Multilizer

PDF
Translator
INTERNATL
MICROBIOL
(1999)
2:207216
Springer-Verlag Ibrica 1999

Free version - translation is limited to ~ 3 pages per translation.

EXAMINA EL ARTCULO

207

No plantas o animales: una breve

Oficina de tecnologas de la informacin,
Universidad-de-Massachusetts-Amherst, los EE. UU historia del origen de Reinos
Protozoa, Protista y Protoctista
Joseph M. Scamardella

Recibido el 30 de mayo de 1999

Aceptado el 28 de agosto de 1999

Correspondencia a:
Oficina de Tecnologas de la informacin,
A149 LGRT. Universidad de Massachusetts.
Amherst, Massachusetts 01003. Los EE. UU.
Tel.: +1-413-5452696. Fax:
+1-413-5453203. Correo
electrnico:
jms@oit.umass.edu

Resumen Como consecuencia de las ideas evolutivas de Darwin, el mediados

de naturalistas del siglo XIX realiz los defectos del sistema de dos reinos
establecido largo de la clasificacin organismal. La colocacin en un esquema
natural de Protozoa, Protophyta, Phytozoa y Bacteria, microorganismos que
expusieron caractersticas parecidas a una planta y parecidas a un animal,
pero obviamente se diferenciaron en la organizacin de plantas y animales
ms grandes, desafi la clasificacin tradicional. Las tentativas de
naturalistas de clasificar estos organismos fuera de las coacciones de los
reinos vegetales y animales llevaron a conceptos de reinos adicionales
(Protozoa, Protista, Protoctista, etc.) para acomodar la naturaleza de estos
organismos
como
no plantas verdaderas
o animales.
Palabras clave
ProtistaProtoctista
Concepto
de Protozoa Monera John
Hogg (18001869) Herbert F. Copeland (19021968)

La mayor agrupacin morfolgica en reinos es, en

cualquier momento, una reflexin de nuestro entendimiento
del mundo vivo. Antes del 20mo siglo, los conceptos de la
clasificacin organismal haban sido reprimidos dentro de
lmites estrechos que definieron toda la vida como planta o
como animal [34, 37]. Sin embargo, haba organismos
complejos, principalmente microscpicos y acuticos, con
las mayores caractersticas de verdes de plantas y el
movimiento de animales que estiraron aquellos lmites
vegetales y animales. El siglo dieciocho investigaciones
microscpicas sobre la naturaleza de estos organismos los
consider como clulas disociadas de plantas y animales o
a lo ms como formas imperfectas de plantas ms altas
[4]. Las innovaciones tecnolgicas, como el condensador
de la subetapa acromtico en 1838 [3, 35], refinaron la
ptica del microscopio ligero y condujeron la ciencia de la
microscopia a lo largo de nuevos caminos de la
investigacin sobre las historias de la vida de organismos
microscpicos. Al mediadosel dle del siglo XIX, las
agrupaciones microbianas generalizadas de Protozoa,
Protophyta, Phytozoa y Bacterias colocaron los organismos
en un contexto de ms abajo, o formas intermedias en la
evolucin a plantas y animales ms altas [22, 33].
Simultneamente, la dicotoma existente de los reinos
vegetales y animales se hizo rpidamente enturbiada en sus
lmites y anticuada ya que los propios organismos antes
mencionados, en su naturaleza muy parecida a una planta y
parecida a un animal, nublaron cualquier definicin sucinta
de una planta o un animal [34, 37].

Protozoa como una clase, phylum y reino

En 1820, el naturalista alemn Georg A. Goldfuss introdujo
el trmino Protozoa (primero, o animales tempranos) en la
literatura cientfica para una clase de organismos dentro de
Reino Animalia que consisti en Infusoria (llam ciliates
hoy), Lithozoa (corales), Phytozoa (p.ej. Cryptomonas), y
Medusinae [47]. En 1845 Carl Theodor von Siebold de
Alemania estableci un phylum de animales invertebrados
dentro de Reino Animalia que llam Protozoa [39]. Phylum
Protozoa consisti en las clases Infusoria (ciliates) y
Rhizopoda (amebas, foraminifera) y von Siebold
consideraron estos organismos como animales
unicelulares, poseyendo la funcin y la estructura de una
clula de animal individual, no el organismo entero [34, 37,
39]. Otros investigadores, como el naturalista Louis Agassiz,
pensaron que el protozoa era ms parecido a una planta que
parecido a un animal y no creyeron que fueran la parte del
reino animal [1]. A mediados - siglo XIX, los organismos
microscpicos eran generalmente considerados dentro de las
agrupaciones generalizadas de Protozoa (animales
primitivos), Protophyta (plantas primitivas), Phytozoa
(plantas parecidas a un animal), y Bacterias (primario
considerado como plantas) [1, 22, 33]. Ningn consenso
claro existi sobre la naturaleza sistemtica de los
organismos y su relacin evolutiva el uno al otro o a plantas
y animales ms grandes [34, 37]. La vida microscpica se
hizo

Multilizer PDF Translator Free version - translation is limited to ~ 3 pages per translation.

Multilizer PDF Translator Free version - translation is limited to ~ 3 pages per translation.

