Botanical Journal o/Ihe Linnean Society (19811, 82: 93-119. With 1 7 figures
Notes on the taxonomy and nomenclature of
the algal classes Eustigmatophyceae
and Tribophyceae (synonym Xanthophyceae)
D. J. HIBBERD
Culture Centre of Algae and Protozoa, 3 6 Storey’s Way,
Cambridge CB3 ODT
Acceptedforpublication January 1980
The systematics of the Eustigmatophyceae are revised at the level ofspecies, genus, family and order.
All known species are included in the Eustigmatales, which is divided into four families: the
Eustigmataceae Hibberd includes Eustzgmatos Hibberd and Vischeria Pascher, each with three species;
the Pseudocharaciopsidaceae includes only Pseudocharaczopsis Lee & Bold with two species; the
Cliloi-obotryaceae includes only Chlorohotlys Bohlin with one species and the Monodopsidaceae
includes Monodopsis Hibberd with one species and Nannochloropsis Hibberd with two species.
Eustigmatophyta and Eustigmatophyceae are published as typified names for the division and the
class, respectively, both based o n Ewtzgmatos. Tribophyceae, based o n Tribonema, is published as the
typified name for the class previously called Xanthophyceae. Nannochloris coccoides Naumann is chosen
as lectotype of the chlorophycean genus Nannochloris Naumann.
K E Y WORDS: -Eustigmatophyceae
Xanthophycrar.
nomenclature
-
taxonomy
-
Tribophyceae
-
-
CONTENTS
Introduction
. . . .
Materials and methods
.
Identity otcultures
. .
Taxa above the rank of family
Families, genera and species
. .
Eustigmataceae
Pseudocharaciopsidaceae
Chlorobotryaceae
Monodopsidacear
.
Discussion
. . . . .
Acknowledgements
. .
References
. . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
93
94
94
95
101
101
107
111
113
116
117
117
INTRODUCTION
The algal class Eustigmatophyceae was segregated from the Xanthophyceae
(Hibberd & Leedale, 1970, 1971, 1972) on the basis of a cytological and
ultrastructural study of 15 strains of yellow-green algae and this step was
subsequently supported by evidence of chloroplast pigment composition
93
0024-4074/8 1/020093 + 27$02.00/0
7
0 198 1 The Linnean Society of London
94
D. J. HIBBERD
(Whittle, 1976; Whittle & Casselton, 1969, 1975).Present knowledge of the group
was reviewed by Loeblich & Loeblich (1978) and Hibberd (1980). The new class
has been generally accepted by phycologists, with the exception of Fott (1974).
Six species were originally included in the Eustigmatophyceae (Hibberd &
Leedale, 1970, 1971) and other taxa have been added since (Lee & Bold, 1973;
Antia, Bisalputra, Cheng & Kalley, 1975). Some of the taxonomic and
nomenclatural problems resulting from the transfer of taxa from the
Xanthophyceae (re-named below as Tribophyceae) to the Eustigmatophyceae
have been outlined by Hibberd 8c Leedale (1972) and Silva (1979) but the
systematics of the group remains confused. The purpose of this paper is to revise
the Eustigmatophyceae at the generic level, to provide a valid classification above
the level of genus and to publish typified names for the division Eustigmatophyta
and the classes Eustigmatophyceae and Tribophyceae in accordance with the
International Code of Botanical Nomenclature, Leningrad (I.C.B.N., 1979).
