Alveolates
Secondary article
Article Contents
Michael A Sleigh, University of Southampton, Southampton, UK
. Outline Description and Characterization
Three groups of Protozoa, the ciliates, dinoflagellates and sporozoans have been grouped
together as ‘alveolates’ because typical cells in all three groups have a pair of subsurface
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
Characterization
The name alveolates has been given to a cluster of three
large groups of protozoa, the ciliates (Ciliophora),
Dinozoa (dinoflagellates) plus a few species with atypical
features) and Sporozoa (more or less equivalent to
Apicomplexa), which in many ways are very different
from one another. In former schemes of classification these
three groups were placed far apart, but the distinctive
feature which they share appears to be a true ancestral
character, since phylogenetic analysis by ribosomal
ribonucleic acid (rRNA) sequencing has shown that the
three groups are more closely related to one another than
any one of them is to any other protist group (Gajadhar
et al., 1991). All three groups have an unusual arrangement
of membranes at the cell surface in most members and at
some stage in their life cycle. These membranes form a
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 Paramecium and Tetrahymena were among
the first cells whose fine structure was studied with the
electron microscope. Sections of these cells showed that
over much of the body the surface membrane was
underlain by two inner membranes separated by a fluidfilled 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 trichocysts could emerge in bands
between the alveoli where only a single membrane was
present (Figure 1a). These alveoli occasionally contain
plates of glycoprotein which may be calcified. Comparable
examination of the cells of dinoflagellates like Ceratium
and Peridinium showed that the thecal plates which cover
these cells are actually situated internally, within alveoli
which lie under the surface membrane (Figure 1b). The fine
structure of sporozoan cells varies with the stage of the life
cycle, and tends to be simplified in intracellular stages of
these parasites. In the extracellular stages of most species
the surface membrane of much of the cell is underlain by
two further membranes, tightly pressed together without
. Phylogeny and Place in Overall Taxonomic Scheme
. Major Subtaxa and Well-known Species
any space between (Figure 1c). In all three groups the triple
membrane structure tends to be underlain by a layer of
granular cytoplasm containing microtubules, so that
comparison of pellicular structure led to the suggestion
that the membrane sandwich of the sporozoans probably
arose from flattened internal alveoli beneath the surface
membrane.
All three groups that comprise the alveolates have had
an extensive evolutionary radiation, in each case dependent upon the development of a distinctive pattern of
organization which is unique in the living world. It is
estimated that there are about 7500 species of ciliates, 2000
living species of dinoflagellates (as well as a similar number
C
C
E
(a)
(b)
M
(c)
Figure 1 Diagrams of sections through the surface of members of the
three alveolate groups to show the arrangement of membranes. In ciliates
(a), rows of cilia (C) and extrusive organelles (trichocysts or mucocysts) (E)
emerge between the alveoli which underlie the surface membrane. In
dinoflagellates (b), thecal plates may occupy the pellicular alveoli. In
sporozoa (c), the two inner membranes are pressed tightly together
without any fluid space between, though these inner layers are interrupted
at pits called ‘micropores’ (M).
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1
Alveolates
of fossil species, due to the traces left by the hard theca in
some forms) and 5000 species of sporozoans.
Characteristics of the three main groups
Ciliates
The ciliates are diploid cells, typically with two types of
nuclei, one or more polyploid macronuclei as well as one or
more diploid micronuclei, and with only the latter
participating in the exchange of genetic material during
the sexual process of conjugation. They also have a cortical
structure in the pellicle, including the highly specific arrays
of cilia and their associated specific patterns of rootlet
fibres (the infraciliature) as well as the system of alveoli,
which is passed on to daughter cells through a mechanism
of nongenetic, somatic inheritance. The majority of ciliates
are free-living cells, actively swimming with their cilia and
feeding on other microorganisms filtered from the water or
picked up from surfaces. Food particles are ingested
through a special area of the body surface, the cytostome,
and digested in food vacuoles. Contractile vacuoles for salt
and water balance are best developed in ciliates. The
parasitic forms typically live in the gut of their host, and
usually retain distinctive ciliate features.