208

Yo
NTERNATL MICROBIOL Volumen 2, 1999

Scamardella

cada vez ms entrelazado y reprimido taxonmicamente

dentro de la dicotoma de los reinos vegetales y animales.
En 1858, el paleontlogo Richard Owen (18041892)
perfil su definicin de plantas y animales en el contexto de
aquellos numerosos seres, generalmente de la talla del minuto
y retener la forma de clulas nucleated que demostraron los
caracteres orgnicos comunes de plantas y animales, pero
sin las superadiciones de planta verdadera y animales.
Llam estos organismos Protozoa, definido como un grupo
que contiene las esponjas o Amorphozoa, Foraminifera o
Rhizopods, Polycystineae, Diatomaceae, Desmidiae,
Gregarinae y la mayor parte de llamados Polygastria de
Ehrenberg o los animlculos infusorial de los autores ms
viejos [31]. En 1860, Owen se refiri a esta agrupacin como
Reino
Protozoa
en su libro
la Paleontologa
[32]. comparti
Aquellos
caracteres
orgnicos
que Protozoa

La opcin de Owen del trmino Protozoa, como los

naturalistas estn divididos en la opinin
y
probablemente seguirn alguna vez as si muchos de
estos organismos o criaturas, son animales o plantas, y
que los lmites entre el animal y reinos de verduras son
ms o menos artificiales, y no pueden ser bien
determinados [20]. Hogg mantuvo que el trmino
Protozoa puede solo incluir a aquellos que son
reconocidos por todos ser animales o zoa y por lo tanto
era un nombre incorrecto para la agrupacin de organismos
que eran bastante ambiguamente animales [19]. Hogg era
consciente que ya que los naturalistas no pueden convenir
en los caracteres precisos que definen plantas y animales
(Hogg crey que las caractersticas de definicin de un
animal eran los sistemas nerviosos y musculares, que no
existen en una fbrica), no hay solucin prctica adems
con plantas y animales estaban basados en la definicin de
de colocar a aquellas criaturas o seres orgnicos, cuya
Owen de una planta y un animal. Una planta es arraigada,
naturaleza es tan dudosa en un cuarto reino [19]. Hogg
no tiene ni la boca, ni el estmago, exhala el oxgeno y
crey que incluso todos estos organismos en el Reino de
hace formar tejidos de 'la celulosa' o de compuestos
Primigenal previene el problema innecesario de
binarios o ternarios [31, 32]. Un animal recibe el asunto
enfrentarse por sus naturalezas supuestas, y de tratar
nutritivo por una boca, inhala el oxgeno, y exhala el
intilmente de distinguir Protozoa de Protophyta [20].
cido carbnico y desarrolla tejidos los principios
Hogg ms totalmente describi Regnum Primigenum como
prximos de los cuales son compuestos quaternary de
conteniendo aquellos organismos inferiores, o cre a seres
carbn, hidrgeno, oxgeno y nitrgeno [31, 32]. Uno
(ctista) & Desmidiae, algunos Infusoria, y Diatomeae, y
podra reconocer fcilmente plantas y animales, segn
Algas dudosas y otro Protoctista, e incluy a todos los
Owen, cuando un cierto nmero de caracteres concurre
seres de la esponja (Spongioctista), y otros por el estilo
en el mismo organismo su ttulo para ser considerado
El trmino
de Hogg
Protoctista
expresivo [20].
de
anmalo
ms abajo
ctista,
criaturas era
u organismos
como una 'planta' o un 'animal', puede ser fcilmente y sin organismos que vinieron primero en el tiempo evolutivo y
duda reconocido [30]. Por otra parte, Protozoa fueron
eran el diagrama - matically representado por Hogg (y al
definidos por su carencia de aquellos un cierto nmero de principio public en color) [20] (Fig. 1). Los Protoctista
caracteres, o superadiciones, de plantas y animales
son representados como una agrupacin de organismos que
verdaderas.
tienen los caracteres comunes de ambas plantas y animales.
La pirmide del reino de la planta y la fusin de la
Protoctista de John Hogg (1860, 1868)
pirmide del reino animal bien antes de sus bases se
encuentran. Esta rea comn es donde los caracteres de
En 1860 el naturalista britnico John Hogg (18001869)
escribi un artculo titulado En las Distinciones de una plantas y animales se hacen menos distintos y donde los
Planta y un Animal y en un Cuarto Reino de la Naturaleza lmites entre los reinos vegetales y animales son
enturbiados. Esta combinacin es representativa de
en la cual perfil su oferta de Regnum Primigenum
[19]. Hogg tambin describi este cuarto reino (los otros Protoctista (y la encarnacin de Regnum Primigenum),
reinos ser Planta, Animal y Mineral, de Linneaus) como el aquellos organismos que han entremezclado caractersticas
comunes para ambas pirmides o reinos. Lo que es
Reino de Primigenal, y consisti de todas las criaturas
significativo en la pintura de Hogg de Protoctista es que las
inferiores o los seres orgnicos primarios, Protoctista
plantas y animales comparten una ascendencia comn de
(que compuso del griego, etimolgicamente como seres
Protoctista.
primero creados) [19]. Protoctista eran ambos
Protophyta o los considerados ahora por muchos como, Protista de Haeckel (1866)
seres inferiores o primarios; y Protozoa o tal son
estimados como seres inferiores o primarios, teniendo En 1866, el naturalista alemn Ernst Haeckel (18341919)
mejor dicho la naturaleza de animales [19]. Tambin
hizo la primera de muchas ofertas de un tercer reino de la
incluido en Regnum Primigenum eran esponjas, agrupadas vida [16]. En su Generelle Morphologie der Organismen
como Amorphoctista, los informes o amorpseres de
llam este tercer reino y los organismos contenidos dentro
horas, si compartiendo ms de una verdura o de una de ello Protista, el en primer lugar, primordial [16, 17].
naturaleza de animal [19].
Haeckel llam la atencin al problema de clasificar todos
El Reino de Hogg de Primigenal por lo tanto
aquellos organismos dudosos de la fila ms baja que no
consisti tanto en organismos multicelulares como en
muestran ningunas afinidades decididas ms cerca a un lado
unicelulares como Reino de Owen Protozoa hizo. Sin
que al otro, o que animal de tropas
embargo, Hogg no estuvo de acuerdo con

Multilizer PDF Translator Free version - translation is limited to ~ 3 pages per translation.

