sign in sign up
<<
Home , Biliphyta, Chromista

A By Default?

WILL H. BLACKWELL MARTHAJ. POWELL

Those Many Kingdoms A Thumbnail on Protozoology Downloaded from http://online.ucpress.edu/abt/article-pdf/63/7/483/50291/4451168.pdf by guest on 02 October 2021

A good start to a revaluationof the is a hanges in concepts of kingdoms of brief look at some main events in the history of study organisms over the latter 20th century of the group, especially in North America. We can have been substantial (Blackwell & Powell here venture the bottom line first. If we span the 1999), sometimes tedious, yet with the worthy goal course of protozoology during the 20th century, we of establishing groupings of organisms reflective of eventually arrive at two apparently contradictory major evolutionarylineages. An increasing number of conclusions: (1) the classification of no group we kingdoms is recognized, typically including two have recognized as a , subkingdom or king- prokaryotic kingdoms, Archaea(Archaebacteria) and dom has changed more, (2) nor has the classification Bacteria(Woese et al. 1990), and six or more eukary- of any group ultimately come more full-circle. otic kingdoms: Protozoa (the amitochondrial mem- Perhaps these seemingly disparate points will be bers sometimes separated as kingdom Archezoa), clear by the end of our discussion. Chromista (including the major group, ), Biliphyta, Plantae, Fungi, and The first major textbook on protozoology in the Animalia (cf. Cavalier-Smith 1987; Corliss 1994; United States, The Protozoa, by Gary N. Calkins Blackwell& Powell 1995). Still more kingdoms have (1901) of Columbia University, probably had more been suggested; Leedale (1974), for example, out- impact in this field of study than any other single lined as many as 19 kingdoms among scenarios he work. Seemingly heedless of the three-kingdom discussed. approach of Haeckel (1866), who proposed a unicel- lular kingdom, Protista, Calkins (1901) followed the Difficulty is encountered in seeking an exclusive Linnaeanview of as divisible along and ani- definition of several of these kingdoms. In particular, mal lines. He recognized the phylum Protozoa as an the Protozoa is loosely characterized;its membership apparently definable group, i.e. unicellular organ- is decided partially by the fact of not belonging to isms, within the otherwise multicellular kingdom another kingdom (Cox 1991; Cavalier-Smith1993). Animalia. But since Protozoa are, in a selection of recent litera- ture, referred to as a kingdom (e.g. Cavalier-Smith Calkins'system of four fundamentalclasses with- 1993; Blackwell& Powell 1995; Beakes 1998; Corliss in the phylum Protozoa-Mastigophora (flagellates), 1994, 1998; Vickerman 1998), it is of possible bene- Sarcodina (amoebae), Infusoria (), and fit to teachers of biology to reassess the characteriza- Sporozoa (gregarines,coccidea)-remains influential tion, confines and membership of this potential king- (a basis for our proposition of the "full-circle"arrival dom of organisms. of knowledge in protozoology). With minor changes, Calkins' system was echoed in works on Protozoa (and in the "protozoan section" in general works of zoology) through the first half of the 20th century. WILLH. BLACKWELLis an AdjunctProfessor and MARTHAAJ.POWELL For example, R. P. Hall (1953), of New York is Professorand Chair of the Departmentof BiologicalSciences at University,produced an excellent survey of Protozoa, the Universityof Alabama, Tuscaloosa,AL 35487-0344. titled "Protozoology";Hall employed the traditional,

THEPROTOZOA, AKINGDOM BYDEFAULT? 483 locomotion-based,light microscopic charactersof some authors (e.g. Levine et al. 1980), but not others Protozoaestablished by Calkins,adding additional (e.g. Jahn et al. 1979). In more recent classifications informationgained during the 50 years following (e.g. Cox 1991; Sleigh 1991), formal headings for Calkins'original text (1901). For reference,we pres- major protozoan groups were often dropped. ent the outlineof Hall'ssystem (Table 1), representa- tiveof mid-century,traditional protozoological classi- Recognition of the Protista; fication.But, changes were in the offing.Questioning the ultimate divisibilityof amoeboid and flagellate Obscuring of the Protozoa protozoans,Honigberg et al. (1964) combinedthese as "Sarcomastigophora'-amodification followed by Having seemingly forgotten, for a hundred years, Haeckel's (1866) proposal for a king- dom Protista,realization reoccurred that a number of unicellular organisms, e.g. TABLE 1. Euglena, , chrysamoebas, Groups of Protozoa, Hall 1953._ , are not readily fitted into

