Zool. J . Linn. Soc., 58: 61-77
January 1976
A revised classification of the Gymnamoebia
(Protozoa: Sarcodina)
FREDERICK C. PAGE F.L.S.
Culture Centre of Algae and Protozoa, 36 Storey's Way, Cambridge, CB3 ODT
Accepted for publication March I975
A revised classification of the naked amoebae is proposed o n the basis of a synthesis of many
kinds of information presently available for taxonomic purposes above the species level. These
amoebae, constituting the subclass Gymnamoebia within the class Lobosea, superclass
Rhizopoda, include not only strictly lobose amoebae but also those with more o r less filose
subpseudopodia produced from a broader hyaline lobe. The subclass is divided into t h e orders
Amoebida, Schizopyrenida, and Pelobiontida, and suborders are recognized within the order
Amoebida. Although the Gymnamoebia are undoubtedly heterogeneous and polyphyletic and
the proposed classification is intended chiefly as a practical system with a logical basis, there are
a few suggestions of natural relationships.
CONTENTS
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Introduction
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A proposed new classification
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Explanatory comments
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General discussion
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Acknowledgements
References
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INTRODUCTION
Before a comprehensive taxonomic system can be constructed for the naked,
non-aggregative, non-spore-forming amoebae, one must answer the same
question which is posed in determining taxa at the generic and specific levels:
What are valid criteria for the taxonomy of amoebae? This question has been
discussed in previous publications (Page, 1967, 1968, 1972a, b, 1974, 1975) and
by other authors (Jahn & Bovee, 1965; Bovee & Jahn, 1965, 1966; Jahn, Bovee
& Griffith, 1974; Pussard, 1973; Singh, 1952; Singh & Das, 1970). I t is not my
purpose t o repeat the detailed history of this problem, which will be found
particularly in Page (1967), but it will be discussed briefly in general terms in
relation to the broad systems which have been proposed.
Briefly, the major criteria on which higher taxa for amoebae have been based
are: (1) locomotive form and behaviour, (2) occurrence or absence of a
flagellate stage, (3) nuclear structure, and (4) mitotic patterns. This summary
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62
assumes that a formal high-level separation of amoebae with tests and those
without tests is already accepted, an assumption challenged by Bovee & Jahn
(1965) but accepted in the present classification for reasons which will be
discussed later.
Besides these major criteria, others have often been recognizcd in determining the position of a particular group and will be noted at appropriate
places.
Nineteenth-century systems for the amoebae were quite simple and
depended on gross appearance, though Leidy’s system (Leidy, 1879), based on
careful observations, distinguished clearly between two suborders, Protoplasta
Lobosa and Protoplasta Filosa, each, as Bovee & Jahn (1965) have pointed out,
including both testate and naked organisms. Penard, one of the principal
investigators at the turn of the century, did not formulate a system (Penard,
1902) and, indeed, considered the erection of new genera not yet possible.
Cash (1905) recognized the subclass Rhizopoda as consisting of the orders
Amoebina, naked amoebae, and Conchulina, testate amoebae. The system of
Poche (1913) does not merit mention but must occasionally be referred to as
the source of a name protected by the law of priority or as an instrument for
the perpetuation of error. Probably no protozoologist today would dispute
Corliss’s description of Poche as a “well-known armchair taxonomist” (Corliss,
1972).
Table 1. System of Schaeffer ( 1926)
Class Rhizopoda
Order Lobosa
Suborder Amoebaea
Family Trimastigamoebidae
(Trimastigamoeba, Vahlkampfia, Guttulidium)
Family Chaidae
(Trichamoeba, Endamoeba. Polychaos, Metachaos, Chaos, Pelomyxa)
Family Mayorellidae
(Flabellula, Mayorella, Vexillifera, Stnolatus, Astramoeba, Dactylosphaerium, Dinamoeba,
Pon tifex)
Family Thecamoebidae
(Rugipes, Thecamoeba)
Family Hyalodiscidae
(Wnda, Hyalodiscus, Gibbodiscus, Flamella, Cochliopodium)
Schaeffer (1926) was the first actual investigator of amoebae (thus excluding
Poche) to offer a detailed system, though he did not attempt to include all the
smaller amoebae. His system (Table 1) was based on wide and perceptive
observations of freshwater and marine amoebae. His guiding principle was,
“The object of systematics in this group is of course to classify amebas, not
nuclei,” enunciated in opposition to the “rather wide-spread notion that
amebas are shapeless” and the “attempts to classify amebas wholly with respect
to the nucleus.” Schaeffer did not reject the use of nuclear structure and
mitotic patterns in the taxonomy of amoebae, a degree of breadth and
perceptiveness lacking in some workers before and since his time, particularly
those to whom the nucleus is the only or decisive criterion.
A REVISED CLASSIFICATION OF NAKED AMOEBAE
63
A quarter of a century later Chatton (1953) attempted to unite Schaeffer’s
system and the various contributions of nuclear taxonomists into a single
scheme (Table 2), to which he himself made some contributions, without,
however, reconciling the inconsistencies of the two sources. I t will be noted
that the criterion on which Chatton based his first dichotomy was the
occurrence or absence of a flagellate stage.