Multilizer PDF Translator Free version - translation is limited to ~ 3 pages per translation.

Protozoa, Protista y Protoctista

209
Yo
NTERNATL MICROBIOL Volumen 2, 1999

la representacin de Hogg de Fig. 1 de la divergencia y unin de varios reinos. De En las distinciones de unas Plantas y animales, y en un Cuarto
Reino de Naturaleza (1860) Nuevo Phil J de Edimburgo, NS 12:216225. Coleccin de la Sociedad Linnean, Londres. (Con permiso.)

y los caracteres de verduras se unieron y se mezclaron [16,

17]. A diferencia de la oferta de Hogg en la cual el Mineral
era un reino, Haeckel slo reconoci Reino Plantae y Reino
Animalia [16]. A Haeckel su tercer reino, Protista (en
primer lugar, primordial), era el reino de formas
primitivas, y consider las bacterias o Monera (simple),
para ser Protista tambin [17].
Haeckel pens que Protista era un intermedio del reino
divisorio entre el animal y reinos de verduras que
contienen organismos ni animales, ni plantas [16, 17].
Haeckel tambin consider el Reino Protista como un
sistema prctico para separar Protista en el sistema de
naturaleza completamente de animales as como de
plantas, en el proceso que ms claramente define las
caractersticas de plantas y animales verdaderas [16]. Sin
embargo, Haeckel nunca tuvo la intencin de erigir una
pared absoluta de la separacin entre el animal y reinos de
verduras [17]. Aunque Haeckel creyera que los animales y
las plantas sacaron su origen de las bacterias, tambin
consider que Protista evolucion independiente de los
linajes del animal y reinos de la planta, y slo era
conveniente por motivos prcticos separar Protista en el
sistema de naturaleza completamente de animales as como
del plants [17].
El objetivo de Haeckel era para Protista considerarse
por separado con objetivos sistemticos, no phylogenetic
(el trmino de Haeckel) [17, 37]. Reino Protista
contenido

aquellos organismos generalmente considerados por

separado por otros naturalistas como Protozoa, Protophyta,
Phytozoa y Bacterias; reino Protista era una agrupacin
tanto de no - nucleated como de organismos nucleated
[17]. Los organismos fueron sistemticamente arreglados
por Haeckel en Protista phyla siguiente: Monera (bacterias
y algunos moldes del lodo celulares), Protoplasta
(amebas), Diatomaceae, Flagellata (p.ej. Euglena,
Peridinium), Myxomycetes (p.ej. Physarum), Noctilucae
(p.ej. dinoflagellates), Rhizopoda (moldes del lodo
celulares y radiolarans, p.ej. heliozoans, actinopods), y
Spongiae [16, 17] (Fig. 2). Reino Protista era por lo tanto
una agrupacin tanto de organismos unicelulares como de
multicelulares. Haeckel coloc Infusoria en Reino
Animalia ya que (y otros investigadores) los consider
animales multicelulares (hasta que el bilogo alemn Otto
Butschli demostrara la naturaleza unicelular de Infusoria
en 1873) [8].

Haeckel redefine Reino Protista

Con el retiro de esponjas de Reino Protista despus de que
concluy que eran animales, Haeckel crey que podra
separar claramente ahora Reino Protista de animales
verdaderos y plantas en la realizacin que el carcter de
definicin de Protista restante era la ausencia de la
reproduccin sexual [17]. Haeckel declar que todos
Protista verdaderos se multiplican exclusivamente por un no
-

Multilizer PDF Translator Free version - translation is limited to ~ 3 pages per translation.

210

INTERNATL MICROBIOL Vol. 2, 1999

Scamardella

sexual reproduction (monogamy) [17]. Basing his

organization of the unicellular protistan organism, or
groupings of organisms on this criterion, he then moved protist (Dobells term), is equivalent to the entire
the phylum Fungi (Inophyta) out of Kingdom Plantae and ensemble of cells constituting a plant or an animal. Calling
into Kingdom Protista. The blue-greens (known as the Protista acellular was Dobells manner of calling
cyanobacteria today) were also moved from Kingdom attention to the fact that the Protista as organisms were
Plantae and placed into Kingdom Protista as the phylum organized quite differently from that of cellular plants
Phycochromacea. Phylum Labryinthulea (slime nets) and animals. Dobell asserted that the great importance of
was moved from the Animal kingdom and placed into the Protista lies in the fact that they are a group of living
Kingdom Protista. Volvocineae (Volvox) was moved out beings which are organized upon quite a different principle
of Flagellata in Kingdom Protista and into Kingdom Plantae [17].
from that of other organisms [14]. Dobells concept of
acellularity laid the foundation of the study of
Haeckel saw these changes in Kingdom Protista
Protistology, as coined by Dobell [13, 14, 36].
occurring as our knowledge of one group or another
becomes apparently more complete [17]. In later revision Investigation of the Protista in the light of acellularity was
the beginning of a shift away from the dogma of German
of Kingdom Protista, he founded a two-kingdom concept
based upon a morphological division between the Protista cell theory of the late 1800s and its concept of the Protista
as unicellular [21, 36]. From the early 1900s and into the
(unicellular plants and animals) and the Histonia
1920s and 1930s, for lack of a viable alternative, Haeckels
(multicellular plants, the Metaphyta, and animals, or
Metazoa) [18]. Haeckel maintained that the blastular stage Kingdom Protista became increasingly regarded as a
makeshift classification too polyphyletic to represent a
of development was the defining characteristic of an
coherent evolutionary look at the organization of life on
animal, and he saw this characteristic as the fundamental
Earth [29, 37]. The Protista began to be regarded more in
division between animals and the Protista [8, 17, 18].
terms of evolutionary systematics rather than in a
However, Haeckels criterion for defining the plant
phylogenetic classification of protist taxa, although the Protista as an evol
kingdom remained primarily nutritive [17, 18]. Haeckel
also returned the terms protozoa (unicellular animals)
and protophyta (unicellular plants) to the forefront,
regarding these groupings as sub-kingdoms of Kingdom Protista [18].

