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Home , Alveolate, Apicomplexa, Babesia, Balantidium, Blastodinium, Ciliate

Alveolates Secondary article

Michael A Sleigh, University of Southampton, Southampton, UK Article Contents

. Outline Description and Characterization Three groups of , the , and sporozoans have been grouped . Phylogeny and Place in Overall Taxonomic Scheme together as ‘’ because typical cells in all three groups have a pair of subsurface . Major Subtaxa and Well-known membranes, forming inflated or flattened alveoli (fluid-filled cushions), beneath the surface membrane. The close relationship between the groups has been confirmed by molecular sequence analysis.

Outline Description and any between (Figure 1c). In all three groups the triple Characterization membrane structure tends to be underlain by a layer of granular containing , so that The name alveolates has been given to a cluster of three comparison of pellicular structure led to the suggestion large groups of protozoa, the ciliates (Ciliophora), that the membrane sandwich of the sporozoans probably Dinozoa (dinoflagellates) plus a few species with atypical arose from flattened internal alveoli beneath the surface features) and Sporozoa (more or less equivalent to membrane. ), which in many ways are very different All three groups that comprise the alveolates have had from one another. In former schemes of classification these an extensive evolutionary , in each case depen- three groups were placed far apart, but the distinctive dent upon the development of a distinctive pattern of feature which they share appears to be a true ancestral organization which is unique in the living world. It is character, since phylogenetic analysis by ribosomal estimated that there are about 7500 species of ciliates, 2000 ribonucleic acid (rRNA) has shown that the living species of dinoflagellates (as well as a similar number three groups are more closely related to one another than any one of them is to any other group (Gajadhar et al., 1991). All three groups have an unusual arrangement of membranes at the surface in most members and at C C some stage in their . These membranes form a E system of alveoli over much of the surface in many ciliates and dinoflagellates, forming part of the pellicles which characterize these two groups, but are pressed together as a sandwich of three membranes in the Sporozoa. Ciliates like and were among the first cells whose fine structure was studied with the (a) . Sections of these cells showed that over much of the body the surface membrane was underlain by two inner membranes separated by a fluid- filled space. It was soon discovered that the inner membranes actually belonged to cushion-shaped alveoli, regularly arranged between the rows of cilia of the cell surface, so that cilia and could emerge in bands (b) between the alveoli where only a single membrane was present (Figure 1a). These alveoli occasionally contain M plates of glycoprotein which may be calcified. Comparable examination of the cells of dinoflagellates like and showed that the thecal plates which cover (c) these cells are actually situated internally, within alveoli Figure 1 Diagrams of sections through the surface of members of the which lie under the surface membrane (Figure 1b). The fine three groups to show the arrangement of membranes. In ciliates structure of sporozoan cells varies with the stage of the life (a), rows of cilia (C) and extrusive (trichocysts or mucocysts) (E) cycle, and tends to be simplified in intracellular stages of emerge between the alveoli which underlie the surface membrane. In dinoflagellates (b), thecal plates may occupy the pellicular alveoli. In these parasites. In the extracellular stages of most species sporozoa (c), the two inner membranes are pressed tightly together the surface membrane of much of the cell is underlain by without any fluid space between, though these inner layers are interrupted two further membranes, tightly pressed together without at pits called ‘micropores’ (M).

ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Publishing Group / www.els.net 1 Alveolates of species, due to the traces left by the hard in in and clams, and some species have unusual internal some forms) and 5000 species of sporozoans. organelles. Where sexual occurs, fertilization involves the fusion of two small biflagellate .