Table 2. System of Chatton (1953)
Superclass Rhizopoda
Class Lobosa
Order Amoebaea
Suborder Mastigogenina (with flagellated stage)
Family Mastigamoebidae
(Mastigamoeba, Mastigina, Mastigella)
Family Paramoebidae
(Paramoeba, Janickina)
Family Vahlkampfiidae
(Vahlkampjia, Tetramitus)
Family Dientamoebidae
(Dientamoeba. Histomonas)
Suborder Amastigogenina (without flagellated stage)
Family Chaosidae
(Chaos, Trichamoeba, Pelomyxa)
Family Thecamoebidae
(Thecamoeba, Rugipes)
Family Hyalodiscidae
(Unda, Hyalodiscus)
Family Hartmannellidae
(Hartmannella, Acan thamoeba, Glaeseria)
Family Mayorellidae
(Flabellula, Mayorella, Vexillifera, Astramoeba, Dinamoeba, Hydramoeba)
Family Endamoebidae
Subfamily Endarnoebinae
(Endamoeba)
Subfamily Entamoebinae
(Entamoeba, Endolimax)
Family Pansporellidae
(Pansporella. Branchipocola, Liegeoisia)
Jepps (1956) did not propose a system beyond subdivision of the order
Amoebaea into the suborders Amoebaea Nuda and Amoebaea Testacea. The
systems employed by Grospietsch (1958) and Harnisch (1959) were
compilations from the literature, and Lepgi’s (1960) sketchy classification
above the generic level can hardly be called a system. The system of Loeblich &
Tappan (1961) was similar t o that of Chatton both in making the occurrence of
a flagellate stage the basis of the first dichotomy and in the families recognized.
Both these systems perpetuated a serious error of Poche’s at the family level, to
which further reference will be made.
To the present day the old controversy between nuclear and pseudopodial
schools of taxonomy has been kept warm, with the current phase dating
approximately from the earlier papers of Singh (1951, 1952) and Bovee
(1953). The position of the present-day nuclear taxonomists is summarized by
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Singh & Das (1970): “The suggested classification is based on the nuclear
structure, mode of nuclear division and possible phylogenetic relationship.”
“Classification of amoebae based on form, locomotion and pseudopodial
characters and on parasitic or free-living nature is of no probable phylogenetic
value.” (No taxonomist today suggests that the parasitic mode of life is in itself
of any great value as a taxonomic criterion.) Pussard, who opposes Singh & Das
on some points and examines the diverse mitotic patterns much more closely,
nevertheless considers nuclear structure and mitotic division to be of primary
importance and to be more objective than criteria involving locomotive form
and behaviour (Pussard, 1973). Bovee considers locomotive form and behaviour
to be the principal criterion for specific and generic distinctions. though he
does not rule out serious consideration of other criteria. “Interphase nuclei,
mitotic figures, or cysts would have no more validity alone, and more likely less
validity than pseudopodial morphologies alone, to distinguish species and
genera of naked lobose amebas. Certainly wherever possible all should be
described” (Bovee, 1970). On the higher levels, Bovee and Jahn have advocated
dividing the Sarcodina as a whole on the basis of what they consider the two
fundamental modes of locomotion, a “contractile-hydraulic” and an “active
sliding” system (summarized in Jahn, Bovee & Griffith, 1974). All the
organisms considered in the present paper would fall into their class Hydraulea,
with locomotion by the contractile-hydraulic mode.
The systems of Singh & Das and Bovee & Jahn are presented in summary in
Tables 3 and 4 . (Families of testate amoebae are omitted from the Bovee &
Jahn classification.) Criticisms of these systems are reserved for the Discussion.
Table 3. System of Singh & Das (1970). (Original version in Singh, 1952)
Order Amoebida
Family Schizopyrenidae
Resting nucleus with a Feulgen-negative nucleolus or several Feulgen-negative nucleoli, which form
“polar masses” during mitosis. Nuclear membrane persisting throughout mitosis, during which
“interzonal bodies” may be present. Some genera may produce a flagellate stage
(Schizopyrenus?Naegleria, Didascalus, Tetramitus, Trimastigamoeba, Heteramoeba, Sappinia)
Family Hartmannellidae
Resting nucleus with a single Feulgen-negative nucleolus or several nucleoli. Nucleolus or nucleoli
disappear during mitosis and a spindle with an equatorial plate develops. Nuclear membrane
disappears during mitosis. No flagellate stages known
(Hartmannella, Amoeba, Pelomyxa, Dobellina)
Family Endamoebidae
Resting nucleus with Feulgen-positive karyosome or Feulgen-positive chromatin granules
Feulgen-negative granules or nucleoli d o not give rise to polar masses in mitosis; nuclear membrane
always intact during mitosis
(Entamoeba, Endamoeba, Hydramoeba)
In the course of preparing a key to freshwater and soil amoebae (Page,
1976), it became apparent that proposal of a system for amoebae based on the
taxonomic criteria which were the theoretical prerequisite for that key could
not be delayed. At the same time, a large number of workers were being
consulted for their opinions on an overall revision of the Sarcodina as part of a
new classification of the Protozoa sponsored by the Society of Protozoologists.