plant and animal kingdoms. As a conse- Downloaded from http://online.ucpress.edu/abt/article-pdf/63/7/483/50291/4451168.pdf by guest on 02 October 2021 Subphylum1.Mastigophora Subclass3.Haemosporidia quence, the kingdom Protista was again Class1. Phytomastigophorea Class2. Cnidosporidea invoked (e.g. Whittaker 1969). With this "rebirth"of Protista came a similar Order1.Chrysomonadida Order1.Myxosporida realizationthat fungal organisms are nei- Order2.Heterochlorida Order2.Actinomyxida ther plant nor animal, and the kingdom Order3.Cryptomonadida Order3.Microsporida Fungi was also established. Whittaker's Order4.Dinoflagellida Order4.Helicosporida five-kingdomproposal - (bacte- OrderS.Phytomonadida Class3. Acnidosporidea ria, prokaryotes), Protista (unicellular Order6.Euglenida Subclass1.Sarcosporidia ), Plantae, Animalia and Fungi - pervaded texts of biology for Order7.Chloromonadida Subclass2.Haplosporidia two decades, and is still occasionally Class2. Zoomastigophorea Subphylum4.Ciliophora advocated. Whittaker (1969), and later Order1.Rhizomastigida Class1. Ciliatea Margulis(1974, 1981), who preferenced Order2.Protomastigida Subclass1.Protociliatia the name Protoctista over Protista, are Order3.Polymastigida Order1.Opalinida associated with the development of the Order4.Trichomonadida Subclass2.Euciliatia five-kingdomconcept; however, the core of this proposal (and a suggested addi- Order5.Hypermastigida Order1.Holotrichida tional kingdom for viruses) appeared in Subphylum2.Sarcodina Suborder1.Astomina Jahn and Jahn's (1949) "How to Know Class1. Actinopodea Suborder2.Gymnostomina the Protozoa." Order1.Helioflagellida Suborder3.Trichostomina What did establishment of the Order2.Heliozoida Suborder4.Hymenostomina five-kingdom system mean to the recog- Order3.Radiolarida Suborder5.Thigmotrichina nition and classification of Protozoa?At Class2. Rhizopodea Suborder6.Apostomina first it simply implied a transfer of the Order1.Proteomyxida Order2.Spirotrichida unicellular phylum (or subkingdom) Protozoa from the multicellular king- Order2.Mycetozoida Suborder1.Heterotrichina dom, Animalia, to the unicellular-based Order3.Amoebida Suborder2.Tintinnina kingdom Protista (e.g. Jahn et al. 1979). Order4.Testacida Suborder3.Oligotrichina However, delimitation of Protozoa soon Order5.Foraminiferida Suborder4. Entodiniomorphina blurred amid the taxonomic melange of Subphylum3.Sporozoa Suborder5.Hypotrichina the inflated kingdom Protista. John Corliss' (1981) paper, "Whatare the tax- Suborder6.Ctenostomina Class1.Telosporidea onomic and evolutionary relationships Order3.Peritrichida Subclass1.Gregarinidia of the Protozoa to the Protista?,"went to Order1.Eugregarinida Order4.Chonotrichida the heart of this issue. This question of Order2.Schizogregarinida Class 2. Suctorea protozoan, and other group, Subclass2.Coccidia identities was again voiced by Corliss

484 THEAMERICAN BIOLOGY TEACHER, VOLUME 63, NO.7,SEPTEMBER 2001 (1983) in a paper titled, perhaps tongue-in-cheek,"A nonetheless continue to be recognized in some Puddle of ." recent biology texts (e.g. Johnson 2000).