Copelands Kingdoms Protista and

Protoctista

Butschlis Protozoa and Dobells Protista

The tenet that all microscopic life was single-celled in
nature was first brought into prominence by von Siebold
some twenty years earlier and became reinforced by the
German zoologist Otto Butschli (18481920) in the 1880s
[8, 21]. Butschlis concurrent rejection of the concept of a
third kingdom entirely was based upon his belief that the
Protista, especially with inclusion of the bacteria, was too
polyphyletic in nature to be considered a single kingdom
[21, 22, 37]. Butschlis grouping of Protozoa was defined
as consisting of only nucleated, unicellular animal-like
organisms; bacteria as well as the protophyta were
considered as a separate grouping [21]. Consequently,
Butschlis influence strengthened the von Siebold concept
of protozoa as single- celled animals and the protophyta
as single-celled plants [13, 21]. The German naturalists
and their academic institutions asserted an authoritarian
view over the rest of the worldwide scientific community,
and by the turn of the century the definitions of these
organisms as unicellular animals and unicellular plants
had become solidly established [13, 36].

In 1938, American biologist Herbert F. Copeland

(19021968) at Sacramento Junior College in California,
proposed a four-kingdom classification of life in a article
entitled The Kingdoms of Organisms [9]. Copelands aim
was to present a taxonomy that systematically reflected
the diversity of the living world beyond the boundaries of
the plant and animal kingdoms. The primary basis for
Copelands four-kingdom concept was his conclusion that
the establishment of several kingdoms of nucleate
organisms in addition to plants and animals is not
feasible; that all of these organisms are to be treated as
one kingdom [9]. What led him to this conclusion was
the extreme difficulty of teaching biology based upon
Haeckels system, and that various authors more recent
than Haeckel have shown a disposition to recognize more
kingdoms than two, but none of them, apparently, has
formulated a system including all organisms [9].

In Copelands proposed four kingdom reclassification

of life (Kingdom Monera, Kingdom Protista, Kingdom
Plantae, Kingdom Animalia), the foundation was in the
exclusion of the bacteria and the blue-green algae
(cyanobacteria) from Haeckels Kingdom Protista into a
separate kingdom he named Monera. Copeland regarded
However, British biologist C. Clifford Dobell
(18861949) in 1911 redefined the concept of unicellularity, the bacteria to be so different in organization from
nucleated cells that this difference was of central
and in doing so reinterpreted the definition of Protista as
importance
acellular instead of unicellular [14]. Dobell argued that the function
and to his proposed four- kingdom system of life, in that the orga

Protozoa, Protista and Protoctista

INTERNATL MICROBIOL Vol. 2, 1999

211

Fig. 2 Haeckels three kingdoms of life. From Generelle Morphologie der Organismen. Vol II. (1866). Berlin: Georg Reimer. Collection of Amherst
College Library, Massachusetts, USA. (With permission.)

212

INTERNATL MICROBIOL Vol. 2, 1999

are evidently to be treated as a kingdom: they are different

from plants and animals in greater degree than the latter are
different from each other [9].
In 1947, Copeland chose to call this fourth kingdom
Protoctista (which he defined etymologically as first
established beings) instead of Protista [10, 11]. Copeland
did not believe that it was appropriate to use Protozoa
based upon Hoggs objections to the term, as well as the
fact that Protozoa had been used previously not only for a
kingdom (Owen) but also as a class (Goldfuss) and a
phylum (von Siebold) [10, 11]. Copeland utilized the term
Protoctista as inclusive of the protophyta and protozoa as
Hogg did for organisms not true plants or animals.
Although Haeckel defined the Protista in the same way,
Copeland chose Protoctista for a kingdom name based on
the fact that after Kingdom Protozoa, the term Protoctista
had priority [10, 11]. Since Copeland recognized the
primary cellular difference between anucleate and
nucleate organisms, he regarded Protista unfit to use any
longer as the name for his kingdom due to the fact that in
all Haeckels versions of Protista the anucleate bacteria
were always included with nucleated organisms [11].