A REVISED CLASSIFICATION O F NAKED AMOEBAE
65
Table 4. Bovee & Jahn system abridzed from Jahn, Bovee & Griffith
(1974). (Originally published in Jahn & Bovee, 1965;
Bovee & Jahn, 1965 1966)
Class Hydraulea
Subclass Cyclia
Superorder Lobeda
Order Granulopodida
Pseudopodia hemispherical o r cylindrical, granule-filled
Suborder Tubulina
Pseudopodia cylindrical, of indeterminate length, one employed as principal avenue of
progress; granular, with clear hemispherical tip ("hyaline cap")
Family Amoebidae
(Amoeba, Chaos, Hydramoeba, Metachaos, Polychaos)
Suborder Limacina
Blunt t o elongately limaciform or bag-like in locomotion; pseudopodia eruptive,
hemispherical, granule-filled, or as granular hemispheroid non-eruptive bulges; radiate
state (if present) granule-filled, or as granual hemispheroid non-eruptive bulges; radiate
state (if present) with tubular, granule-filled pseudopodia
Family Pelomyxidae
(Pelomyxa, Trichamoeba)
Family Saccamoebidae
(Saccamoeba)
Order Hyalopodida
Pseudopodia clear, nongranular, usually determinate in length, arising from clear
antero-lateral border in locomotion, or from the body surface, or both
Suborder Eruptina
Pseudopodia eruptive, hemispherical, melding into clear anterior border; also may form
filose pseudopodia from body surface; body ovate, trapezoidal, or limaciform in
locomotion
Family Hartmannellidae
Subfamily Hartmannellinae
(Acanthamoeba, Didascalus, Glaeseria, Hartmannella, Hartmannina, Naegleria,
Pansporella, Rosculus, Sappinia. Schizopyrenus, Trimastigarnoeba)
Subfamily Endamoebinae
(Endamoeba)
Suborder Conopodina
Pseudopodia clear, conical, at least for the distal portion, with rounded ends
Family Mayorellidae
Subfamily Mayorellinae
(Dinamoeba, Flagellipodium, Mayorella, Pontifex, Striolatus, Triaenamoeba,
Vexillifera)
Subfamily Oscillosigninae
(Oscillosignum, Subulamoeba)
Family Flabellulidae
Subfamily Flabellulinae
(Flabellula. Flamella)
Subfamily Flabellulinae
Gibbodiscus, Wnda, Vannella)
Family Cochliopodiidae
(Cochliopodium, Gocevia)
Order Thecida
Body with thick, clear, ectoplasmic layer; rarely form pseudopodia other than short, blunt
bulges
Suborder Rugina
Large amoebae with heavy, much-wrinkled ectoplasm in locomotion; wrinkles dorsal,
more or less parallel; pseudopodia only as blunt bulges
Family Thecamoebidae
(Thecamoeba)
Suborder Striatina
Small amoebae with distinct parallel dorsal longitudinal ridges in locomotion; pseudopodia
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66
Table 4-(cont. )
rarely formed. then only as blunt bulges
Family Striamoebidae
(Striamoeba, Rugipes, Platyamoeba)
Suborder Discina
Body more or less oval, without or with very faint ridges; pseudopodia rarely formed,
then only as blunt bulges
Family Discamoebidae
(Discamoeba)
The revised classification for the amoebae sensu strict0 (=order Amoebida in
Honigberg et al., 1964) is being published in the new key (Page, 1976), but it is
presented here in more detail with the explanatory comments which cannot be
included in such a key. The version which will appear as a part of the
comprehensive Protozoa classification will be the result of collective decisions
and may vary from that proposed here, and the committee preparing the new
Protozoa classification does not share any responsibility for the present system.
Colleagues whose replies to correspondence on that project were especially
helpful in the classification of the Gymnamoebia are acknowledged in a later
section.
From the diagnoses of the taxa it will be apparent that no single criterion
was considered in isolation, and it will be just as apparent that the character of
locomotive form/behaviour was of special importance. This is a complex
character, both morphological and physiological, and it cannot be emphasized
too strongly that no valid classification of amoebae is possible without
extensive examination of living organisms. The other criteria listed in the
second paragraph of this Introduction were also given major attention. The
diagnoses give some evidence of the employment of other characters, and even
when not specifically mentioned, such information as is available on
ultrastructure, nutrition, and immunology has been considered, though much
of it is still helpful only in specific and generic distinctions. Special attention
has been given to correlations between apparently independent characters, such
as locomotive form/behaviour on the one hand and mitotic pattern on the
other. Further justification for details of the classification is offered in the
Explanatory Comments.