Corliss raised a two-partedissue: Purging the Protista; 1. The kingdom Protistawas too large, too inclu- sive, too polyphyletic (a largely unnatural Reemergence of the Protozoa 45 phyla assemblage). Corliss (1984) listed The solution to an identity dilemma (i.e. what under Protista, with more to come. The "uni- does/does not constitute Protista?)lies in acquisition in Protista cellular criterion"for "membership" of knowledge. An advance was Cavalier-Smith's was compromised by inclusion of predomi- (1986, 1989) recognition of the kingdom Chromista. brown nantly multicellular groups, such as The largest assemblage within the Chromista is phy- (Phaeophyta) and lum Heterokonta,a name referringto unequal flagel- (Rhodophyta). la of many of its members; the more forwardof these 2. Distinctions of formal, major taxonomic flagella generally bears tubular (2- or, more often, mastigonemes (flagellarhairs). In reference groups within the Protistawere vanishing. 3-parted) Downloaded from http://online.ucpress.edu/abt/article-pdf/63/7/483/50291/4451168.pdf by guest on 02 October 2021 to these mastigonemes, Patterson (1989) gave this Given this breakdown of protistan macrosystem- natural assemblage the appropriate,but atic infrastructure, Corliss (1981) recognized five informal, name Stramenopiles ("straw hairs"). informalgroupings of protist phyla:(1) the protozoan Stramenopila, more monophyletic than Chromista, group;(2) the protozoalgalgroup; (3) the algal group; has been suggested as a candidate kingdom (e.g. (4) the protozofungalgroup; and (5) the fungalgroup, Campbell et al. 1999). for "fungalprotists," not for the kingdom Fungi. Photosynthetic Stramenopiles typicallypossess a The Protistabecame an unwieldy colossus, hous- " endoplasmic reticulum" (cf. Cavalier- ing both related and unrelated "protists" (Corliss Smith 1986) of two extra membranes around the 1984). Among a number of groups shoe-horned into chloroplast. The outer membrane usually has conti- Protista were alleged "fungal protists" such as nuity with the nuclear envelope. These additional Chytridiomycetes (related to true Fungi; cf. Powell membranes provide evidence of a former (probably 1993); Mycetozoa or "Myxomycetes"(slime molds), /eukaryote) endosymbiosis, demarcating which belong generally with amoeboid protozoa the chromophytous algal lineage (cf. Blackwell & (Olive 1975); and Plasmodiophoromycetes ("endo- Powell 1995). parasitic slime molds"), which are "amoebo-flagel- late" protozoa (Beakes 1998). Still more problemati- Recognition of a chromistan complex allowed cal, as stated by Corliss (1983), is that "Protozoaand group realignments.Chromophyte "algae," e.g. chrys- Algae are so inextricably intermixed and commin- ophytes (golden algae), xanthophytes (yellow-green gled, we must find new ways of grouping them."The algae, heterochlorids), raphidophytes (chloromon- problem of delineating algae and protozoa is not ads), and phaeophytes (), could be new. Botanists (cf. Bold & Wynne 1978) traditional- removed from Protista, and placed in the Chromista ly laid claim to certain "protozoan"groups, particu- (more specificallyin Stramenopila).Related fungal or larly those of the Class Phytomastigophorea (see protozofungal groups, such as and Table 1). The grouping "algae"includes organisms Hyphochytrids (together, the ""), are from differentkingdoms (e.g. , and "blue- also placed with Stramenopiles,as are protozoan-like green algae" or cyanobacteria),and is not a tenable Bicosoecids and Labyrinthulids.Accurate taxonomic systematic category (Blackwell& Powell 1995). If we referralof a significant segment (chromistans) of the attempt to use Corliss' informal groups of Protista, unnatural Protistacould thus be accomplished. we deal with the problem of which Orders of Phytomastigophorea(or more explicitly, members of A review of kingdom placement of other algal or & these orders) are more protozoan, protozoalgal, or protozoalgal groups (Blackwell Powell 1995, algal? Consider Euglena and its "colorless counter- 1999) revealed relationships of (1) dinoflagellates part" Astasia (Bold & Wynne 1978). Does one and ciliated protozoa; (2) euglenoids and trypanoso- belong in the algal or protozoalgal group, and the mal protozoa;and, possibly of (3) cryptomonads (i.e. other in the protozoan group? A number of such the host cell) to "retortamonad-like, pro- cases call forjudgments too subjective to permit con- tozoa" (Cavalier-Smith1989). In reference to Hall sensus. Informal "corlissean"categories of Protista (1953), Table 1, we note that phytomastigophorean