Scamardella

In 1957 Robert H. Whittaker (19241980), a biologist at

Brooklyn College in New York City, began a reassessment
of Copelands four-kingdom system from an ecologists
point of view [43]. Whittaker, who studied the New Jersey
pine barrens, recognized an ecological division of the
living world by distinction between autotrophs and
heterotrophs [43]. This outlook did not correspond to
Copelands four-kingdom concept or to the two-kingdom
system of plants and animals [43]. Whittaker detailed his
own four-kingdom system of Protista, Fungi, Plantae, and
Animalia in his 1959 article, On the Broad Classification of Organisms [44

Whittaker based his kingdom groupings upon the three

main modes of nutrition in natural communities: absorption,
ingestion, and autotrophy [43, 44]. He also credited the
evolutionary sequence of unicellular to multicellular with
central importance to his classification scheme [44].
Utilizing these criteria as the basis for classification,
Whittaker returned the bacteria to Kingdom Protista (also
based upon their unicellular nature) and placed all algae
(green, brown, and red) into Kingdom Plantae [44]. The
protozoa of Copelands Protoctista were reassigned by
In 1956, Copeland presented a more detailed taxonomic Whittaker to his Kingdom Protista. Whittakers primary
phyletic interest overall was, however, in establishing a
view of his four-kingdom system in his book The
separate kingdom to contain macroscopic fungi [44]. In
Classification of Lower Organisms [11]. Copelands
particular, Whittaker observed the absorptive role of the
definition of Kingdom Protoctista relied upon a sharp
fungi in the natural environment. He rejected the common
limitation of the plant and animal kingdoms. Kingdom
Plantae was defined to contain organisms demonstrating the belief that the superficial resemblance of fungi to plants,
with their non-motile habit and cell walls, made them true
presence of chlorophyll a and b, carotene, xanthophyll,
and the production of starch [11]. This group of organisms plants [44]. Whittaker did not believe that the fungi were
included all plants, as well as the green algae. Photosythetic derived from algae, but rather he thought they evolved from colorless, flage
organisms that did not meet these criteria were the brown
In 1969 Whittaker published a revision of his
and red algae. Kingdom Animalia was defined (after
four-kingdom system to expand it to five kingdoms, now
Haeckel) by the presence of the multicellular blastular stage including a separate bacterial kingdom named Monera in
of development [11]. What remained of these organisms, on recognition of the fundamental division of life as
the surface the miscellany [of] the kingdom Protista of
prokaryotic versus eukaryotic (as Copeland did, but
Haeckel, consisted of nucleate organisms not of the
expressed as anucleate and nucleate) [45]. This
characters of plants and animals [10, 11]. Thus the
distinction was first conceived by French protozoologist
Protoctista were those nucleate organisms, either
Edouard Chatton (18831947) in 1925 in an article entitled
unicellular or multicellular with or without photosynthetic
Pansporella perplexa: Amoebien a Spores Protges
pigments but not of the type in plants; without a blastular
Parasite des Daphnies. Rflexions sur la Biologie et la
stage, and consisting of the broad groups red algae, brown
Phylogenie des Protozoaires, (Ann Sci Nat Sr X (Zool),
algae, fungi, and protozoans [11]. Copeland also realized
8:584, cited by Ragan [35]) and again in 1938 in his own
that so many unicellular organisms have multicellular
bound works entitled Titres et Travaux Scientifiques [7, 26,
descendants that a unicellular/multicellular dichotomy is
34, 35, 41]. Whittaker noted that this concept was now more
invalid [11]. Even though Copeland recognized the fact that evident due to the writings of microbiologist Roger Y.
the organisms of Kingdom Protoctista were an unfamiliar Stanier in 1962 and 1963 [41, 42] and that this evolutionary
assemblage and undeniably heterogeneous and may be
divergence in cellular structure had to be accounted for by
distinguished as a group by the absence of true plant and
the recognition of Kingdom Monera [45]. Otherwise,
animal characteristics, he nonetheless believed it is not by Whittakers reasoning remained the same for retaining the
characters but by relationship that groups are defined, and
other four kingdoms in this Five Kingdom system. He
the more numerous will be the exceptions to the formal
reasserted his ecological model as well as the belief that
descriptive characters. We may with equanimity abandon the attempt
toof
define
Protista organisms
by characters,
negative [9].
inclusion
multicellular
into positive
KingdomorProtista