A PROPOSED N E W CLASSIFICATION
Kingdom PROTISTA Haeckel, 1866
Subkingdom PROTOZOA Goldfuss, 1818;emend. von Siebold, 1845
Phylum SARCOMASTIGOPHORA Honigberg & Balamuth, 1963
Subphylum SARCODINA Hertwig & Lesser, 1874
Superclass RHIZOPODA von Siebold, 1845
Locomotion associated with formation of lobopodia, filopodia, or
reticulopodia, or with protoplasmic flow without production of discrete
pseudopodia; no sorocarps, sporangia, or similar fruiting bodies,
Class LOBOSEA Carpenter, 1861
A REVISED CLASSIFICATION O F NAKED AMOEBAE
67
Pseudopodia lobose, or more or less filose but produced from a broader
hyaline lobe, not anastomosing; usually uninucleate; multinucleate forms
not as flattened or much-branched plasmodia.
Subclass GYMNAMOEBIA Haeckel, 1862
Without test.
Order AMOEBIDA Kent, 1880
Typically uninucleate; mitochondria typically present; no true
bidirectional flow of cytoplasm; no flagellate stages known.
Suborder TUBULINA Bovee & Jahn, 1966; emend.
Body a branched or unbranched cylinder, with hyaline cap present
or absent; nuclear division mesomitotic.
Family AMOEBIDAE Diesing, 1848
Usually polypodial, with pseudopodial tips hemispherical and
usually with hyaline cap, and with pseudopodia of radiate
floating form granular for most of length, not tapering strongly;
usually with granular nucleus ; if usually monopodial in
locomotion, then with nucleus, locomotive pseudopodia, and
floating form characteristic of family.
(Amoeba,
Polychaos,
Chaos,
Trichamoeba, possibly
Hydramoeba. )
Family HARTMANNELLIDAE Volkonsky, 193 1 ; emend. Page,
1974
Monopodial (limax) amoebae with locomotion by generally
steady flow, sometimes with gentle hemispherical bulging to
either side at anterior end; with vesicular nucleus; cysts, if
formed, uninucleate, in one genus often binucleate.
(Hartmannella, Glaeseria, Saccamoeba. Cashia, R hizamoeba.)
Family ENTAMOEBIDAE Chatton, 1925
Monopodial amoebae with endosome a small granule or cluster
of granules; mature cyst, if cyst occurs, usually with 4, 8, or
more nuclei produced by divisions within cyst; all known
species except one parasitic.
(Entamoeba, Endamoeba, Iodamoeba, Endolimax.)
Suborder THECINA Bovee & Jahn, 1966; nom. transl.
Flattened, often oblong, ovate, or flabellate and more or less
regular in outline; often with extensive hyaline zone; often with
discernible pellicle-like layer which may be distinctly wrinkled ;
rolling movement of surface in locomation, with most species
never showing any branching; nuclear division patterns diverse.
Family THECAMOEBIDAE Schaeffer, 1926
With characters of the suborder.
(Thecamoeba, Sappinia, Platyamoeba, Pessonella, Vannella.)
Suborder FLABELLINA subord. nov.
Flattened, broad, with extensive hyaline zone but no obvious
pellicle-like layer; sometimes discoid ; locomotion often
accompanied by gentle eruption or by rolling activity of entire
cytoplasm; nuclear division where known mesomito tic.
Family FLABELLULIDAE Bovee, 1970
No sub-pseudopodia produced during normal locomotion; often
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F. C. PAGE
irregular and rapidly-changing form, sometimes spatulate or
flabellate, and often with eruptive cytoplasmic flow.
(Flabellula, Rosculus.)
Family HYALODISCIDAE Poche, 191 3 ; emend.
Fairly regularly discoid or somewhat fan-shaped, with breadth
usually greater than length; with central, post-central or
posterior granular hump surrounded completely or anteriorly
and laterally by flattened hyaline border; sometimes with
narrowly conical hyaline projections or subpseudopodia; rolling
movement often apparently involving entire cytoplasm; no
tectum of scales.
(Hyalodiscus, Flamella. 1
Suborder CONOPODINA Bovee & Jahn, 1966; emend.
Digtiform or mamilliform, usually bluntly conical, hyaline
subpseudopodia usually produced from a broader hyaline zone;
locomotive form with length almost always greater than breadth,
not discoid; floating form often but not always radiate with
slender, finely tipped hyaline pseudopodia; seldom forming cyst;
nuclear division typically mesomitotic but with possible polar
structures in some species.
Family PARAMOEBIDAE Poche, 191 3 ; emend.
With the characters of the suborder.
(Para m o eba,
May orella,
Vexillifera,
Subulamoeba,
Oscillosignum, Dinamoeba, possibly Pontifex and others.)
Suborder ACANTHOPODINA subord. nov.
More or less finely tipped, sometimes filose, often furcate hyaline
subpseudopodia produced from a broader hyaline zone; not
regularly discoid, though sometimes expanded on substratum;
usually forming cysts; nuclear division mesomitotic or
metamitotic.
Family ACANTHAMOEBIDAE Sawyer & Griffin, 1975
Several to many subpseudopodia (acanthopodia), usually
pointed but sometimes blunt; outline of amoeba in locomotion
oval, more or less triangular, elongate, or irregular; extranuclear
centrospheres reported; cysts polyhedral or thickly biconvex,
with cellulose-containing wall consisting of more or less
polygonal or stellate endocyst and more or less rippled ectocyst;
excystment by removal of operculum at point of contact
between endocyst and ectocyst.