Characteristics of the three main groups Sporozoans Ciliates The sporozoans are haploid parasitic protozoa, mostly The ciliates are diploid cells, typically with two types of with complex life cycles usually involving at least one stage nuclei, one or more polyploid macronuclei as well as one or when the parasite grows within a cell. Although the more diploid micronuclei, and with only the latter traditional name of Sporozoa has remained widely used participating in the exchange of genetic material during and understood, the principal subgroup was given the new the sexual process of conjugation. They also have a cortical name Apicomplexa a few ago, in recognition of the structure in the pellicle, including the highly specific arrays fact that there is a distinctive group of organelles at the of cilia and their associated specific patterns of rootlet apical end of specific stages (those capable of penetrating fibres (the infraciliature) as well as the system of alveoli, host cells) in the life cycle of most species. This apical which is passed on to daughter cells through a mechanism complex of polar organelles consists of the conoid, a of nongenetic, inheritance. The majority of ciliates truncated cone of short spiral microtubules, through which are free-living cells, actively swimming with their cilia and pass the stalks of secretory organelles called , and feeding on other filtered from the water or around which there are two rings, one circling the distal end picked up from surfaces. Food are ingested and the other circling the proximal end of the conoid. The through a special area of the body surface, the , apical complex is a site of attachment of the sporozoan to a and digested in food . Contractile vacuoles for salt host cell, and the rhoptries are believed to release products and water balance are best developed in ciliates. The that stimulate the host cell to invaginate and draw in the parasitic forms typically live in the gut of their host, and parasite. In many cases hosts are infected with sporozoans usually retain distinctive features. by ingesting ; these spores develop in the gut of the host to release spindle-shaped infective cells called sporozoites, which enter cells of the host. Similar sporo- Dinoflagellates zoites are injected into certain hosts by , Most dinoflagellates are haploid cells whose nucleus like the when it transmits the malarial parasite. contains obvious condensed throughout Parasite growth and (usually repeated cycles of) reproduc- the . This is because the of dino- tion take place before a process of fertilization between two flagellates contains little , a feature that led parasite cells occurs, their nuclei fuse, and subsequent to the suggestion that dinoflagellates were ‘mesokaryotic’ is followed by and/or sporozoite formation. organisms that belonged part way between the prokaryotic In some cases the cells which fuse are similar with no and the with many amoeboid cells, and in other cases a flagellate microgamete histones. However, dinoflagellates are true eukaryotes in swims to fuse with a stationary macrogamete. other respects, with mitotic and meiotic nuclear divisions and fertilization. They are typically biflagellate cells, generally with one longitudinal, backwardly-directed flagellum and one transverse flagellum which executes a Phylogeny and Place in Overall helical beat, often within an equatorial groove. The pellicle Taxonomic Scheme generally has a pattern of alveoli (called amphiesmal vesicles by workers on this group) which appear empty or Until recently the three groups that comprise the alveolates contain thin plates in the ‘naked’ or ‘unarmoured’ species were classified separately, and rather far apart. The ciliates but contain thick thecal plates in the thecate or ‘armoured’ were generally regarded as the most advanced of the species. The plates are principally composed of poly- protozoa, largely because many of them are among the saccharide material and impose specific shapes upon most complex cells known. Although Haeckel in 1866 thecate forms. About half of the species contain brown included ciliates (as ) in the , and are photosynthetic. Most colourless species, as they were regarded as a separate in the well as some which contain plastids, engulf other micro- Protozoa in Bu¨ tschli’s 1880 classification and as a separate organisms at a naked area near the flagellar bases; some phylum in the kingdom Protozoa by Levine et al. in 1980. species produce, from the naked area, which The Sporozoa were likewise a separate class of the extend to form a thin protoplasmic veil around Protozoa in 1880 and a separate phylum (Levine’s larger than themselves and digest them within a food Apicomplexa) in 1980. With their haploid and rather outside the main body. There is a considerable simpler cells, the Sporozoa were regarded as more lowly diversity of body form, in free-living forms as well as in protozoans in most systems. Dinoflagellates were claimed parasites in higher and photosynthetic symbionts as by phycologists, and this was widely accepted