The Five-Kingdom system of classification

would make the Five Kingdom system an evolutionarily unnatural, heterogen

Protozoa, Protista and Protoctista

INTERNATL MICROBIOL Vol. 2, 1999

213

diagnostic of the group, the same as Haeckels Protista was Protoctista as a grouping of independent lineage, some of
known at the turn of the century.
which evolutionarily led to plants, animals and fungi and
In 1968, just prior to Whittakers publication of his five- some did not [25]. Protoctists could be recognized more
clearly as organisms in their own right, not in terms of being
kingdom classification, biologist Lynn Margulis at Boston
lower, or intermediate solely leading to higher organisms [27].
University proposed a four-kingdom system based upon the
model of Copeland, who was at the time the only researcher
to offer a detailed taxonomic work that recognized the
biological discontinuity between prokaryotic and eukaryotic A return to Kingdoms Protozoa and Protista
organisms [23]. Differing from Copelands Protoctista,
Margulis Kingdom Protoctista included the green algae,
John Corliss, protozoologist at the University of Maryland,
which she did not consider plants; this change was
has reinterpreted the taxonomy of Kingdom Protista of
considered in light of the theory of bacterial endosymbioses
Whittaker and Kingdom Protoctista of Margulis based
in the evolution of the Protoctista [23]. Increasing evidence
primarily, but not exclusively, upon unicellularity [12]. He
of genetic and ultrastructural nature of mitochondria and
draws a line of demarcation regarding differentiated,
plastids showed these eukaryotic cell organelles having
functional tissues of multicellularity, similar to concerns
independent bacterial genomes, and consequently plants and Whittaker had voiced [12]. Corliss in turn describes plants
animals themselves were regarded by Margulis as
and animals by the presence of more than a single tissue and
evidencing a polyphyletic nature, evolving from protoctist ancestors
[23].while showing multicellularity to varying degrees
protists,
in certain groups, and occasionally even huge body size,
After Whittakers publication of his five-kingdom
again fail to demonstrate the organization of cells into two
concept, Margulis incorporated the phylogenetics of her
or more clearly differentiated tissues [12]. To Corliss, red
system with the five-kingdom system and accepted the
and brown algae appear not to have the complexity of
kingdom name of Protista instead of Protoctista [24].
tissues as true plants and animals and therefore can not be
However, Margulis Kingdom Protista differed from
seen in the same light of plant and animal multicellularity;
Whittakers in that hers contained all algae (green, brown,
they are placed within the Kingdom Protista primarily on
red), limiting Kingdom Plantae to the botanical phylum
this basis [12]. Corliss also defines plants and animals upon
Embryophyta [24]. These modifications were in direct
mode of nutrition (autotrophy and heterotrophy,
consideration of endosymbiotic evidence that protozoans
respectively), which are invalid distinctions as there are
and nucleate algae represent a large group of organisms
phototrophic animals (e.g. Convoluta roscoffensis) and fully
with flagellated heterotrophic eukaryote ancestors [24].
heterotrophic plants (e.g. Monotropa) [26]. Corliss, who
Margulis further viewed the Protista as a heterogeneous
bases his four eukaryotic kingdoms (Animalia, Plantae,
grouping of unicellular and multicellular eukaryotes
Fungi, Protista) on degree of cellular organization also
representing polyphyletic evolutionary experiments
overlooks
leading toward the ultimate establishment of mitosis and regular
meiosis the
[24]. fact that multicellular, differentiated
organisms are known in all four eukaryotic kingdoms and in Kingdom Moner
Relying more upon morphological and ultrastructural
comparisons within the Protista, Margulis departed from
Corliss takes the issue with the major high-level
Whittakers nutritional and unicellular morphological
taxonomic and nomenclatural problems presented in
criteria of the Protista, and led her to accept the kingdom
recognition of a kingdom Protista, and his main concern is
name Protoctista from Copeland. Plants became defined as
that proponents of a separate kingdom of protists have
the group of organisms that develop from a multicellular
characterized it in a negative fashion [12]. Corliss has
embryo retained in maternal tissue, then, animals develop
weighed this concern in his taxonomic arrangement of
from a multicellular blastular stage, fungi as organisms that
protists to stress major uniqueness, emphasizing the
develop from spores and lack flagella (today termed as
presence rather than the absence of a structure or function
undulipodia) at any stage of life history. Protoctista were
[12]. However, Copeland maintained that absence of positive
eukaryotic organisms either unicellular or multicellular that characters in the definition of the Protista is not a detriment
are not plants, animals or fungi [46]. Margulis also
to classification as a coherent grouping: it is not the presence
introduced the term protoctist to refer to an individual
or absence of animal and plant characters that define the
organism of the Protoctista, whether unicellular or
kingdom but by relationship between organisms within the greater grouping [8
multicellular [46]. Defining the Protoctista by exclusion was
Corliss has advocated adopting the term Kingdom
the extension of sharply defining, or limiting, the
Protista instead of Protoctista, as his opinion is that Protista
characteristics of organisms in kingdoms Plantae, Animalia,
is more popular and etymologically simpler [12, 13]. He also
and Fungi. The fact remained, however, that as a grouping
advocates usage of the term protist to denote all forms of
the organisms of Protoctista had more in common with each
Protista, both unicellular and multicellular. However, the
other than to the larger plants, animals, or fungi. Increased
term protist, as coined by Dobell, was defined by Dobell in
research combining genetic (16S rRNA comparisons), biochemical, and ultrastructural observations of protoctists has evidenced the
reference to the Protista possessing the unicellular type of organization [14]

214

INTERNATL MICROBIOL Vol. 2, 1999

Scamardella

Table 1 Concepts of Kingdoms Protozoa, Protista, and Protoctista (18601998) discussed in the text
Kingdom Protozoa

Kingdom Protista

Kingdom Protoctista

Owen (1860)*

Haeckel (1866, 1869, 1905)

Hogg [Regnum Primigenum] (1860, 1868)

Cavalier-Smith (1983, 1998)

Copeland (1938)

Copeland (1947, 1956)

Whittaker (1957, 1959, 1969, 1978)

Margulis (1968, 1970, 1990, 1996, 1998)

Margulis (1970)
Corliss (1984, 1986)
* Years correspond to works cited in the list of References.