(Acanthamoeba.)
Family ECHINAMOEBIDAE Page, 1975
Several to many finely-pointed subpseudopodia, either filiform
or spiny; amoebae more or less flattened in locomotion but not
with a hyaline border around entire periphery; known species
cyst-forming, but not with endocyst polygonal or stellate, and
not excysting by removal of operculum.
(Echinamoeba, Stachyamoeba, Filamoeba.
Order SCHIZOPYRENIDA Singh, 1952; nom. transl.
Body a monopodial cylinder (limaciform). usually moving with
A REVISED CLASSIFICATION OF NAKED AMOEBAE
69
more or less strongly eruptive, hyaline, hemispherical bulges;
typically uninucleate; nuclear division promitotic; temporary
flagellate stages common.
Family VAHLKAMPFIIDAE Jollos, 1917; Zulueta, 1917
With the characters of the order.
( VahEkampJia,
Naegleria,
Adelphamoeba,
Tetramitus,
Heteramoeba.)
Order PELOBIONTIDA ord. nov.
Body a thick cylinder or elongate ovoid, monopodial, with true
bidirectional fountain flow of cytoplasm common; typically
multinucleate; lacking mitochondria but with symbiotic bacteria;
often containing mineral particles and plant matter; in
micro-aerobic habitats; no flagellate stage known.
Family PELOMYXIDAE Schulze, 1877
With the characters of the order.
(Pelomyxa.)
EXPLANATORY COMMENTS
The proposed revision is presented in abbreviated form in Table 5 .
The raising of taxonomic ranks at upper levels is in accordance with the
current trend and likely future practice for the Protozoa. Corliss (1974) now
considers the Ciliophora a separate phylum of protistans, and the
Sarcomastigophora are here, as in the past (Honigberg et al., 1964) regarded as
of equal rank. Despite recognition of a separate kingdom Protista,
Table 5 . Proposed revised classification (genera listed in text)
Phylum Sarcomastigophora
Subphylum Sarcodina
Superclass Rhizopoda
Class Lobosea
Subclass Gymnamoebia
Order Amoebida
Suborder Tubulina
Family Amoebidae
Family Hartmannellidae
Family Entamoebidae
Suborder Conopodina
Family Paramoebidae
Suborder Acanthopodina
Family Acanthamoebidae
Family Echinamoebidae
Suborder Flabellina
Family Flabellulidae
Family Hyalodiscidae
Suborder Thecina
Family Thecamoebidae
Order Schizopyrenida
Family Vahlkampfiidae
Order Pelobiontida
Family Pelomyxidae
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F. C. PAGE
protozoologists are likely t o continue their adherence to the International Code
of Zoological Nomenclature (1964) as does Corliss (1974). Separation of
Mastigophora and Sarcodina into separate phyla would not seem justified, since
they show more mutual affinities than either does to other protozoan groups.
so that there are cases where the alternative position of a taxon in the
Sarcodina or the Mastigophora can be argued either way with good reason.
At a somewhat lower level, though various groups of testate amoebae are
very probably derived from different groups of naked amoebae, the
connections are still so far from clear that it seems best to retain for the time
being the separation of testate and naked amoebae at a higher level than the
familial. The family Cochliopodiidae can with justification be placed into either
group. For putting it into the naked amoebae, one can point out that. just as
ultrastructurally complex scales have been demonstrated in Cochliopodium
(Bark, 1973), so they have also been found in certain organisms that no one
considers other than naked amoebae (Grell & Benwitz, 1966; Pennick &
Goodfellow, 1975). However, certain species of Cochliopodium have spines
visibly light-microscopically. The scales of Cochliopodium constitute a tectum
(Bark, 1973), which as a whole forms a flexible, light-microscopically visible,
doubly-contoured covering which is absent over all or the greater part of any
pseudopodia as well as over the advancing edge of the amoeba while the scales
of those Paramoeba and Mayorella species possessing them cover even the tips
of the pseudopodia and cannot be detected light-microscopically (personal
observations), though they may have a diameter of 0.5 pm; apparently the
fineness of their constituent parts does not permit the whole t o be resolved
with the light microscope. Since some undoubted members of the genera
Mayorella and Paramoeba lack scales, they cannot be placed into the testate
amoebae by any argument. Those who wish to consider the Cochliopodiidae
naked amoebae might place them into the suborder Flabellina in the present
classification or erect a separate suborder. Some species of Cochliopodium have
a radiate floating form with fine, hyaline pseudopodia similar to those of
several species of Mayorella and Paramoeba, but floating forms of this kind
have been found useful only as one taxonomic criterion among others and
occur in genera which otherwise do not appear closely related.
For the naked amoebae Haeckel’s term Gymnamoebia has been resurrected.
Restriction of the junior term Amoebida to one of the three orders will be
discussed in the next section.