THEPROTOZOA, AKINGDOM BYDEFAULT? 485 Orders are accounted for (either as Stramenopiles,or tory heading should be provided for their referral. as Protozoa), save Phytomonadida (including Though perhaps a kingdom only shakily,perhaps by Chlamydomonasand Volvox); such "phytomonads" default, referral as the kingdom Protozoa seems are green algae, and are in the kingdom Plantae or presently the best option available. It is interesting (cf. Blackwell & Powell 1995). Red that Cox (1991) and Sleigh (1991), though informal- algae (Rhodophyta) are removed from Protista,either ly, not only used the name Protozoa, but employed to kingdom Plantae or Biliphyta (cf. Cavalier-Smith Calkins' (1901) basic categories - flagellates, amoe- 1987; Corliss 1994; Blackwell & Powell 1995):. boid forms, ciliates, and sporozoa. Better understanding of the "biology"of critical If we cannot sharply define Protozoa,we may still groups (e.g. chrysomonads, dinoflagellates, eugle- discuss their attributes. Protozoa typically carry out noids) gained during the 1980s and early 1990s led their life cycles at a one-celled level of organization; to: dispensing with the unnatural kingdom Protista; though sometimes colonial, e.g. vorticellid ciliates, taxonomic group refinements (e.g. Stramenopila); they do not exhibit the tissue-level multicellularityof and placement of certain taxonomically troublesome higher animals and . Historical arguments that

groups, e.g. "phytomonads," in appropriate king- protozoans are acellular or, conversely, multicellular, Downloaded from http://online.ucpress.edu/abt/article-pdf/63/7/483/50291/4451168.pdf by guest on 02 October 2021 doms. An improved understanding of group relation- have not been sustained (Corliss 1989; Sleigh 1991). ships/delineations has been accompanied by an Protozoa are fundamentally unicellular eukaryotes increase in the number of kingdoms recognized. For (Vickerman 1998). However, since some Protozoa example, we presently not only recognize kingdom effect complicated life cycles, but at a one-celled level, Chromista (or Stramenopila), but Protozoa have protozoan cells can be- large (Corliss 1991), and reemerged from the relative obscurity of Protista and among the most complex of cells (Sleigh 1991). are now often referred to as a kingdom - yet, Protozoa is a kingdom very difficult to define. Unicellularity, however, is not restricted to Protozoa - occurring also in Stramenopiles, Fungi and Viridiplantae.The putative "Archezoa"excepted Attempting To Define Protozoa (cf. Brugerolle 1991; Corliss 1994; Vickerman 1998), most Protozoa possess mitochondria;and most pro- It might be argued that, if we recognize Protozoa tozoan mitochondrialcristae (save the discoid cristae as a kingdom, we should be able to define or precise- found in "")are of tubular shape (Corliss ly describe this kingdom, or, restated, determine 1998; Scheffler 1999). Tubularmitochondrial cristae what is requisite to membership in this kingdom. In generally distinguish Protozoa from animals, plants the case of Protozoa, however, the of is goal defining and fungi, but not from Stramenopiles.Protozoa were only partly attainable (cf. Lee et al. 1985). Difficulty probably primitively phagotrophic and lacked plas- of definition relates to the fact that Protozoa are tids (Vickerman 1998). However, Protozoa are not "diverse organisms with mor- divergent life-styles, universally phagotrophic (parasitic Protozoa are phologies, habits, and reproductive cycles" often osmotrophic), and phagotrophy also occurs in (Lipscomb 1991). They are not the coherent phylo- primitive Stramenopiles. Certain Protozoa acquired genetic group that certain other or kingdoms candi- secondarily (by endosymbiosis), e.g. dinofla- date kingdoms apparentlyare, e.g. We Stramenopila. gellates and most euglenoids. Protozoa lack collagen may not just look at one character as the mul- (such and chitin, tissues or substances characteristic of tiparted, tubular flagellarhairs of Stramenopila) and Metazoa; but, these "negative" (absent) traits of decide membership in Protozoa. Protozoa are "shared"by Metaphyta. Protozoa typi- Protozoa are defined in part by "negative"charac- cally do not produce starch or cellulose (dinoflagel- teristics (cf. Cavalier-Smith1993) - that is, they do lates providing an exception); but, neither do not have "this or that"character, which (if possessed) Metazoa nor true Fungi. would project a member of the Protozoa into some We could further belabor this list, but it is per- other kingdom. The elusiveness of a precise, positive haps obvious that, while Protozoa have a number of definition for Protozoa indicates that are still not they positive and negative features in common, no single a group - monophyletic a topic which will surely featureprovides distinction from all other kingdoms. receive further attention. However, as Cox (1991) Only through a combination of characters may a pointed out, this large assemblage of protozoal organ- meaningful picture of the Protozoa emerge (cf. isms, significant to human and animal health, should Corliss 1991). The general belief that the number of not be left as taxonomic "orphans."Some classifica- characters required for distinction decreases as we