Protoctist, a term recovered by Margulis, has always

terminology of lower and primitive in describing the
referred to both unicellular and multicellular eukaryotes evolutionary context of the organisms [6]. As far back as
within the Kingdom Protoctista [26, 46].
1911 Clifford Dobell wrote that simple, lower, unicellular,
Other researchers are primarily concerned by the lack of or primitive are terms that have arisen chiefly through
misconceptions involved in the cell theory and the theory of
physiological and morphological features that fail to unite
organic evolution [14]. These labels can also be seen as
the Protoctista into natural, or monophyletic classification
more of a holdover from the Victorian age and its prevailing
[2, 6, 35]. Since the late 1970s and widespread use of the
techniques and concepts of Woese et al. [48] there has been idea of ascension up the ladder of progress leading to
perfection rather than reflecting any meaningful quality of
greater focus upon 16S rRNA sequence comparisons and
evolutionary history of organisms [15].
cellular architecture, with less integration of biochemical
and morphological characteristics [2, 6, 35]. Tom
A brief account of the different names used by some
Cavalier-Smith, botanist at the University of British
authors is indicated in Table 1. The years in the Table
Columbia, Canada, has argued for a six- kingdom system of correspond to the works cited in the list of References.
classification that emphasizes monophyly [5, 6]. The basic
outline of his classification contains the Kingdoms Bacteria
(prokaryotic kingdom), Protozoa and Animalia (two
The three-domain system of life
eukaryotic zoological kingdoms), and Fungi, Plantae, and
Chromista (e.g. oomycetes, xanthophytes), the three
In the late 1990s it is becoming more tempting for biologists
eukaryotic botanical kingdoms [6]. Cavalier-Smiths
and scientists of different disciplines alike to give more
dispersion of the Protista/Protoctista throughout his five
weight to a completely non-morphological system of
eukaryotic kingdoms presents an evolutionary look at life
organismal classification as advocated by bacteriologist Carl
that is less polyphyletic. The goal of monophyly neglects the
Woese [48, 49]. Woese does not share in common with most
endosymbiotic history of eukaryotes [25]. In his search for
biologists the recognition that the living world is primarily
ultrastructural similarities between organisms, the overt
classified by a dichotomy of prokaryotic and eukaryotic
morphological distinctions that define plants and animals
cellular organization [48, 49]. He has instead presented an
are seemingly lost; animals are instead defined as
argument for life on earth being composed of three primary
ancestrally phagotrophic multicells with collagenous
divisions, or domains: Archaea (archaebacteria), Bacteria
connective tissue between two dissimilar epithelia, and
(eubacteria), and Eucarya (all eukaryotes) [48, 49]. This
plants defined as organisms with plastids with double envelope in cytosol; starch; no phagocytosis [6].
concept sketches out a basic evolutionary perspective
between the two prokaryotic domains (Archaea and Bacteria)
Cavalier-Smith also considers that there is value in
holding on to the term Protozoa for a Kingdom name, very and the domain of Eucarya. Relying upon 16S rRNA gene
sequences and to a lesser extent lipid content in order to
similar in composition to Owens (1858) for eukaryotic
organisms more primitive form of life than animals, plants, determine evolutionary relationships between organisms,
Woese neglects any evolutionary significance of
or fungi [6]. He believes that retaining the term protozoa
(which he terms a kingdom of lower organisms) is justified endosymbioses in eukaryotic cell evolution [25]. What may
because the term has been so widely used by biologists since be regarded on one hand as being more scientifically
precise (and certainly, fashionably reductionist), is on the
the nineteenth century, and that there is real value in
other hand expressive only of relative change for a single
keeping as close as possible to the historically dominant
gene over evolutionary time. Furthermore, in nature it is not
meaning [6]. However, this historical meaning can be
molecules
populations
of whole organisms that are selected [25]. Still, W
misleading, as Hogg himself pointed out in 1860 [19]. Cavalier-Smith
alsobut
retains
the

Protozoa, Protista and Protoctista

not its outcomes [49]. Yet the greater morphological,

biochemical and even ultrastructural, distinctions between
organisms are no longer considered, blurring the
boundaries of how even plants and animals are defined.
Harvard University zoologist Ernst Mayr takes umbrage
at Woeses manner of classification as not adequately
expressing the phenotypic diversity of living organisms,
asserting that to claim that the difference between the two
kinds of bacteria is of the same weight as the difference
between the prokaryotes and the extraordinary world of the
eukaryotes strikes me as incomprehensible [28].
Utilizing the same techniques of Woese, Mitchell Sogin
(Woeses former student) of the Marine Biological
Laboratory at Woods Hole, has focused upon the small and
large subunit rRNA gene sequencing of protoctist Eukarya
[40]. When taking into account the endosymbiotic life
histories of the organisms, Sogin finds protoctists to be a
collection of independently evolved lineages of
tremendous diversity [40]. However he does not take into
account phenotypic differences in his classification, since
the rate of genotypic change is not necessarily linked to
phenotypic variation, measures of genetic similarity
between protists cannot be determined from traditional
studies of morphology, physiology, or biochemistry [40].
Clearly, biological classification is at a crossroads.
Technology is providing a new manner of systematic
investigation and evolutionary interpretation, much the same
way microscopic investigation in the 1850s was intensified
by the improved optics of the light microscope and the
intricacies of cellular ultrastructure became uncovered by
electron microscopy beginning in the 1950s [2]. However
defined, the diversity of life is evidenced by our changing
interpretation of the system of living organisms, never set in
stone, ripe for revision in response to the changing light of
biological investigation.