An extensive explanation of terms will be found in Page (1976), but a few
essential definitions are given here. The vesicular nucleus, the most common
kind in amoebae, has a single, usually central, nucleolus (endosome,
karyosome). Some vesicular nuclei have two or three nucleolar bodies arranged
around the periphery of the nucleus. In some larger amoebae, the apparent
nucleolar material consists of many small particles or granules, often arranged
just inside the nuclear membrane; these are the granular nuclei of the
classification. The terms promitosis, mesomitosis, and metamitosis are used as
defined by Page (1969): In promitosis the nucleolus divides into two polar
masses during mitosis, and the nuclear membrane persists throughout division.
Mesomitosis is like that of metazoan cells, except that centrioles of any kind
are absent; the nuclear membrane may persist at least through metaphase or
may disappear in prophase. Metumitosis is like the pattern of metazoan cells,
A REVISED CLASSIFICATION O F NAKED AMOEBAE
71
with the presence, if not of centrioles with the classical ultrastructure, then at
least of morphologically detectable polar units such as “centrospheres.” Such
bodies have been reported in some species of Acanthamoeba (Pussard, 1964,
1966; Bowers & Korn, 1968). Pussard (1973) has recently re-defined the
categories of mitotic patterns, but the definitions given above are those
employed in this classification.
A few comments are needed regarding certain groups.
In the order Amoebida, the position of the Entamoebidae is uncertain. We
do not have enough information about their possible relationships to other
amoebae or the relationships among genera within the family t o go beyond the
present definition, based largely on parasitic habit and nuclear division within
the cyst. (Glaeseria, family Hartmannellidae, often has binucleate cysts
resulting from division during encystment, but it has distinct similarities to
other hartmannellids. Other genera, particularly vahlkampfiids, may have cysts
with two or more nuclei simply as the result of encystment of cells with
supernumerary nuclei.)
The family Paramoebidae includes the Mayorellidae Schaeffer, 1926. See
Page (1972a) for union of the families, where the inaccuracy of Poche’s (191 3)
concept of the family Paramoebidae is discussed, an error perpetuated, though
excusably, in the classifications of Chatton (1953) and Loeblich & Tappan
(1961). The union of these families in 1972 was based on locomotive
form/behaviour, mitotic patterns, and floating forms, and the subsequent
finding of scales on several species of Mayorella similar to those of Paramoeba
eilhardi (Pennick & Goodfellow, 1975; Pennick, pers. comm.) has provided
further evidence of a connexion and a striking example of correlation among
apparently independent characters.
The Hyalodiscidae are another family about which too little is known, and
both the composition and the position of the family are still rather uncertain.
The association of Hyalodiscus and Flamella is based on certain apparent
similarities in locomotive mechanisms, as described by Bovee (1956) in
Flamella and Haberey & Hiilsmann (1973) in Hyalodiscus. There is no good
reason to group Hyalodiscus and the Hyalodiscidae with the Vampyrellidae as
was done by Poche (191 3) but not by Schaeffer (1926).
The name of the order Schizopyrenida by elevation of Singh’s familial name
(Schizopyrenidae Singh, 1952) is intended to preserve a most apt descriptive
coinage for the promitotic division pattern characteristic of this group, though
Singh’s genus Schizopyrenus is considered a junior synonym of Vahlkampfia
and the familial name derived from the latter genus is retained. (The status of
the name Vahlkampfia was confused by several errors and inconsistencies early
in the century.) These amoebo-flagellates are placed into the Sarcodina rather
than the Mastigophora because their principal phase is the amoeboid one.
Further remarks about their possible relationships will be found in the next
section. I t should be noted that the listing of Sappinia in the family
Schizopyrenidae by Singh & Das (1970) on the basis of its supposed promitotic
division is unjustified. Their statement that Nzgler’s (1909) cytological work on
S. diploidea was “very poor” is equally unjustified, since that work agrees well
with recent good haematoxylin preparations of that species (Goodfellow,
Belcher & Page, 1974), which Singh & Das do not appear to have investigated
at first hand. These preparations show a pattern of nuclear division in which
72
F. C . PAGE
the nucleolus does indeed elongate as in promitosis but other aspects differ
greatly from vahlkampfiid mitosis. In the present classification (as in some
others) Sappinia is in the Thecamoebidae. Some other members of that family
(e.g., several species of Platyamoeba and at least one of Thecamoeba) also form
pseudo-aggregative mounds when cells are abundant in a culture (pers. obs.),
one of the characters which has led some authors t o consider Sappiniu close to
the cellular slime moulds.
The order Pelobiontida is known to contain only the genus Pelomyxa, which
may itself contain only a single polymorphic species. Pelomyxa appears unique
in its locomotive pattern, possibly its method of feeding and the variety of
material (including mineral particles) which it ingests, and (among free-living
non-marine amoebae) its lack of a contractile vacuole. The absence of
mitochondria and the micro-aerobic way of life are unique among larger
amoebae and unusual among free-living amoebae in general. Lumping of the
multinucleate Chaos carolinense with this genus is untenable in view of today’s
knowledge of locomotion and cytological characteristics. The position given to
Pelomyxa and the Pelobiontida and their diagnoses are based on the
ultrastructural work of Daniels & Breyer (1967) and Andresen,
Chapman-Andresen & Nilsson (1968) and on the investigation of locomotion
by Griffin (1964) and personal observations. These can be compared with the
characters of Chaos in the publications of Andresen (1956, 1973), Griffin
(1964), and Daniels (1973).