486 THEAMERICAN BIOLOGY TEACHER, VOLUME 63,NO. 7, SEPTEMBER 2001 proceed to higher taxonomic categories (cf. Corliss Insights have been gained into relationships of 1984) seems contradicted by kingdom Protozoa.The Protozoa to other kingdoms. A molecular similarity difficulty of delimiting Protozoa reminds us of Hall's has been established between Protozoa and (1953) deceptively clever remark, that "Protozoa Stramenopiles(Bhattacharya & Medlin 1995; Van de include a variety of microorganismswhich, by gener- Peer & De Wachter 1997). In corroboration,residual al agreement of protozoologists, are currently plastids in the malarial parasite (, assigned to the phylum." Our ability to define ), and in nonmalarial apicomplexans Protozoa is not greatly improved today. (Toxoplasma),suggest a relationship to plastids and/or plastids of stramenopilous chromis- Advances in Understanding tans (cf. Blanchard & Hicks 1999; Cavalier-Smith 1999). Actinophryid heliozoan protozoa have been Protozoa: Relationships, postulated to have chromistan connections Connections to Other Kingdoms (Patterson 1986), as have Opalinid protozoa (Delviquier & Patterson 1993). Molecular data relate Advancesin knowledgeof ultrastructureduring the protozoans to Sponges, thus to

1970s and 1980s, and in molecular biology in the Animalia(Zrzavy et al. 1998). Interestingly,molecular Downloaded from http://online.ucpress.edu/abt/article-pdf/63/7/483/50291/4451168.pdf by guest on 02 October 2021 1990s, enhanced understandingof relationshipswithin sequencing also supports a relationship of Protozoa. Trichomonadsand Hypermastigidsbecame and Fungi (Vickerman 1998). grouped as the Parabasalia,based on golgi-like struc- Small subunit rRNA studies suggest that tures (parabasalbodies) flanking the axostyle (micro- Microsporidia(small parasiticprotozoa with unusual tubular supporting rod), cf. Levine et al. (1980). "pole filaments") are allied to Fungi (Weiss et al. Bodonids and Trypanosomes were included in the 1999); Myxozoa (also parasitic) appear more related Kinetoplastida(characterized by a large anterior mitochondrion/nucleoid com- plex, the "kinetoplast,"associated with flagellarbases); Euglenoids were found TABLE 2. to be related to the Kinetoplastida,and Listof protozoan groups now recognized. united by some in the "Euglenozoa"(cf. Cavalier-Smith 1981; Sleigh 1989). Mastigophora Sarcodina Caryoblasteans(cf. Margulis& Schwartz Choanoflagellates Rhizopoda 1988; Hausmann & Hulsmann 1996), Cercomonads LoboseAmoebae including flagellated forms (e.g. Mastigella) and large, multinucleated Retortamonads FiloseAmoebae amoeboid forms (e.g. Pelomyxa),were Pyrsonymphids GranuloreticuloseAmoebae grouped, based on their lack of mito- Parabasalia (IncludingForaminiferans) chondria and of golgi apparatus. The Trichomonads Acarpomyxeans Apicomplexa became recognized as an Hypermastigids Mycetozoa(sensu lato) assemblage of "sporozoan"groups: gre- Oxymonads garines, coccidia, hematozoa (including Diplomonads Plasmodiophorids piroplasms), and perhaps Perkinsus(cf. Corliss 1991).Apicomplexans are related Euglenozoa Actinopoda by special organelles (the "apicalcom- Euglenoids Acanthareans plex") in the cell's anterior (Lee et al. Kinetoplastida Radiolarians 1985; Barnes 1998). The Apicomplexa Bodonids Heliozoans were subsequentlydetermined to be part Trypanosomatids AlveolateProtozoa of a largergrouping, Alveolate Protozoa Hemimastigophorans Ciliophora (Cavalier-Smith 1993; Hausmann & Hulsmann 1996). - including Pseudociliates Ciliates Apicomplexa, Dinoflagellates and Prymnesiomonads() Suctorians Ciliates - are taxonomically connected Cryptomonads Dinoflagellates by "alveoli"(flattened vesicles under the Proteromonads Apicomplexa(Sporozoa) plasma membrane).Molecular phyloge- Opalinids Microspora(Microsporidia) nies support Alveolate relationships Caryoblasteans Myxozoa(sensu lato) (Philippe& Adoutte 1998).