INTERNATL MICROBIOL Vol. 2, 1999

215

6. Cavalier-Smith T (1998) A revised six-kingdom of life. Biol Rev Cam

Philos Soc 73:203266
7. Chatton E (1938) Titres et Traveaux Scientifiques (19061937). Ste
8. Churchill F (1989) The guts of the matter. Infusoria from Ehrenberg to
Butschli: 18381876. J Hist Biol 22:189213
9. Copeland HF (1938) The kingdoms of organisms. Quart Rev Biol
13:383420
10. Copeland HF (1947) Progress report on basic classification. Amer Nat
81:340361
11. Copeland HF (1956) The Classification of Lower Organisms. Palo Alto:
Pacific Books
12. Corliss J (1984) The Kingdom Protista and its 45 Phyla. BioSystems
17:87126
13. Corliss J (1986) The kingdoms of organismsfrom a microscopists
point of view. Trans Am Microsc Soc 105:110
14. Dobell C (1911) The principles of protistology. Arch Protist 23:269310
15. Gould SJ (1996) The power of the modal bacter, or why the tail cant
wag the dog. In: Full House. New York: Three Rivers Press, pp 167216
16. Haeckel E (1866) Generelle Morphologie der Organismen. Vol. II.
Berlin: Georg Reimer
17. Haeckel E (1869) Monograph of Monera. Quarterly J Microsc Sci
9:2742, 113134, 219232, 327342
18. Haeckel E (1905) The Wonders of Life. New York: Harper & Brothers
19. Hogg J (1860) On the distinctions of a plant and an animal and on a
Fourth Kingdom of Nature. Edinburgh New Phil J, NS 12:216225
20. Hogg J (1868) Is the fresh-water sponge (Spongilla) an Animal? Pop
Sci Rev 7:134141
21. Jacobs N (1989) From unit to unity: Protozoology, cell theory, and the
new concept of life. J Hist Biol 22:215242
22. Kent WS (18801881) A Manual of the Infusoria. Vol. 1. London: David
Bogue
23. Margulis L (1968) Evolutionary criteria in thallophytes: A radical
alternative. Science 161:10201022
24. Margulis L (1970) Whittakers five kingdoms of organisms: Minor
revisions suggested by considerations of the origin of mitosis.
Evolution 25:242245
25. Margulis L (1996) Archaeal-eubacterial mergers in the origin of Eukarya:
Phylogenetic classification of life. Proc Nat Acad Sci USA 93:10711076 26.
Margulis L, Corliss JO, Melkonian M, Chapman DJ (eds) (1990) Handbook of
Protoctista. Boston: Jones and Bartlett

27. Margulis L, Schwartz KV (1998) Five Kingdoms. An Illustrated Guide

to Life on Earth. 3rd edn. New York: WH Freeman
28. Mayr E (1998) Two empires or three? Proc Natl Acad Sci USA
95:97209723
Acknowledgments The extensive historical collections at the University of
29. Minchin EA (1912) An introduction to the study of the protozoa.
Massachusetts at Amherst, Mount Holyoke College, and Smith College
London: Edward Arnold
libraries afforded me a wealth of resources. I would like to thank Gina
30. Owen R (1855) Lectures on the Comparative Anatomy and Physiology
Douglas (Linnean Society, London) for correspondence by John Hogg,
of the Invertebrate Animals. 2nd edn. London: Longman, Brown, Green &
and Mark Ragan (Canadian Institute for Advanced Research, Halifax)
Longmans
for providing me with research material. I especially thank Ricardo
Guerrero (University of Barcelona) for his generous editorial assistance,
31. Owen R (1858) Palaeontology. In: Encyclopedia Britannica. 8th edn.
Jim Strick (University of Arizona) for insight, and Lynn Margulis
17:91176
(University of Massachusetts at Amherst) for that spark of inspiration.
32. Owen R (1860) Palaeontology. Edinburgh: Adam and Charles Black
33. Pritchard A (1861) A History of Infusoria. London: Whittaker and Co
34. Ragan M (1997) A third kingdom of eukaryotic life: history of an idea.
Arch Protist 148:225243
35. RaganM (1998) On the delineation and higher-level classification of
References
algae. EurJ Phycol 33:115
36. Richmond M (1989) Protozoa as precursors of metazoa: German cell
1. Agassiz L (1859) An Essay on Classification. London: Longman,
theory and its critics at the turn of the century. J Hist Biol 22:243276 37.
Brown, Green, Longmans & Roberts
Rothschild L (1989) Protozoa, Protista, Protoctista: whats in a name? J
2. Andersen RA (1998) What to do with protists? Aust Syst Bot
Hist Biol 22:277305
3. 11:185201 Bradbury S (1967) The Evolution of the Microscope. London: Pergamon
38. Shapiro JA, Dworkin M (eds) (1988) Bacteria as multicellular
4. Calkins G (1911) The scope of Protozoology. Science 34:129138
organisms. New York: Oxford University Press
5. Cavalier-Smith T (1983) A 6-kingdom classification and a unified
39. Siebold CT von (1854) Anatomy of the Invertebrata. Boston: Gould
phylogeny. In: Endocytobiology II. Berlin: DeGruyter, pp 10271034
and Lincoln

216

INTERNATL MICROBIOL Vol. 2, 1999

40. Sogin M (1996) Ancestral relationships of the major eukaryotic

lineages. Microbiologa SEM 12:1728
41. Stanier R, van Neil C (1962) The concept of a bacterium. Archiv fur
Mikrobiologie 42:1735
42. Stanier R, Doudoroff M, Adelberg E (1963) The microbial world. 2nd
edn. Englewood Cliffs, NJ: Prentice-Hall
43. Whittaker RH (1957) The kingdoms of the living world. Ecology
38:536538
44. Whittaker RH (1959) On the broad classification of organisms. Quart
Rev Biol 34:210226
45. Whittaker RH (1969) New concepts of kingdoms of organisms. Science
163:150160

Scamardella

46. Whittaker RH, Margulis L (1978) Protist classification and the

kingdoms of organisms. BioSystems 10:318
47. Wilson T, Cassin J (1863) On a third kingdom of organized beings. Proc
Acad Nat Sci Phila 15:113121
48. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system
of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.
Proc Natl Acad Sci USA 87:45764579
49. Woese CR (1998) Default taxonomy: Ernst Mayrs view of the microbial
world. Proc Natl Acad Sci USA 95:1104311046