MATERIALS AND METHODS
The majority of the strains investigated were obtained from the Culture Centre
of Algae and Protozoa, Cambridge (CCAP) (George, 1976); the Culture
Collection of Algae at the University of Texas (UTEX, formerly at Indiana
University) (Starr, 1978); Sammlung von Algenkulturen, Gottingen (GO)(Koch,
19641, and the Culture Collection of Autotrophic Organisms, Prague (PRA)
(Baslerova and DvoEakova, 1962).These strains with their collection numbers are
included in Table 1. In addition, the following were obtained from the
Collection of the Institute for Botanical Systematics, Innsbruck (Gartner, 1976):
Pleurochloris magna J. B. Petersen - strains S1 (now CCAP 887/4), S2, T8 (now
CCAP 860171, V1, V2; Pleurochloris po(yphem Pitschmann - strains IB 207 (now
CCAP 860/8), IB 208 and Vzscheria punctata Vischer - strain T10 (now CCAP
88713). Cultures of the alga listed in Adamson 8c Sommerfeld (1978) as
Pleurochloris pyrenoidosa Pascher was supplied by Mr R. P. Adamson (now CCAP
86015 and 86016); Dr P. A. Broady provided an isolate of Eustigmatos vischeri
Hibberd (no. IA 29).
Most strains were axenic and stocks were maintained on nutrient agar slopes
containing the following: proteose peptone (Difco) 0.1%; KNO, 0.02%; K,HPO,
0.002%; MgSO,. 7H,O 0.002%. Agnotoxenic strains were maintained on slopes
having the same mineral composition but with the proteose peptone replaced by
10% by volume soil extract. Experimental cultures were grown in liquid standing
batch cultures of either Bold’s Basal Medium (Bischoff & Bold, 1963) with soil
extract added to 10%;in the soil extracdmineral medium described above; or in
biphasic (soil/water) media utilizing a range of different soil types. No attempt
was made to keep the experimental cultures bacteria-free since it was soon found
that this made no difference to the morphology of the cells. The morphology of
the strains was compared in these various media in a range of temperatures and
illumination regimes.
IDENTITY OF CULTURES
Initial attempts to resolve some of the taxonomic and nomenclatural problems
resulting from removal of several species of Tribophyceae into the
Eustigmatophyceae were hampered by the discovery that two CCAP strains,
Pleurochloris magna (86012) and Vischeria stellata (R.Chodat ex Poulton) Pascher
T A X O N O M Y O F EUSTIGMATOPHYCEAE
Y i
(887/2) did not agree with the earlier descriptions of the same strains by Vischer
(1945) and Poulton (19251, respectively. In the case of I/. stellata (887/2), the
culture used for the present investigation, which started in 1974, appeared
different from the culture received from CCAP in 1964. These discrepancies led
to a detailed comparative investigation extending over a number of years of all
eustigmatophyceari strains at CCAP listed under the generic names Vischeria,
Polyedriella and Pleurochloris and their equivalents at UTEX, GO and PRA. Each of
the strains concerned originated from the same source and should have been
identical. The results of this comparison are listed in Table 1 which gives the
origin and numbers of the various strains; the name under which they were
originally held; their identity previous to the present revision; changes made in
the collection listings as a result of the transmission of this information to the
curators of the collections and their names resulting from the present taxonomic
revision. I t can be seen that the confusion over identity extended further than the
two CCAP strains already mentioned. Some of the discrepancies could be
accounted for by errors in subculturing but, in the case of Pleurochloris magna, it
appears that Vischer’s original isolate must have been lost and somehow
replaced by a strain of Vischeriapunctata in the interval between its description by
Vischer (1945) and the formation of the collections at Gottingen and Indiana
from the Cambridge collection in 1953.
TAXA ABOVE. T H E RANK O F FAMILY
The principles of typification and priority do not necessarily apply to taxa
above the rank of family according to the current (Leningrad) International
Code of Botanical Nomenclature (I.C.B.N., 1979). However, names of taxa in the
higher ranks are now considered as automatically typified when they are
ultimately based on generic names (Art. 16). The application of the priority
principle to all typified names is recommended but is not mandatory (Art. 11.4).
Following the recent replacement, under the new rules, of several descriptive
algal class names with typified names (Hibberd, 1976; Christensen, 19781, a
different and typified name is proposed here for the Xanthophyceae P. Allorge ex
Fritsch (the Heterokontae of Luther). Similarly, the descriptive name
Eustigmatophyceae is replaced by the same name based o n a newly included
genus Eustigmatos ; a new division and order are also based on the same generic
name.