GENERAL DISCUSSION
The time is appropriate for a revision embodying recent advances in
knowledge of the amoebae, and practical reasons alone would justify such a
revision at this time. To give only one example, several genera of very common
free-living amoebae have been implicated as human pathogens, and the notion
that some of these quite diverse genera are closely related can hardly be helpful
in investigating their characteristics.
This classification is the first one derived from a synthesis of so many kinds
of available data. The basic principle has been simply to use as much
information and as many kinds as possible, rather than ruling out certain kinds
on dogmatic grounds. I t has not been possible to apply this principle of
synthesis evenly over the entire range of Gymnamoebia because the
information available differs quantitatively and qualitatively from group to
group. Also, as mentioned earlier, some of the newer methods have thus far
been applied only at the specific and, at times, the generic levels. The present
revision is therefore only a first step in applying such a diversity of
information.
All such systems are provisional, intended to present in organized form the
picture which can be built up from our understanding at a given time. This is
especially true of groups whose taxonomy is so slightly developed as in the
Gymnamoebia. Each system will, it is hoped, be more useful and perhaps even
more accurate than its predecessors. We can hope that the next system will
benefit from the application of numerical taxonomy, which though invoked by
name a decade ago, has for the first time been actually applied to a small group
of amoebae by Friz (1974). Some promising characters at lower taxonomic
A REVISED CLASSIFICATION OF NAKED AMOEBAE
73
levels include ultrastructural studies of the cell surface, such as those of Grell &
Benwitz (1966), Bark (1973), and Pennick & Goodfellow (1975).
Immunological investigations such as those pursued by a fair number of
workers should also be applied to comparisons between amoebae which by
other criteria are not related at the generic or familial level, and the same can
be said of the studies of DNA base composition pioneered, for amoebae, by
Adam & Blewett (1974 and earlier papers). A better understanding of the
classical criterion of mitotic pattern is promised by the painstaking and
ingenious investigations on living material by Pussard.
Of the two principal systems advocated today, one is struck at first glance by
the apparent simplicity of the Singh & Das system and the apparent complexity
of the Bovee & Jahn system. Most workers consider these schemes to be at
extreme poles, but it would be an error to assume that a “correct” system is to
be found by following the ancient wisdom of the via media, nor is the synthetic
(or multiple-character) approach advocated here to be seen as such a search for
a mean. Of the Singh & Das system, it must first be said that it rejects most of
the available information, and second that it is based on investigations of a very
limited range of amoebae. Many quite different organisms are grouped together
as a result of these two basic weaknesses. The unsupported repetition of the old
allegation that locomotive form/behaviour is useless defies much evidence to
the contrary, such as that now gathered together in the photographic
illustrations of Page (1976). Despite some good studies of mitotic patterns and
some valuable non-taxonomic contributions by these authors, it must be said
that their system is supported more by polemics than by data.
Although the system here advocated is indebted to the work of Bovee &
Jahn (as also indeed to some degree to that of Singh & Das), it would obviously
not be proposed if the Bovee & Jahn system were entirely satisfactory. The
distinction which Jahn & Bovee (1965) made between their classes Autotractea
and Hydraulea on the basis of two principal modes of locomotion is perhaps an
over-simplification (Allen, 1970). Bovee & Jahn separated some apparently
closely related organisms by distances as great as the ordinal (e.g., Saccamoeba
and Hartmannella) and also represented some relationships as closer than can
be justified. For example, there does not appear to be good evidence of a
special affinity between Pelomyxa on the one hand and Saccamoeba and
Trichamoeba on the other. The division of their order Thecida into three
suborders, each containing species which would seem even to belong to a single
genus Thecamoeba (Page, 1976 and work in progress) is an example of the
splitting tendency. The hotch-potch nature of their family Hartmannellidae,
containing such widely divergent organisms as Acan thamoeba, Naegleria, and
Sappinia is an example of the opposite tendency, with the additional provision
that these genera cannot be grouped together on the authors’ own criterion of
locomotive mechanisms. Nevertheless, the Bovee & Jahn system has great value
as a stimulus to further investigation, and future systems of the Sarcodina as a
whole will probably continue to be indebted to it. Its basic weakness is the
rather inconsistent way in which the authors have applied their primary
criterion. Bovee (pers. comm.) shares the view that taxonomic systems are
provisional structures subject to change with advancing knowledge rather than
ramparts at which the builder takes a stand.
I t should be mentioned at this point that Bovee & Jahn (1973) have
74
F. C. PAGE
presented a detailed review, beyond that possible in this paper, of the many
kinds of characters which could be used for taxonomic purposes. The
theoretical basis of the present system and the eventual aim has nowhere else
been better summarized than in the statement of Bovee & Jahn that “the whole
biology of an amoeba is requisite to its full characterization and relationship to
other amoebae.”