Dinoflagellates
Most dinoflagellates are haploid cells whose nucleus
contains obvious condensed chromosomes throughout
the cell cycle. This is because the chromatin of dinoflagellates contains little histone protein, a feature that led
to the suggestion that dinoflagellates were ‘mesokaryotic’
organisms that belonged part way between the prokaryotic
bacteria with no histones and the eukaryotes with many
histones. However, dinoflagellates are true eukaryotes in
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
helical beat, often within an equatorial groove. The pellicle
generally has a pattern of alveoli (called amphiesmal
vesicles by workers on this group) which appear empty or
contain thin plates in the ‘naked’ or ‘unarmoured’ species
but contain thick thecal plates in the thecate or ‘armoured’
species. The plates are principally composed of polysaccharide material and impose specific shapes upon
thecate forms. About half of the species contain brown
plastids and are photosynthetic. Most colourless species, as
well as some which contain plastids, engulf other microorganisms at a naked area near the flagellar bases; some
species produce, from the naked area, pseudopodia which
extend to form a thin protoplasmic veil around diatoms
larger than themselves and digest them within a food
vacuole outside the main body. There is a considerable
diversity of body form, in free-living forms as well as in
parasites in higher animals and photosynthetic symbionts
2
in corals and clams, and some species have unusual internal
organelles. Where sexual reproduction occurs, fertilization
involves the fusion of two small biflagellate gametes.
Sporozoans
The sporozoans are haploid parasitic protozoa, mostly
with complex life cycles usually involving at least one stage
when the parasite grows within a host cell. Although the
traditional name of Sporozoa has remained widely used
and understood, the principal subgroup was given the new
name Apicomplexa a few years ago, in recognition of the
fact that there is a distinctive group of organelles at the
apical end of specific stages (those capable of penetrating
host cells) in the life cycle of most species. This apical
complex of polar organelles consists of the conoid, a
truncated cone of short spiral microtubules, through which
pass the stalks of secretory organelles called rhoptries, and
around which there are two rings, one circling the distal end
and the other circling the proximal end of the conoid. The
apical complex is a site of attachment of the sporozoan to a
host cell, and the rhoptries are believed to release products
that stimulate the host cell to invaginate and draw in the
parasite. In many cases hosts are infected with sporozoans
by ingesting spores; these spores develop in the gut of the
host to release spindle-shaped infective cells called
sporozoites, which enter cells of the host. Similar sporozoites are injected into certain hosts by vector organisms,
like the mosquito when it transmits the malarial parasite.
Parasite growth and (usually repeated cycles of) reproduction take place before a process of fertilization between two
parasite cells occurs, their nuclei fuse, and subsequent
meiosis is followed by spore and/or sporozoite formation.
In some cases the gamete cells which fuse are similar
amoeboid cells, and in other cases a flagellate microgamete
swims to fuse with a stationary macrogamete.
Phylogeny and Place in Overall
Taxonomic Scheme
Until recently the three groups that comprise the alveolates
were classified separately, and rather far apart. The ciliates
were generally regarded as the most advanced of the
protozoa, largely because many of them are among the
most complex cells known. Although Haeckel in 1866
included ciliates (as Infusoria) in the Animal Kingdom,
they were regarded as a separate class in the phylum
Protozoa in Bütschli’s 1880 classification and as a separate
phylum in the kingdom Protozoa by Levine et al. in 1980.
The Sporozoa were likewise a separate class of the
Protozoa in 1880 and a separate phylum (Levine’s
Apicomplexa) in 1980. With their haploid and rather
simpler cells, the Sporozoa were regarded as more lowly
protozoans in most systems. Dinoflagellates were claimed
as algae by phycologists, and this was widely accepted
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Alveolates
because the most familiar species were brown photosynthetic cells, an observation which probably led Bütschli to
place them near diatoms. On the other hand many
dinoflagellates feed as animals, so that protozoologists
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
already leading to suggestions that these groups were
probably more closely related than had previously been
believed. The possibility that the membrane arrangement
of Sporozoa might reflect a common ancestry with ciliates
and dinoflagellates made it easier to accept the evidence
from the similarity of sequences of small subunit rRNA,
which placed the three groups together on a separate
branch of the phylogenetic tree. The recent confirmation
that sporozoan cells contain relict organelles containing
plastid-like, circular deoxyribonucleic acid (DNA) (Wilson, 1998), gives rise to the possibility that the ancestor of
all alveolates may have been photosynthetic. In the
universal phylogenetic scheme there appear to have been
a number of early branches from the main trunk of
eukaryote evolution, including Archezoa and Euglenozoa,
before a wide radiation of protists towards the crown of the
tree gave rise to alveolates and to some other groups of
flagellate and amoeboid Protozoa as well as the kingdoms
Chromista, Fungi, Animalia and Plantae.