THEPROTOZOA, A KINGDOM BYDEFAULT? 487 to metazoan animals (Anderson 1998). SSU rRNA Blanchard,J.L. & Hicks,J.S. (1999). The non-photosynthet- sequences point to a grouping of Biliphyta (glauco- ic in malarialparasites and other apicomplexans phytes, red algae) with Cryptomonads (Van de Peer is derivedfrom outside the green plastid lineage.Journal & De Wachter 1997). Nakayama et al. (1998) pro- of EukaryoticMicrobiology, 46, 367-375. vided molecular evidence that primitive flagellates Bold, H.C. & Wynne, Mj. (1978). Introductionto the Algae: (protozoans) occurred in the ancestry of Structure and Reproduction.Englewood Cliffs, NJ: (green algae). Prentice-Hall. Protozoa are connected phylogeneticallyto other Brugerolle,G. (1991). Flagellarand cytoskeletalsystems in eukaryote kingdoms. Other eukaryotickingdoms are amitochondrialflagellates: Archamoeba, Metamonada, probably derived with respect to Protozoa and Parabasala.Protoplasma, 164, 70-90. (Vickerman 1998). The erstwhile megakingdom Calkins, G.N. (1901). The Protozoa.New York: Columbia Protista (Protoctista) occupied a systematic position Press/Macmillan. foundational to other eukaryote kingdoms (Margulis & Schwartz 1988). This basal position now defaults Campbell,N.A., Reece,J.B.& Mitchell,L.G. (1999). Biology, to the somewhat less heterogeneous kingdom, 5th ed. Menlo Park,CA: Addison Wesley Longman. Downloaded from http://online.ucpress.edu/abt/article-pdf/63/7/483/50291/4451168.pdf by guest on 02 October 2021 Protozoa - itself perhaps recognized by default. Cavalier-Smith,T. (1981). Eukaryote kingdoms: Seven or Protozoa is a useful category; no other taxonomic nine? BioSystems,14, 461-481. home now exists for unicellular eukaryotes not belonging to other kingdoms. Some Protozoa are Cavalier-Smith,T. (1986). The kingdom Chromista:Origin in related, but others are not. Though recognized as a and systematics. Progress PhycologicalResearch, 4, 309-347. kingdom, "Protozoa"is a taxonomic half-wayhouse, with some members destined for other taxonomic Cavalier-Smith,T. (1987). The origin of eukaryote and dwellings. We present, without indication of rank, archaebacterialcells. Annalsof the New YorkAcademy of organismalgroups belonging to the Protozoain Table Sciences,503, 17-54. 2. Traditional headings, Mastigophora (flagellated Cavalier-Smith,T. (1989). The kingdom Chromista.In J.C. protozoans) and Sarcodina (amoeboid protozoans), Greenet al. (Eds.), TheChromophyte Algae: Problems and are retained in this Table for convenience of reference. Perspectives(pp. 381-407). Oxford:Clarendon Press.