In facing the question of how much the present or any future system can
reflect phylogeny, we are not inclined to deny the truism that amoebae are
polyphyletic, but we might register some objection to the supposition that we
cannot now say anything at all about natural relationships and probably shall
never be able to do so. However, at present no classification on any basis could
profess to give an accurate picture of most of the relationships of the diverse
groups comprehended under the term Gymnamoebia. Even a tentative
phylogenetic diagram such as that ventured by Bovee & Jahn (1973) appears
daring at this time.
One positive statement that should be made is that the Schizopyrenida
(Vahlkampfiidae) are almost certainly a homogeneous group with either a
common origin or an origin in closely related ancestors. The vahlkampfiids
should, however, be retained in the Sarcodina and the Gymnamoebia for the
reasons stated in the explanatory comments. The Sarcodina as a taxon would
no longer exist if all organisms with any flagellate tendencies were removed.
The other group separated from the Amoebida proper is the order
Pelobiontida. The nuclei of these are usually granular, but that one character
alone does not demonstrate a special relationship to other larger amoebae
(those in the family Amoebidae and some in the family Thecamoebidae), since
it is also found in quite different Sarcodina. The speculation of Margulis (1970)
that Pelomyxa might represent “possible codescendants of the
protoeukaryotes” is interesting, but, as she recognizes, there is no clear
evidence that the mitochondrion-less condition of Pelomyxa is primitive rather
than secondary. Her own “detailed eukaryote phylogeny’’ is not to be taken
seriously, as far as the amoebae are concerned, if for no other reason than the
occurrence of the same species under synonymous names at different places in
her dendrogram.
Relationships among the various suborders and families of the order
Amoebida, in its newly retricted sense, are barely to be perceived, and the
order is almost certainly polyphyletic. Possibly the suborders Conopodina and
Acanthopodina should be formally separated at the ordinal level from the other
suborders of Amoebida, but to do so at this time would be to imply more than
can even be guessed about the relationships between and within those two
suborders. Within the suborder Tubulina, there is a suggestion of a relationship
between the Hartmannellidae and the Amoebidae, particularly in locomotive
behaviour and also in the mitotic pattern of the hartmannellid Saccamoeba,
which resembles those patterns of the Amoebidae which are known.
Considering families in different suborders, there may, on the basis of
locomotive form/behaviour and of nuclear structure and mitotic patterns, be a
relationship between the Flabellulidae (Flabellina) and the Hartmannellidae
(Tubulina), but the indications of such a relationship are insufficient to justify
a different subordinal classification. There are similar suggestions of a
connexion between the Thecamoebidae (Thecina) and the Amoebidae
A REVISED CLASSIFICATION OF NAKED AMOEBAE
75
(Tubulina), an opinion expressed also by Bovee & Jahn (1973). I t is likely that
each of these latter two families represents a good degree of natural
relationship within itself.
On the generic level, Rhizamoeba (Hartmannellidae) has some characters
slightly suggestive not only of the Flabellulidae but also of the plasmodium-like
Leptomyxida, a somewhat isolated sarcodinan group. Dinamoeba
(Paramoebidae) grossly resembles Acanthamoeba but is itself sometimes
considered synonymous with the amoeboid flagellate Mastigamoeba.
Acanthamoeba has certain nutritional and other biochemical characters
suggesting a closer relationship t o more plant-like protistans than can be seen
for most Amoebida. Echinamoeba, which has never been seen to produce any
structure more complicated than a simple, round, uninucleate cyst, bears some
resemblance in its locomotive stage to the myxamoebae of certain plasmodia1
and non-plasmodia1 mycetozoans. The list of suggestions could be extended,
but one cannot yet offer more than such vague and tantalizing possibilities.
ACKNOWLEDGEMENTS
In preparing the proposed revision of the Sarcodina as a whole for the
Society of Protozoologists, many workers were consulted. The present
detailed revision of the Gymnamoebia was not under consideration in that
correspondence, but some of the comments received proved most relevant to
the latter project. I wish t o acknowledge the special relevance of the replies
from Dr K. M. G. Adam, Dr E. C. Bovee, Dr Cicily Chapman-Andresen, and Dr
T. K. Sawyer. I wish also t o acknowledge my appreciation t o Dr Marc Pussard
for interesting discussions by post and in person. These acknowledgements do
not imply approval of the proposed system by those mentioned, some of whom
do indeed differ with it on more than one point. Nor does the association with
the preparation of the forthcoming comprehensive revision of the Protozoa
imply any approval by the Committee on Systematics and Evolution, Society
of Protozoologists. The final classification of the Sarcodina approved by that
committee may be similar t o or differ in some degree from that assumed here.
This revision is in a sense the product of 1 5 years’ investigation of amoebae.
All the recent work was done at the Culture Centre of Algae and Protozoa
(Natural Environment Research Council). Most earlier sources of support have
been acknowledged in previous publications, but I should like t o thank the
Carver Research Foundation of Tuskegee Institute for its support during one
extended early phase of the work on which this classification is based.
This account is published with the permission of the Director of the Culture
Centre of Algae and Protozoa.
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