In a recent revision of his classification of the kingdom
Protozoa within the empire Eukaryota, Cavalier-Smith
(1998) placed the three main groups of alveolates in the
following manner:
Kingdom Protozoa
Subkingdom Eozoa
Infrakingdom Alveolata
Superphylum Miozoa
(a)
(b)
Phylum Dinozoa
Phylum Sporozoa
Superphylum Heterokaryota
Phylum Ciliophora
Major Subtaxa and Well-known Species
The phylum Dinozoa
A series of comprehensive reviews on features of dinoflagellates can be found in the book edited by Taylor
(1987). At that time dinoflagellate taxonomy was stated to
be ‘in a greater than usual state of flux’, and a number of
genera remained unclassified. Some of these have been
placed in the subphylum Protalveolata by Cavalier-Smith
(1998), including the common marine Oxyrrhis (Figure 2a)
and some other forms, all of which have typical eukaryote
chromosomes. The remaining dinozoans are placed in
some 14 orders in the subphylum Dinoflagellata. Knowledge of the group is limited by the fact that, with a few
notable exceptions, research on the nonphotosynthetic
members, and particularly the parasitic forms, has not
been well integrated with that on photosynthetic forms.
This probably depends on the general view among
zoologists that dinoflagellates were the province of
botanists, and a general lack of interest among botanists
in parasites that live in animals.
Photosynthetic dinoflagellates are found abundantly in
the plankton. Almost all freshwater dinoflagellates are
motile autotrophic forms belonging to such thecate genera
as Ceratium and Peridinium (Figure 2b), and naked forms
like Gymnodinium and Amphidinium, with rather typical
dinoflagellate shapes, which live in lakes, and can form
(c)
(d)
Figure 2 Examples of the Dinozoa. (a) The protalveolate Oxyrrhis (about 25 mm long). (b) Peridinium with a typical dinoflagellate shape and thick thecal
plates (cell about 50 mm long). (c) In Ornithocercus 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.
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Alveolates
blooms under favourable conditions of nutrients, light
and temperature. Marine dinoflagellates are more
diverse; marine species of the same four genera are
joined by similar forms like Gonyaulax and by forms
like Dinophysis and Ornithocercus (Figure 2c), with deep
thecal flanges between which the transverse flagellum
moves, and Prorocentrum (Figure 2d), with no transverse
groove at all. Species of Protoperidinium, Ceratium and
Gyrodinium, among others that contain chloroplasts, are
also known to ingest particulate food, and about half of all
dinoflagellate species are heterotrophs that have no
chloroplasts; these include species in genera like Protoperidinium and Gyrodinium, many of whose members are
photosynthetic.
Photosynthetic dinoflagellates have importance beyond
the fact that they are among the principal primary
producers in the plankton. Many species form conspicuous
blooms, containing millions of cells per litre, referred to as
‘red tides’ (in a minority of cases other types of flagellate, or
even the ciliate Mesodinium, may be responsible for the red
water). Such blooms create problems for other aquatic
organisms, killing fish and other animals; these problems
may be of a more general nature when they result from the
depletion of oxygen by bacteria in the water where dead
dinoflagellate cells are decaying. A few of the bloomforming dinoflagellates (e.g. Gymnodinium breve) are
directly toxic to fish at levels below those which severely
deplete oxygen levels, but more important are the
dinoflagellate toxins which are accumulated by filterfeeding bivalve molluscs, and indirectly kill animals that
eat the shellfish. Toxins (saxitoxin and gonyautoxins) from
several species of Gonyaulax, especially G. tamarensis, and
Pyrodinium can accumulate to sufficient levels in the tissues
of clams, mussels and oysters to cause severe cases of
paralytic shellfish poisoning in humans by blocking
sodium fluxes through neuromuscular membranes. Another type of toxin accumulated in shellfish, and thought to
come from species of Prorocentrum, has caused diarrhoetic
shellfish poisoning in Japan and Europe. It is thought that
ciguatera toxins in the moray eel and some other fish may
also come from dinoflagellates.