Cavalier-Smith,T. (1993). Kingdom Protozoa and its 18 phyla. MicrobiologicalReviews, 57, 953-994, References Cavalier-Smith,T. (1999). Principlesof protein and lipid tar- Anderson, C.L. (1998). Phylogenetic relationships of the geting in secondary :Euglenoid, dinofla- Myxozoa. In G.H. Coombs et al. (Eds.), Evolutionary gellate,and sporozoanplastid origins and the eukaryote RelationshipsAmong Protozoa (pp. 341-350). Dordrecht, family tree. Journal of Eukaryotic Microbiology,46, The Netherlands:Kluwer Academic Publishers. 347-366.

Barnes, R.S.K. (Ed.). (1998). The Diversity of Living Corliss,J.O. (1981). What are the taxonomic and evolution- Organisms.Oxford, UK: BlackwellScience. ary relationships of the Protozoa to the Protista? BioSystems,14, 445-459. Beakes,G.W. (1998). Relationshipsbetween lower fungi and protozoa. In G.H. Coombs et al. (Eds.), Evolutionary Corliss,J.O.(1983). A puddle of protists:There's more to life RelationshipsAmong Protozoa (pp. 351-373). Dordrecht, than animals and plants. The New YorkAcademy of The Netherlands:Kluwer Acaemic Publishers. Sciences,"The Sciences," 23(3), 34-39.

Bhattacharya,D. & Medlin, L. (1995). The phylogeny of Corliss,J.O. (1984). The kingdom Protistaand its 45 phyla. plastids: A review based on comparisons of small-sub- BioSystems,17, 87-126. unit ribosomalRNA coding regions.Journal of Phycology, Corliss, J.O. (1989). The protozoan and the cell: A brief 31, 489-498. twentieth-centuryoverview. Journal of the History of Blackwell,W.H. & Powell, Mj. (1995). Where have all the Biology,22, 307-323. algae gone, or, how many kingdoms are there? The Corliss, J.O. (1991). Introduction to the Protozoa. AmericanBiology Teacher, 57(3), 160-167. MicroscopicAnatomy of Invertebrates,1, 1-12. Blackwell, W.H. & Powell, (1999). Reconciling king- Mj. Corliss,J.O. (1994). The place of the protists in the micro- doms with codes of nomenclature: Is it necessary? bial world. U.S. Federationfor Culture Collections, SystematicBiology, 48(2), 406-412. Newsletter,24(3), 1-6.

488 THEAMERICAN BIOLOGY TEACHER, VOLUME 63,NO.7, SEPTEMBER 2001 Corliss,J.O. (1998). Classificationof protozoa and protists: revealed by analyses of nuclear-encoded SSU rRNA The current status. In G.H. Coombs et al. (Eds.), sequences. Protist,149, 367-380. EvolutionaryRelationships Among Protozoa (pp. 409- 447). Dordrecht, The Netherlands: Kluwer Academic Olive, L.S. (1975). The Mycetozoans.New York:Academic Publishers. Press.

Cox, F.E.G.(1991). Systematicsof parasiticprotozoa. InJ.P. Patterson, D.H. (1986). The actinophryid Kreier& J.R. Baker (Eds.), ParasiticProtozoa, 2nd ed., (Sarcodina, Actinopoda) as chromophytes. In J. Vol. 1 (pp. 55-80). San Diego:Academic Press. Kristiansen & R.A. Andersen (Eds.), Chrysophytes: Aspects and Problems (pp. 49-67). Cambridge: Delvinquier,B.LJ. & Patterson,DJ. (1993). The opalines. In CambridgeUniversity Press. J.P.Kreier &J.R. Baker(Eds.), ParasiticProtozoa, 2nd ed., Vol. 3 (pp. 247-325). San Diego:Academic Press. Patterson,D.H. (1989). Stramenopiles:Chromophytes from a protistan perspective. In J.C. Green et al. (Eds.), The Haeckel, E. (1866). GenerelleMorphologie der Organismen. ChromophyteAlgae: Problems and Perspectives(pp. 357- Berlin:G. Reimer. 379). Oxford:Clarendon Press.