2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net Alveolates because the most familiar species were brown photosyn- Phylum Dinozoa thetic cells, an observation which probably led Bu¨ tschli to Phylum Sporozoa place them near diatoms. On the other hand many Superphylum Heterokaryota dinoflagellates feed as animals, so that protozoologists Phylum Ciliophora included them in protozoan classifications as members of the subphylum Mastigophora. However, in the 1970s and 1980s structural similarities between features of ciliates and dinoflagellates were Major Subtaxa and Well-known Species already leading to suggestions that these groups were probably more closely related than had previously been The phylum Dinozoa believed. The possibility that the membrane arrangement of Sporozoa might reflect a common ancestry with ciliates Aseries of comprehensive reviews on features of dino- and dinoflagellates made it easier to accept the evidence flagellates can be found in the book edited by Taylor from the similarity of sequences of small subunit rRNA, (1987). At that dinoflagellate was stated to which placed the three groups together on a separate be ‘in a greater than usual state of flux’, and a number of branch of the . The recent confirmation genera remained unclassified. Some of these have been that sporozoan cells contain relict organelles containing placed in the subphylum Protalveolata by Cavalier-Smith -like, circular deoxyribonucleic acid (DNA) (Wil- (1998), including the common marine (Figure 2a) son, 1998), gives rise to the possibility that the ancestor of and some other forms, all of which have typical all alveolates may have been photosynthetic. In the chromosomes. The remaining dinozoans are placed in universal phylogenetic scheme there appear to have been some 14 orders in the subphylum Dinoflagellata. Knowl- a number of early branches from the main trunk of edge of the group is limited by the fact that, with a few eukaryote , including and , notable exceptions, research on the nonphotosynthetic before a wide radiation of towards the crown of the members, and particularly the parasitic forms, has not tree gave rise to alveolates and to some other groups of been well integrated with that on photosynthetic forms. flagellate and amoeboid Protozoa as well as the kingdoms This probably depends on the general view among , Fungi, Animalia and Plantae. zoologists that dinoflagellates were the province of In a recent revision of his classification of the kingdom botanists, and a general lack of interest among botanists Protozoa within the empire Eukaryota, Cavalier-Smith in parasites that live in animals. (1998) placed the three main groups of alveolates in the Photosynthetic dinoflagellates are found abundantly in following manner: the . Almost all freshwater dinoflagellates are Kingdom Protozoa motile autotrophic forms belonging to such thecate genera Subkingdom Eozoa as Ceratium and Peridinium (Figure 2b), and naked forms Infrakingdom Alveolata like and , with rather typical Superphylum Miozoa dinoflagellate shapes, which live in lakes, and can form

(a) (b) (c) (d)

Figure 2 Examples of the Dinozoa. (a) The protalveolate Oxyrrhis (about 25 mm long). (b) Peridinium with a typical shape and thick thecal plates (cell about 50 mm long). (c) In the thecal plates are produced into wide flanges around the flagellar groove and at the posterior (cell about 100 mm long). (d) Prorocentrum (about 50 mm long) lacks an equatorial flagellar groove, but still has flagella which beat in different patterns.

ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net 3 Alveolates blooms under favourable conditions of nutrients, light carbonate deposition in the or shells of organ- and temperature. Marine dinoflagellates are more isms such as corals and foraminiferans. diverse; marine species of the same four genera are Parasitic dinoflagellates often bear little resemblance to joined by similar forms like and by forms their free-living relatives, but betray their relationship by like and Ornithocercus (Figure 2c), with deep the structure of the motile dinospores, which have a thecal flanges between which the transverse flagellum characteristic dinoflagellate appearance. Three principal moves, and Prorocentrum (Figure 2d), with no transverse groups were recognized by Cachon and Cachon (1987): groove at all. Species of Protoperidinium, Ceratium and one extracellular and living on other protozoa, inverte- Gyrodinium, among others that contain , are brates and fish (e.g. , ); a second also known to ingest particulate food, and about half of all living entirely intracellularly, usually in radiolarians, but dinoflagellate species are that have no sometimes in and in fish eggs (e.g. , chloroplasts; these include species in genera like Proto- Ichthyodinium); and in a third the parasite starts to grow peridinium and Gyrodinium, many of whose members are within the cells of its host, usually a protozoan, and then photosynthetic. emerges as a worm-like body before dividing into Photosynthetic dinoflagellates have importance beyond dinospores (e.g. Amoebophrya). Some of the fish parasites the fact that they are among the principal primary in the first group cause economic damage in aquaculture, producers in the plankton. Many species form conspicuous and damage to fisheries has also been attributed blooms, containing millions of cells per litre, referred to as to dinoflagellates. ‘red ’ (in a minority of cases other types of flagellate, or even the ciliate , may be responsible for the red water). Such blooms create problems for other aquatic The phylum Sporozoa organisms, killing fish and other animals; these problems may be of a more general nature when they result from the The composition of this entirely parasitic phylum has depletion of by bacteria in the water where dead recently been revised and broadened by Cavalier-Smith dinoflagellate cells are decaying. Afew of the bloom- (1998) under the name Sporozoa, which includes groups forming dinoflagellates (e.g. Gymnodinium breve) are formerly classified in the Apicomplexa. For some time an directly toxic to fish at levels below those which severely oyster parasite was regarded as a (possibly deplete oxygen levels, but more important are the primitive) apicomplexan, because it has parts of the apical dinoflagellate which are accumulated by filter- complex and pellicular alveoli, but it also has features of feeding bivalve molluscs, and indirectly kill animals that dinoflagellates, and has been transferred by Cavalier- eat the shellfish. Toxins ( and ) from Smith to the Protalveolata group of the Dinozoa. several species of Gonyaulax, especially G. tamarensis, and Three classes (or subphyla) of sporozoans, the Gregar- Pyrodinium can accumulate to sufficient levels in the tissues inidea, the Coccidea and the Haematozoea, have been of clams, and oysters to cause severe cases of recognized for a long time, although some authors retain paralytic shellfish poisoning in by blocking the Haematozoea and Coccidea within a single class, as is sodium fluxes through neuromuscular membranes. An- the case in the widenened scope of the coccidian group in other type of accumulated in shellfish, and thought to Cavalier-Smith’s recent revision. Like other parasites, come from species of Prorocentrum, has caused diarrhoetic sporozoans must reproduce very effectively in order to shellfish poisoning in Japan and Europe. It is thought that ensure enough progeny to infect a new host; they may show ciguatera toxins in the moray eel and some other fish may reproduction in some or all of the following three stages: by also come from dinoflagellates. mitotic division to increase the within a host Afew species of photosynthestic dinoflagellates live in (schizogony); by mitotic division in the formation of vaculoes within the cells of marine protozoa and animals, numerous gametes (gametogony); and following fertiliza- including radiolarians, acantharians, foraminiferans, cni- tion by divisions that include meiosis in the formation of darians (jellyfish, sea anemones and corals), flatworms and infective sporozoites (sporogony). molluscs (clams) (Smith and Douglas, 1987). At one time All sporozoans commence their parasitic life with an all of these symbiotic dinoflagellates were referred to as intracellular stage resulting from the entry of a sporozoite ‘’; it is now believed that most of them belong into a host cell (Kreier and Baker, 1987). After this initial to one species, microadriaticum, but a few intracellular growth, gregarines outgrow the space avail- hosts contain other symbionts (e.g. species of Amphidi- able within the host cell and escape to live and grow further nium). Both partners in the relationship benefit because within the digestive tract or body cavity of their varied products of are released by the or lower host, before joining in pairs symbiont and used by the host, and nitrogen and within a common membrane and producing large numbers phosphorus compounds released by the host are used by of gametes. Fusion of paired gametes is followed by the symbionts. In addition it is believed that the photo- sporogony forming sporozoites within sporocysts, resting synthetic activity of the symbiont accelerates calcium stages which infect a new host by being eaten. Generally the