A few species of photosynthestic dinoflagellates live in
vaculoes within the cells of marine protozoa and animals,
including radiolarians, acantharians, foraminiferans, cnidarians (jellyfish, sea anemones and corals), flatworms and
molluscs (clams) (Smith and Douglas, 1987). At one time
all of these symbiotic dinoflagellates were referred to as
‘zooxanthellae’; it is now believed that most of them belong
to one species, Symbiodinium microadriaticum, but a few
hosts contain other symbionts (e.g. species of Amphidinium). Both partners in the relationship benefit because
varied products of photosynthesis are released by the
symbiont and used by the host, and nitrogen and
phosphorus compounds released by the host are used by
the symbionts. In addition it is believed that the photosynthetic activity of the symbiont accelerates calcium
4
carbonate deposition in the skeletons or shells of organisms such as corals and foraminiferans.
Parasitic dinoflagellates often bear little resemblance to
their free-living relatives, but betray their relationship by
the structure of the motile dinospores, which have a
characteristic dinoflagellate appearance. Three principal
groups were recognized by Cachon and Cachon (1987):
one extracellular and living on other protozoa, invertebrates and fish (e.g. Blastodinium, Oodinium); a second
living entirely intracellularly, usually in radiolarians, but
sometimes in crustaceans and in fish eggs (e.g. Syndinium,
Ichthyodinium); and in a third the parasite starts to grow
within the cells of its host, usually a protozoan, and then
emerges as a worm-like body before dividing into
dinospores (e.g. Amoebophrya). Some of the fish parasites
in the first group cause economic damage in aquaculture,
and damage to crustacean fisheries has also been attributed
to dinoflagellates.
The phylum Sporozoa
The composition of this entirely parasitic phylum has
recently been revised and broadened by Cavalier-Smith
(1998) under the name Sporozoa, which includes groups
formerly classified in the Apicomplexa. For some time an
oyster parasite Perkinsus was regarded as a (possibly
primitive) apicomplexan, because it has parts of the apical
complex and pellicular alveoli, but it also has features of
dinoflagellates, and has been transferred by CavalierSmith to the Protalveolata group of the Dinozoa.
Three classes (or subphyla) of sporozoans, the Gregarinidea, the Coccidea and the Haematozoea, have been
recognized for a long time, although some authors retain
the Haematozoea and Coccidea within a single class, as is
the case in the widenened scope of the coccidian group in
Cavalier-Smith’s recent revision. Like other parasites,
sporozoans must reproduce very effectively in order to
ensure enough progeny to infect a new host; they may show
reproduction in some or all of the following three stages: by
mitotic division to increase the infection within a host
(schizogony); by mitotic division in the formation of
numerous gametes (gametogony); and following fertilization by divisions that include meiosis in the formation of
infective sporozoites (sporogony).
All sporozoans commence their parasitic life with an
intracellular stage resulting from the entry of a sporozoite
into a host cell (Kreier and Baker, 1987). After this initial
intracellular growth, gregarines outgrow the space available within the host cell and escape to live and grow further
within the digestive tract or body cavity of their
invertebrate or lower chordate host, before joining in pairs
within a common membrane and producing large numbers
of gametes. Fusion of paired gametes is followed by
sporogony forming sporozoites within sporocysts, resting
stages which infect a new host by being eaten. Generally the
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Alveolates
(a)
(b)
Figure 3 Examples of Sporozoa. (a) Extracellular gregarine cells like this
Gregarina from the gut of a mealworm may reach lengths of 200 mm or
more. (b) Coccidians of different genera form characteristic spores, as
shown by this Eimeria in which the outer oocyst (35 mm long) contains four
sporocysts, each containing two sporozoite cells.
most extensive multiplication of gregarines takes place
during gametogony. Well-known examples are Monocystis
in earthworms, Selenidium in marine annelids and Gregarina (Figure 3a) in insects.