Hall, R.P. (1953). Protozoology.Englewood Cliffs, NJ: Philippe,H. & Adoutte,A. (1998). The molecularphylogeny Downloaded from http://online.ucpress.edu/abt/article-pdf/63/7/483/50291/4451168.pdf by guest on 02 October 2021 Prentice-Hall. of Eukaryota:Solid facts and uncertainties. In G.H. Coombs et al. (Eds.), EvolutionaryRelationships Among Hausmann, K. & Hulsmann, N. (1996). Protozoology,2nd Protozoa (pp. 25-56). Dordrecht, The Netherlands: ed. Stuttgart:Georg Thieme Verlag. KluwerAcademic Publishers.

Honigberg,B.M. et al. (1964). A revised classificationof the Powell,Mj. (1993). Looking at mycology with a Janus face: phylum Protozoa.Journal of Protozoology,11, 7-20. A glimpse at Chytridiomycetesactive in the environ- ment. Mycologia,85, 1-20. Jahn, T.L. & Jahn, F.F. (1949). How to Know the Protozoa. Dubuque, IA:William C. Brown. Scheffler,I.E. (1999). Mitochondria.New York:Wiley-Liss.

Jahn, T.L.,Bovee, E.C. &Jahn, F.F.(1979). How to Knowthe Sleigh, M.A. (1989). Protozoaand other Protists.London: Protozoa,2nd ed. Dubuque, IA:William C. Brown. EdwardArnold.

Johnson, G.B. (2000). The Living World,2nd ed. Boston: Sleigh, M.A.(1991). The nature of protozoa.InJ.P. Kreier& McGrawHill. J.R. Baker(Eds.), ParasiticProtozoa, 2nd ed., Vol. 1 (pp. 1-53). San Diego:Academic Press. Lee, JJ., Hutner, S.H. & Bovee, E.C. (Eds.). (1985). An IllustratedGuide to theProtozoa. Lawrence, KS: Society of Van de Peer,Y. & De Wachter,R. (1997). Evolutionaryrela- Protozoologists. tionships among the eukaryoticcrown taxa taking into account site-to-siterate variation in 18S rRNA.Journal of Leedale, G.F.(1974). How many are the kingdoms of organ- MolecularEvolution, 45, 619-630. isms? Taxon,23(2/3), 261-270. Vickerman,K. (1998). Revolutionamong the protozoa. In Levine, N.D. et al. (1980). A newly revised classificationof G.H. Coombs et al. (Eds.), EvolutionaryRelationships the Protozoa.Journal of Protozoology,27, 37-58. AmongProtozoa (pp. 1-24). Dordrecht,The Netherlands: Lipscomb, D. (1991). Broad classification:The kingdoms KluwerAcademic Publishers. and the protozoa. In J.P. Kreier & J.R. Baker (Eds.), Weiss, L.M.,Edlind, T.D., Vossbrinck, C.R. & Hashimoto,T. ParasiticProtozoa, 2nd ed., Vol. 1 (pp. 81-136). San (1999). Microsporidianmolecular phylogeny:The fun- Diego:Academic Press. gal connection.Journal of EukaryoticMicrobiology, 46(5), Margulis,L. (1974). Five-kingdomclassification and the evo- 17S-18S. lution and origin of cells. EvolutionaryBiology, 7, 45-78. Whittaker, R.H. (1969). New concepts of kingdoms of Margulis,L. (1981). How many kingdoms?Current views of organisms.Science, 163, 150-160. biological classification. The AmericanBiology Teacher, Woese, C.R.,Kandler, 0. & Wheelis, M.L.(1990). Towardsa 43(9), 482-489. natural system of organisms:Proposal for the domains Margulis,L. & Schwartz,K.V. (1988). Five Kingdoms:An Archaea, Bacteria, and Eucarya. Proceedingsof the National IllustratedGuide to the Phyla of Life onl Earth, 2nd ed. Academyof Science,87, 4576-4579. New York:W.H. Freeman. Zrzavy,J.,Mihulka, S., Kepka,P., Bezdek, A. & Tietz,D. (1998). Phylogenyof Nakayama,T. et al. (1998). The basal position of scaly green the Metazoabased on morphologicaland 18Sribosomal DNA Cladistics, flagellates among the green algae (Chlorophyta) is evidence. 14, 249-285.

490 THEAMERICAN BIOLOGY TEACHER, VOLUME 63, NO.7,SEPTEMBER 2001