Tribophyceae Hibberd, nomen classis nova typificatum
SYNONYMS: Heterokontae Luther, Bihang till K . Svenska vetenskapsakadamiens
handlingar, 2 4 , ZIZ, 13: 1 7 ( 1899).
Heterocontae Oltmanns, Morphologie und Biologie der Algen, I : 18 ( 1904).
Xanthophyceae P. Allorge ex Fritsch, The Structure and Reproduction Ofthe Algae I :
470 (1935).
Algae eucaryotae chlorophyllo a cum chlorophyllo c et pigmentis
carotenoidibus, i.a. diatoxanthino, photosyntheticae. Cellulae plerumque
solitariae, coccoides, chloroplastis viridibus vel flavo-viridibus discoidibus.
Polysaccharum penarium solidum bene limita nulla. Pyrenoida ubi praesentia et
in cellulis vegetativis et in zoosporis manifesta, semiimmersa, lamellis non
96
D . J. HIBBERD
dd
CCAP 822/1
CCAP 864/1
LJTEX 21 13
CCAP810/1
CCAP 848/1
UTEX 151
CCAP 849/1
UTEX 2 164
Ellipsoidion acuminatum Pascher
Westldkr, 1955 a5 E . oocystoideb
t’\rudothnraci[i~\i~luxrrc\i\ Lee & Bold
Tupa, 1969
Chlorobotrys regularis (W. West) Bohlin
H ibhci-d, 1967
Muuodu\ \ubtrrraneu\ J . B. Pcic‘iwi
Nnnnochlun \ oculaln Droop
D i o o p , pie 1955
,Moiiallan/u~whna B o u i - Iclly
Mae\tIini, 1967
Lewin, 1949
CCAP 860/4
860/ 1b
CCAP 860/la
GOT 860/1
PRA A 295
UTEXSIO
l’/i,uio(ldori\ m a p i J B. Pelei \cii
blint, p w 1974, N o . 3 2
I’/rurothlon\ tumi/mlala w u \ u V I X ~ I C-[ICCAP
Flint, p I c s 1974, N o . 27
Pleurochloris commutata sensu Vischer
Vischei- 1940, No. 241
b
Nannochloris oculata
Monodus subterraneus
Chlorobotrys regularii
Nannochloropsis salina Hibberd
Nannochloropsis oculata Droop
Petersen) Hibberd
Monodopsis subterranea (J. B.
Chlorobotryr regularis Bohlin
Pieudocharaciopsts minula (Braun)
H ib berd
Pseudocharactupsis ovalts (Chodat)
Hi bberd
Characiopris ovalts
Pseudocharactopsis texensts
Lustigmatus magnui (J. B .
Petersen) Hibberd
Eusttgmatos vascheri Hibberd
Plrurochlol-ir magna
Pleurochloris commutata
D. J. HIBBERD
98
penetrata. Membrana haud raro e binis partibus composita altera alteri
superposita. Zoosporae nudae, plerumque ovoides, bilateraliter symmetricae,
flagellis binis inaequalibus subapicalibus natantes. Pars transitoria cuiusque
flagelli helicem praebens. Flagellum longius porro directum, mastigonematibus
tubularis lateralibus obsessum; brevius mastigonematibus carens, prope basem
ad unum latus incrassaturn, hic copori cellulae adpressum. Chloroplasti
plerumque discoides, thylacoidibus ternis in strues conjunctis, lamella cingulari
plerumque alias cunctas involvente. Stigma chloroplasto immersum,
plasmatolemmati sub ipsa parte incrassata flagelli brevioris contiguum. Nucleus
singulis, pyriformis, parte attenuata corpusculis basalibus flagellorum
appropinquata, involucro pro more cum parte reticuli endoplasmatici
chloroplastos induente continuo. Corpusculum Golgianum parvum, parabasale,
nucleo appositum.