Most coccidians gain entry to their hosts by being eaten
as sporocysts, from which sporozoites emerge to infect,
typically, cells of the gut wall. After entry to cells these
sporozoans remain intracellular, generally going through
many cycles of asexual reproduction (schizogony), bursting the host cells to release many infective merozoites
which enter new cells within the same host. Eventually the
parasite cells mature into gametes, one macrogamete being
formed per host cell or many flagellate microgametes. The
microgametes escape and swim to fertilize macrogametes;
after fertilization the zygote divides a few times, with
meiosis, to form sporozoites within sporocysts (Figure 3b).
Multiplication here takes place principally by schizogony.
This group contains important parasites in the genus
Eimeria, long known to be responsible for coccidiosis in
domestic animals and birds. There are several coccidians
that cause serious disease in immunocompromised patients, although others seem to carry them without illness.
Among these is Toxoplasma, which has a high human
prevalence but does not undergo a complete life cycle in
humans, although it develops as a typical coccidian, similar
or identical to Isospora, in cats. Sarcocystis, named from its
cysts found in sheep, and occasionally, human, muscle, is a
related Isospora, with a sporogony stage in dogs. Cryptosporidium, whose spores find their way into drinking water,
and which has caused recent health scares, is another
coccidian. The group also includes some blood parasites
which have coccidian features in their life cycle; these
include Haemogregarina and Lankesterella, found in lower
vertebrates, but with vector stages in invertebrates that are
usually eaten by the vertebrate, although some inject
parasites with saliva.
The apical complex of infective cells of haematozoeans
lacks the conoid or polar rings. The sporozoites develop in
blood-sucking arthropods and are injected as naked cells
into the vertebrate 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 fertilization to form a migratory zygote, whose growth and
sporogony produces many sporozoites. Members of both
orders of haematozoeans are important parasites. Those in
the order Haemosporida are transmitted by dipteran flies.
The best known examples of this group are malarial
parasites belonging to the genus Plasmodium, several
species of which are transmitted between humans by
mosquitoes; other species are found in other mammals and
birds. Leucocytozoon and Haemoproteus are genera found
in birds and reptiles and transmitted by midges and
blackfly. Important members of the order Piroplasmida,
which are transmitted by ticks, belong to the genera
Babesia and Theileria. These are responsible for serious
diseases of domestic animals throughout the world, and
generally only cause human disease in cases of immune
deficiency or removal of the spleen.
Cavalier-Smith (1998) has included within the Sporozoa
several genera of other spore-producing protozoa (Paramyxa, Haplosporidium and Metchnikovella), formerly
classed elsewhere in independent groups, or as microsporidians. These are parasites of invertebrates; their phylogenetic relationships remain to be firmly established.
The phylum Ciliophora
The characteristics of ciliates and the composition of this
phylum have been comprehensively described by Corliss
(1979). They have been classified in many different ways,
generally on the basis of the arrangement of cilia on the
general body surface and in the region of the cell mouth
(cytostome). In a recent scheme Corliss (1994) divided this
phylum into eight classes, following ultrastructural studies
and extensive discussion by many authors. This scheme is
likely to change when the results of rRNA analysis are also
taken into account; at present the molecular sequences of
too few species have been studied (Hirt et al., 1998) to
propose more than small changes to the scheme put
forward by Corliss.
Members of the class Karyorelictea are probably the
most primitive surviving ciliates and are unusual in
possessing nondividing, diploid macronuclei and generally
lacking pellicular alveoli; they are often long, but flattened,
ciliates, mostly from marine sands. Within the class
Polyhymenophora, all of which have a conspicuous row
of large membranelle cilia associated with the cytostome,
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Alveolates
P
M
M
(b)
(c)
C
(d)
(a)
(e)
Figure 4 Examples of the Ciliophora. (a) Stylonychia (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) Didinium (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 soil ciliate Colpoda (about 75 mm long).
the subclass Heterotrichia, which also have a full body
covering of ciliary rows, appear from rRNA analysis to be
closely related to karyorelicteans. Members of several
genera of heterotrich ciliates are commonly encountered,
probably the best known are the large species of the
trumpet-shaped Stentor and the cylindrical Spirostomum,
which commonly reach 2 mm in length; Metopus species
are anaerobes and Nyctotherus is a common symbiont in
the gut of amphibians.