4 ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net Alveolates

The apical complex of infective cells of haematozoeans lacks the conoid or polar rings. The sporozoites develop in blood-sucking and are injected as naked cells into the host in saliva. The sporozoites enter cells of the vertebrate host, grow and undergo repeated stages of schizogony, mostly, but not exclusively, in blood cells. Eventually parasite cells prepare to form gametes, but will not mature into gametes unless they are taken into the gut of a blood-sucking vector. Within the vector gut the parasites form macro-or microgametes, performing ferti- lization to form a migratory , whose growth and sporogony produces many sporozoites. Members of both (a) (b) orders of haematozoeans are important parasites. Those in Figure 3 Examples of Sporozoa. (a) Extracellular gregarine cells like this the order are transmitted by dipteran flies. Gregarina from the gut of a mealworm may reach lengths of 200 mmor The best known examples of this group are malarial more. (b) Coccidians of different genera form characteristic spores, as parasites belonging to the , several shown by this in which the outer oocyst (35 mm long) contains four species of which are transmitted between humans by sporocysts, each containing two sporozoite cells. mosquitoes; other species are found in other mammals and . and are genera found in birds and reptiles and transmitted by midges and most extensive multiplication of gregarines takes place blackfly. Important members of the order , during gametogony. Well-known examples are which are transmitted by , belong to the genera in earthworms, in marine and Gregar- and . These are responsible for serious ina (Figure 3a) in . diseases of domestic animals throughout the world, and Most coccidians gain entry to their hosts by being eaten generally only cause disease in cases of immune as sporocysts, from which sporozoites emerge to infect, deficiency or removal of the . typically, cells of the gut wall. After entry to cells these Cavalier-Smith (1998) has included within the Sporozoa sporozoans remain intracellular, generally going through several genera of other spore-producing protozoa (Para- many cycles of (schizogony), burst- myxa, Haplosporidium and Metchnikovella), formerly ing the host cells to release many infective merozoites classed elsewhere in independent groups, or as microspor- which enter new cells within the same host. Eventually the idians. These are parasites of ; their phyloge- parasite cells mature into gametes, one macrogamete being netic relationships remain to be firmly established. formed per host cell or many flagellate microgametes. The microgametes escape and swim to fertilize macrogametes; after fertilization the zygote divides a few , with The phylum Ciliophora meiosis, to form sporozoites within sporocysts (Figure 3b). Multiplication here takes place principally by schizogony. The characteristics of ciliates and the composition of this This group contains important parasites in the genus phylum have been comprehensively described by Corliss Eimeria, long known to be responsible for in (1979). They have been classified in many different ways, domestic animals and birds. There are several coccidians generally on the basis of the arrangement of cilia on the that cause serious disease in immunocompromised pa- general body surface and in the region of the cell mouth tients, although others seem to carry them without illness. (cytostome). In a recent scheme Corliss (1994) divided this Among these is Toxoplasma, which has a high human phylum into eight classes, following ultrastructural studies prevalence but does not undergo a complete life cycle in and extensive discussion by many authors. This scheme is humans, although it develops as a typical coccidian, similar likely to change when the results of rRNAanalysis are also or identical to , in cats. , named from its taken into account; at present the molecular sequences of found in , and occasionally, human, muscle, is a too few species have been studied (Hirt et al., 1998) to related Isospora, with a sporogony stage in dogs. Crypto- propose more than small changes to the scheme put sporidium, whose spores find their way into drinking water, forward by Corliss. and which has caused recent health scares, is another Members of the class are probably the coccidian. The group also includes some blood parasites most primitive surviving ciliates and are unusual in which have coccidian features in their life cycle; these possessing nondividing, diploid macronuclei and generally include and , found in lower lacking pellicular alveoli; they are often long, but flattened, , but with vector stages in invertebrates that are ciliates, mostly from marine sands. Within the class usually eaten by the vertebrate, although some inject Polyhymenophora, all of which have a conspicuous row parasites with saliva. of large membranelle cilia associated with the cytostome,

ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net 5 Alveolates

P M

M

(b)

(c)

C

(d) (a) (e)

Figure 4 Examples of the Ciliophora. (a) (about 200 mm long) with a row of membranelles (M) and other cilia formed into bundles as cirri (C). (b) Strombidium (about 30 mm long) with a short band of feeding membranelles (M). (c) (about 100 mm long) with a ‘proboscis’ (P) for feeding and two bands of swimming cilia. (d) The suctorian Podophrya (about 50 mm in diameter) with tentacles for feeding and an attachment stalk. (e) The ciliate (about 75 mm long). the subclass Heterotrichia, which also have a full body Podophrya (Figure 4d). Some forms have a prominent covering of ciliary rows, appear from rRNAanalysis to be cytopharyngeal basket of microtubular rods, which is also closely related to karyorelicteans. Members of several present in a related class, the , e.g. , genera of ciliates are commonly encountered, some of which ingest filamentous algae. Close to these two probably the best known are the large species of the classes is the class , most of whom, like the trumpet-shaped and the cylindrical , ubiquitous Colpoda species (Figure 4e), are found in , at which commonly reach 2 mm in length; species least as cysts. are anaerobes and Nyctotherus is a common symbiont in Most of the remaining ciliates belong to the class the gut of amphibians. , named from the presence of a small The other subclass of polyhymenophorans are the number (3–4, commonly) of membranelles or comparable Spirotrichia, apparently more-evolved ciliates that have compound cilia around the mouth, and rows of body cilia. few body cilia, often grouped into compound cirri; this Among the six subclasses, the Hymenostomatia, e.g. group includes several well-known ciliates that ‘run’ Tetrahymena, the protozoan most studied by biochemists, around over surfaces, e.g. Stylonychia (Figure 4a), and the Peniculinia, e.g. the familiar Paramecium species and and Aspidisca, both of which are common in fresh the Peritrichia, e.g. and Carchesium, well-known and salt water and important consumers of bacteria in and extremely important in sewage treatment sewage treatment works, as well as important planktonic systems, all have important places. Of the other three ‘’ ciliates like Strombidium (Figure 4b) and the subclasses, the Astomatia are endoparasites, mostly in , whose cup-shaped or cylindrical loricas are annelids and the Apostomatia are mostly ectoparasites on abundant in plankton samples. Asecond group at this crustaceans, but the Scuticociliatia are often abundant intermediate level of evolution, according to rRNA bacterivorous forms with few cilia, e.g. , Pleur- evidence, is the class , including forms with onema. The final class, the , contains ciliates very simple, or even lacking, mouth cilia; it includes with an anterior mouth and simple mouth ciliature, which , the only ciliate parasitic in humans, ciliates are often predatory or detritivores. which inhabit the rumen of mammals and the hind-gut of other herbivores like horses, as well as active predatory ciliates like Didinium (Figure 4c) which preys on species of Paramecium. References The first group to separate at the more advanced level of evolution appears to be the class , Cachon J and Cachon M (1987) Parasitic dinoflagellates. In: Taylor FJR (ed.) The Biology of Dinoflagellates, pp. 571–610. Oxford: Blackwell. characterized by the possession of ribbons of microtubules Cavalier-Smith T (1998) Neomonada and the origin of animals and around the cytopharynx leading into the cytoplasm from fungi. In: Coombs GH, Vickerman K, Sleigh MAand Warren A(eds) the cell mouth, e.g. Chilodonella or chonotrichs, or from Evolutionary Relationships Among Protozoa, pp. 375–407. London: the multiple mouths of the suctorians, e.g. Acineta, Chapman and Hall.