Eukaryotic algae with chlorophyll a and chlorophyll c and carotene pigments
including diatoxanthin. CELLS mostly solitary, coccoid, with discoid green or
yellow-green chloroplasts. No clearly delimited solid storage polysaccharide.
Pyrenoids when present occurring in both the vegetative cell and the zoospores,
semi-immersed, matrix not traversed by lamellae. Cell wall sometimes composed
of two overlapping parts. ZOOSPORES naked, mostly ovoid, bilaterally symmetrical, bearing 2 unequal flagella inserted subapically. Flagellar transition region
with a transitional helix. Long flagellum directed anteriorly bearing tubular
mastigonemes laterally, short flagellum smooth with a lateral swelling at its
proximal end, applied to the surface of the cell. Chloroplasts usually discoid
with 3- thylakoid lamellae and usually a girdle lamella. Eyespot intraplastidial,
the region of the chloroplast containing it closely applied to the plasmalemma in
the region overlain by the swelling on the short flagellum. Nucleus single,
pyriform, with its pointed end close to the flagellar basal bodies, nuclear
envelope typically confluent with the chloroplast endoplasmic reticulum. Golgi
body present, small, parabasal, lying close to the nucleus.
Tribonema Derbes & Solier in Castagne, Catalogue des plantes qui croisent naturellement aux environs de Marseille. Supplement. Aix: 96 ( 185 1).
TYPE :
The order Tribonematales Pascher ( 1939) and family Tribonemataceae Pascher
(1912) are both based on the genus Tribonema Derblts & Solier.
Eustigmatophyta Hibberd, divisio nova
Eustigmatophyta Hibberd, British Phycological Journal, 7 : 28 1 ( 1972),
nomen nudum.
SYNONYM:
Algae eucaryotae chlorophyllo a et pigmentis carotenoidibus, i.a. violaxanthino,
photosyntheticae. Cellulae plerumque solitariae, coccoides, plerumque
chloroplasto singulari viridi vel flavoviridi parietali. Pyrenoides speciebus
plurimis praesens sed non nisi in cellulis vegetativis numquam in zoosporis;
pyrenoides plerumque magnum e superficie chloroplasti in caudiculo angustato
exstans, laminis materiae photosynthese factae quae per microscopium
electronicum subtiliter lamellata esse videtur, circumnexum; matrix pyrenoidis
thylakoidibus non transita. Zoosporae nudae, plerumque lageniformes, duabus
trientibus posterioribus corporis complanatis extremo angustato oblique
truncato. Cellula aut flagello uno et corpore basali secundo aut flagellis duobus
T A X 0 N 0 MY 0 F EUSTI GM A T 0 PHY CEAE
99
instructa ; flagella subapicaliter inserta. Pars transitoria flagellorum helicem
praebens. Flagellum (longius ubi duo emergentia) prorsum exstans,
mastigonematibus tubularibus bilateraliter dispositis instructum; flagellum
alterum (ubi emergens) multo brevius q u a m illud longius, sine
mastigonematibus et lateraliter exstans vel retroflexum. Tumor flagelli ex
expansione vaginae dilatatae flagelli; ad basem flagelli pilosi factus, semper ad
membranam cellulae prope stigma appressus. Chloroplastus unus, elongatus,
lamellis trium thylacoidum compositus, sine lamella cinguliformi. Stigma
grande, miniatum, in extremitate anteriore cellulae mobilis locatum,
chloroplasto nihil cohaerens, ex guttulis nullis membranis contentis compositum
et sine membrana ipsum totum continente. Nucleus unus, inter stigma et
extremitatem anteriorem chloroplasti positus. Connectio nulla inter involucrum
nuclei et reticulum endoplasmicum quod chloroplasturn continet. Zoosporae
flagello uno corpusculis Golgianis carentes, zoosporae flagellis duobus
corpusculo Golgiano parabasali instructae. Propagatio vegetativa per
divisionem in autosporas duas vel quatuor, rarenter per zoosporas, effecta.
Status dormientes non cogniti. Reproductio sexualis ignota.