The other subclass of polyhymenophorans are the
Spirotrichia, apparently more-evolved ciliates that have
few body cilia, often grouped into compound cirri; this
group includes several well-known ciliates that ‘run’
around over surfaces, e.g. Stylonychia (Figure 4a), and
Euplotes and Aspidisca, both of which are common in fresh
and salt water and important consumers of bacteria in
sewage treatment works, as well as important planktonic
‘oligotrich’ ciliates like Strombidium (Figure 4b) and the
tintinnids, whose cup-shaped or cylindrical loricas are
abundant in plankton samples. A second group at this
intermediate level of evolution, according to rRNA
evidence, is the class Litostomatea, including forms with
very simple, or even lacking, mouth cilia; it includes
Balantidium, the only ciliate parasitic in humans, ciliates
which inhabit the rumen of ruminant 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.
The first group to separate at the more advanced level of
evolution appears to be the class Phyllopharyngea,
characterized by the possession of ribbons of microtubules
around the cytopharynx leading into the cytoplasm from
the cell mouth, e.g. Chilodonella or chonotrichs, or from
the multiple mouths of the suctorians, e.g. Acineta,
6
Podophrya (Figure 4d). Some forms have a prominent
cytopharyngeal basket of microtubular rods, which is also
present in a related class, the Nassophorea, e.g. Nassula,
some of which ingest filamentous algae. Close to these two
classes is the class Colpodea, most of whom, like the
ubiquitous Colpoda species (Figure 4e), are found in soils, at
least as cysts.
Most of the remaining ciliates belong to the class
Oligohymenophorea, named from the presence of a small
number (3–4, commonly) of membranelles or comparable
compound cilia around the mouth, and rows of body cilia.
Among the six subclasses, the Hymenostomatia, e.g.
Tetrahymena, the protozoan most studied by biochemists,
the Peniculinia, e.g. the familiar Paramecium species and
the Peritrichia, e.g. Vorticella and Carchesium, well-known
and extremely important bacterivores in sewage treatment
systems, all have important places. Of the other three
subclasses, the Astomatia are endoparasites, mostly in
annelids and the Apostomatia are mostly ectoparasites on
crustaceans, but the Scuticociliatia are often abundant
bacterivorous forms with few cilia, e.g. Uronema, Pleuronema. The final class, the Prostomatea, contains ciliates
with an anterior mouth and simple mouth ciliature, which
are often predatory or detritivores.
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Kreier JP and Baker JR (1987) Parasitic Protozoa. Winchester, MA:
Allen and Unwin.
Sleigh MA (1989) Protozoa and Other Protists. Cambridge: Cambridge
University Press.
Smith DC and Douglas AE (1987) The Biology of Symbiosis. London:
Edward Arnold.
Taylor FJR (ed.) (1987) The Biology of Dinoflagellates. Oxford:
Blackwell.
Wilson RJM (1998) Plastid-like DNA in apicomplexans. In: Coombs
GH, Vickerman K, Sleigh MA and Warren A (eds) Evolutionary
Relationships Among Protozoa, pp. 293–304. London: Chapman and
Hall.
Further Reading
Anderson OR (1987) Comparative Protozoology. Ecology, Physiology,
Life History. Berlin: Springer.
Coombs GH, Vickerman K, Sleigh MA and Warren A (eds) (1998)
Evolutionary Relationships Among Protozoa. London: Chapman and
Hall.
Grell KG (1973) Protozoology, 3rd edn. Berlin: Springer.
Hausmann K and Hülsmann N (1996) Protozoology, 2nd edn. Stuttgart,
Germany: Thieme.
Kudo RR (1996) Protozoology, 5th edn. Springfield, IL: Thomas.
Lee JJ, Hutner SH and Bovee EC (eds) (1985) An Illustrated Guide to the
Protozoa. Lawrence, KS: Society of Protozoologists.
Levine ND (1988) The Protozoan Phylum Apicomplexa. Boca Raton,
FL: CRC Press.
Puytorac P de, Grain J and Mignot J-P (1987) Precis de Protistologie.
Paris: Boubée.
Sleigh MA (1989) Protozoa and Other Protists. Cambridge: Cambridge
University Press.
ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
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