- at the present state of our knowledge -- be grouped into distinct subkingdoms or superphyla with formal taxonomic names, unique diagnoses, etc.

Conclusions

My concluding recommendations, not detailed in the original manuscript in order to conserve space, may be considered as follows:

(1) Drop the word "Protozoa" (with a capital "P") as a formal group.name and category at any taxonomic level (phylum, superphylum; subkingdom, etc.). Retain in the vernacular form the words "protozoon" and "protozoa" (with a small "p"), the adjective "protozoan", the science of "protozoology" and its pmctioners, the "protozoologists", etc. All such useful terms are accurate enough and will continue to possess a high value didactically. But protozoan and quasi-protozoan groups themselves are simply too diverse and too polyphyletic to (continue to) be lumped together under the single formal heading of '~Protozoa".

(2) Drop, for similar reasons, such names as "Algae" and "Lower Fungi", while retain- ing the very handy vernacular forms (e.g.,

(3) Use "phytoflagellate" and "zooflegel- late", formally or informally, with caution, since they are traditional terms of rather misleading connotation today. For example, species of the curious Stephanopogon, not to mention those of the trypanosomatids, appear to be quite closely related to euglenids, yet phycologists would likely be loath to call them "phytoflagellates" since they are not "plant-like" (in the sense of possessing chlorophyll), are not biflagellate, etc.

(4) Accept the unifying "Protista" at the kingdom level and consider it to contain some three doZen phyla (mainly of unicellular and microscopic forms, pigmented and non- pigmented) that may -- for the principal purpose of convenient discussion -- be packaged into these five informal Groups of

protists: I, the Protozoan; II, the Protozoalgal; III, the Algal; IV, the Protozofungal; and V, the Fungal. [My Group I organisms are generally studied by protozoologists; III, by phycologists; and V, by mycologists. Histori- cally, as my choice of names concisely indicates, Group II has been studied and claimed by both protozoologists and phycologists; and Group IV, similarly, by protozoologists and mycologists. But such facts are of no help at all in determining natural phylogenetic groupings among the numerous protist phyla involved.]

(5) Recognize that these sometimes polyphyletic Groups cannot be fully "naturalized" or it then wou/d be possible to give them formal taxonomic status with formal names, etc. Some phyla within each of them are more closely related phylogenetically to certain phyla in other Groups than to ones within their own, underlining my persistent thesis that the protists overall represent a collection of inextricably intertwined lower-level groups than can best be united only at the kingdom level. Nevertheless, some obvious inconsisten- cies or deficiencies within or among my five more or less classical "historical associations" should perhaps be corrected or at least dearly identified in order to give the Groups, informal though they be, an improved degree of "naturalness" and internal consistency. At the same time, we should maintain our awareness that they simply cannot ever be rendered monophyletic for reasons given throughout my paper. Such problems were given little direct attention on earlier pages.

(a) For example, in the Protozoan Group (my Group I), some workers would eject the myxosporidians (the "Myxozoa")outright. In fact, these strange forms are no longer considered even as protists by some investigators who have studied them (one claim is that they are degenerate cnidarlans). Also, the rhizopodians of my list are very likely closer evolutionarily to some members of my Protozofungal Group (IV) than they are to some other phyla within Group I. Recall, too, that I have already removed the con-

458

ventional "lower zooflagellates" (see main text of this paper) to a position within the phylum of euglenids (Group II). This reassign- ment is likely to cause considerable consterna- tion, evidence notwithstanding, among zoological/parasitological workers on the trypanosonmtids, for example, as well among many phycologicai botanists.

(b) My Protozoalgal Group (II) itself contains three rather disparate groups, viz., five phyla that are clearly assignable to the aigologists' "Chlorophyte Series" (although the choanoflageUates present some problems); five others, identifiable with the "Chromo- phyte Series" (which, like its counterpart, also contains other phyla or divisions from my Group III, especially); and the dinoflagellates, showing affinities with chromophytes but unique in numerous ways. Both phycologists and protozoologists may object to my placing some non-pigmented "lower zooflsgel- lates" in with the euglenids, as already mentioned above, but such a transfer is long overdue (and I am not the first to propose it). The phytomonads or volvocids should be removed from my Group II to Group III, if we are to properly preserve the integrity of the chlorophytes sensu stricto: this serves as still one more crystal-clear example of the futility (and thus the inadvisability) of trying to separate "algae" and "protozoa" by a formidable taxonomic barrier!

Practically all members of this Group II could be moved, en bloc, into my Group I, as many protozoologists have in fact done (though with great and iU-advised reduction of their rank). But, by the same token, they could be comfortably placed with my Group III, as phycologists have traditionally done. Both are "natural" moves. Is this, then an irresolvable dilemma? Only if one insists on separate highest-level taxonomic hierarchies for algae and protozoa (which I don ' t , of course).

(c) The phyla of my Algal Group (III) are certainly not all equally close to one another phylogenetically. And some workers would, today, not hesitate to throw the controversial

red and brown algae entirely out of the kingdom Protista. Others would consider the green algae as plants rather than protists. I retain those three important groups in the first o f the eukaryotic kingdoms, but admittedly as atypical forms.

(d) Members of my Protozofungal Group (IV), the slime molds sensu lato, are simul- taneously claimed by both protozoologists and mycologists, often with little appreciation or even knowledge of each other's views. Recognizing them as phyla of protists, only, seems to be a compromiae of sound value. Their closest relatives, in my opinion, are among other phyla within the Protista, not among the group of true ("higher") Fungi.

(e) The three taxa of my Fungal Group (V, last on my list of Groups) have never been claimed by protozoologists. Their affinities seem to rest largely with the Fungi, as long claimed. The chytrids, however, share a few important characteristics with "algae" of the Chromophyte Series (e.g., phyla 6--10 of my Group II), although they have flattened mitochondrial cristae. There is support for considering these Fungal Group forms as "good" protists, though not necessarily very close evolutionarily to one another. It is particularly true that members of this Group have too often been neglected by microbiolo- gists and general protistologists, let alone protozoologists.

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What are the taxonomic and evolutionary relationships of the protozoa to the protista?