Eukaryotic algae with chlorophyll a and carotene pigments including violaxanthin. CELLS mostly solitary, coccoid, mostly with a single green or yellow-green
parietal chloroplast. Pyrenoid present in most species but only in the vegetative
cells, not the zoospores; pyrenoid usually large, projecting from the inner face of
the chloroplast on a narrow stalk, surrounded by plates of a photosynthate which
appear finely lamellate in the EM; pyrenoid matrix not traversed by thylakoids.
ZOOSPORES naked, lageniform with the posterior two-thirds of the body flattened,
the narrow end obliquely truncate. Either 1 flagellum and a second short basal
body or 2 flagella; flagella inserted subapically. Transitional region of the flagella
with a transitional helix. Flagellum (the longer when 2 are emergent) directed
anteriorly, with a bilateral array of tubular mastigonemes ; second flagellum,
when emergent, much shorter than the long one, smooth and directed laterally or
posteriorly. A flagellar swelling consisting of an expansion of the dilated flagellar
sheath at the proximal end of the hairy flagellum, always closely applied to the
cell membrane in the region of the eyespot. Chloroplast single, elongate, with
3-thylakoid larnellae; no girdle lamella. Eyespot a large orange-red body at the
extreme anterior end of the motile cell, completely independent of the single
chloroplast, consisting of an irregular group of droplets without bounding membranes and with no membranes around the whole complex. Nucleus single, lying
between the eyespot and the anterior end of the chloroplast; no direct connexion
between the nuclear envelope and the endoplasmic reticulum which bounds the
chloroplast. Golgi body absent from uniflagellate zoospores; a single parabasal
Golgi body in biflagellate zoospores. Vegetative propagation by division into 2 or
4 autospores, more rarely by the production of zoospores. Resting stages and
sexual reproduction unknown.
TYPE:
Eustigmatos Hibberd.
It may reasonably be argued that recognition of the division Eustigmatophyta
containing the single class Eustigmatophyceae (Margulis, 1974 ; Loeblich &
Loeblich, 1978) constitutes “excessive hierarchical inflation” (Silva, 1979).
However, in discussions of algal phylogeny the concept of such a division has
several times proved useful, particularly in contrasting the distinctive
D. J. HIBBERD
100
organization of eustigmatophytes with that of the strictly heterokont groups
Tribophyceae, Chrysophyceae, Fucophyceae (= Phaeophyceae) and
Bacillariophyceae which, with or without the Raphidophyceae, have been
considered as classes in a single ‘natural’ division Heterokontophyta (Hibberd,
1969; van den Hoek, 1978; Leedale, in ress). (Leedale, in press, also includes
the Oomycetes in this division.) One less inflationary’ alternative, that of grouping the Eustigmatophyceae together with the Prymnesiophyceae, Cryptophyceae,
Dinophyceae and Raphidophyceae as well as the heterokont classes in the single
division Chromophyta sensu Christensen ( 1962) results in a highly polyphyletic
group, impossible to define sensibly in terms of cell structure. Nevertheless,
Chromophyta is still useful as a term to contrast this assemblage with the more
distantly related chlorophyll b - containing Chlorophyta and the red algae,
Rhodophyta. Since it is probable that a variety of concepts of divisional limits
within the algae will be in use at any one time and that some will include a
eustigmatophyte division, it seems sensible to publish its name validly. The name
proposed is based on the genus Eustigmatos and thus automatically typified.
P
Eustigmatophyceae Hibberd, classis nova
Eustigmatophyceae Hibberd 8c Leedale, Nature, London 225 : 758
(19701, nomen nudum.
Eustigmatophyceae Hibberd 8c Leedale, Taxon, 20: 524 (197l), nomen descr+tivum.
SYNONYMS:
TYPE : Eustigmatos H ibberd.