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Corliss JO (1979) The Ciliated Protozoa: Characterization, Classification Relationships Among Protozoa, pp. 293–304. London: Chapman and and Guide to the Literature, 2nd edn. Oxford: Pergamon. Hall. Corliss JO (1994) An interim utilitarian (‘user friendly’) heirarchical classification of the protists. Acta Protozoologica 33: 1–51. Gajadhar AA, Marquardt WC, Hall R et al. (1991) Ribosomal RNA Further Reading sequences of Sarcocystis muris, Theileria annulata and Crypthecodi- nium cohnii reveal evolutionary relationship among apicomplexans, Anderson OR (1987) Comparative Protozoology. , , dinoflagellates and ciliates. Molecular and Biochemical Parasitology Life History. Berlin: Springer. 45: 147–154. Coombs GH, Vickerman K, Sleigh MAand Warren A(eds) (1998) Hirt RP, Wilkinson M and Embley TM (1998) Molecular and cellular Evolutionary Relationships Among Protozoa. London: Chapman and evolution of ciliates: phylogenetic perspective. In: Coombs GH, Hall. Vickerman K, Sleigh MAand Warren A(eds) Evolutionary Relation- Grell KG (1973) Protozoology, 3rd edn. Berlin: Springer. ships Among Protozoa, pp. 327–340. London: Chapman and Hall. Hausmann K and Hu¨ lsmann N (1996) Protozoology, 2nd edn. Stuttgart, Kreier JP and Baker JR (1987) Parasitic Protozoa. Winchester, MA: Germany: Thieme. Allen and Unwin. Kudo RR (1996) Protozoology, 5th edn. Springfield, IL: Thomas. Sleigh MA(1989) Protozoa and Other Protists. Cambridge: Cambridge Lee JJ, Hutner SH and Bovee EC (eds) (1985) An Illustrated Guide to the University Press. Protozoa. Lawrence, KS: Society of Protozoologists. Smith DC and Douglas AE (1987) The Biology of . London: Levine ND (1988) The Protozoan Phylum Apicomplexa. Boca Raton, Edward Arnold. FL: CRC Press. Taylor FJR (ed.) (1987) The Biology of Dinoflagellates. Oxford: Puytorac P de, Grain J and Mignot J-P (1987) Precis de Protistologie. Blackwell. Paris: Boube´e. Wilson RJM (1998) Plastid-like DNAin apicomplexans. In: Coombs Sleigh MA(1989) Protozoa and Other Protists. Cambridge: Cambridge GH, Vickerman K, Sleigh MAand Warren A(eds) Evolutionary University Press.

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