The descriptive name Eustigmatophyceae, although validly published, cannot
be regarded as typified under Article 16.1 of the I.C.B.N. since at the time of its
publication it was not based on the name of an included genus. I t is therefore
proposed that the name Eustigmatophyceae be based on the genus Eustigmatos
described below, and that from this time it be regarded as automatically typified.
Eustigmatales Hibberd, ordo novus
Pseudocharaciopsidales Lee 8c Bold, Phycological Studies, XII, Austin:
69 (19741, nomen nudum.
SYNONYM :
Eustigmatophyceae unicellulares membrana genuina, non affixae vel per
stipitem substrato a f b a e . Reproductio per zoosporas et aplanosporas effecta.
Unicellular Eustigmatophyceae with a true cell wall. Free living or attached to the
substratum by means of a stipe. Reproduction by zoospores and aplanospores.
TYPE:
Eustigmatos Hibberd.
The number of known eustigmatophytes is small and all are unicells possessing
cell walls; it seems reasonable, therefore, to place them all in a single order. (If
flagellate or filamentous forms should be discovered, they might be classified
in one or more separate orders.) The order Eustigmatales is erected here to
include all such species whether attached or free-living. The name
Pseudocharaciopsidales Lee 8c Bold was published without a description or
discussion of ordinal limits (Lee & Bold, 1974), although apparently it included
only Pseudocharaciopsis texensis Lee 8c Bold, a species in which the cells are attached
by a stipe to the substratum. Should separation of coccoid forms at the ordinal
TAXONOMY O F EUSTIGMATOPHYCEAE
101
level ever be envisaged, the name Pseudocharaciopsidales could be taken up
again, validated and used for an order including only stipitate forms.
FAMILIES, GENERA A N D SPECIES
Although only a very small number of eustigmatophytes has so far been
described, they may be considered as forming four families differentiated by
vegetative cell structure, ability to produce motile cells and motile cell structure.
.Key to thefamilies
1.
1’.
3.
3’.
Reproductionatleastpartlybymeansofzoospores . . . . . . 2
Reproduction always azoosporic
. . . . . . . . . . . 3
Cells more or less isodiametric, free-floating; zoospores
2.
with a single emergent flagellum. . . . . . Eustigmataceae
2’. Cells ovoid/ellipsoidal, capable of producing a stipe and
discoid attaching structure; zoospores with two emergent
flagella . . . . . . . . . . Pseudocharaciopsidaceae
Cells mostly greater than 10 pm and in pairs, surrounded by
lamellate mucilage . . . . . . . . . . Chlorobotvaceae
Cells less than 10 km in diameter, solitary, without mucilage
layers . . . . . . . . . . . . . . Monodopsidaceae
Eustigmataceae
Eustigmataceae Hibberd, familia nova
Eustigmatophyceae unicellulares, plus minus isodiametricae, sphaericae aut
polyedricae aut stellulatae. Zoosporae elongate lageniformes, complanatae,
flagello emergente cuique unico natantes.
Unicellular Eustigmatophyceae with more or less isodiametric cells, either
perfectly spherical or polyhedral or stellate. Zoospores elongate lageniform,
flattened, with a single emergent flagellum.
TYPE : Eustigmatos
Hibberd.
Taxa in this family show all of the unusual features of motile and vegetative
cell structure which ultimately led to the separation of the Eustigmatophyceae
from the Tribophyceae. Members of this family are easily recognized using the
light microscope, the vegetative cells by their large polyhedral pyrenoids and
typically a reddish globule and large vacuole, the zoospores by their unusual
shape, single flagellum and large red extraplastidial eyespot at the anterior end.
Key to the genera
1.
1’.
Cell wall always smooth and featureless
. . .
Cell wall typically raised into projections or ridges
.
.
.
. . . .
Eustigmatos
Vzscheria
Eustigmatos Hibberd, genus novum
Since a new generic name was needed for eustigmatophytes
previously known under the name Pleurochloris (see below), one with a suitable
DERIVATION:
D . J. HIBBERD
102
root was chosen in order that the existing class name, Eustigmatophyceae could
be retained as a typified name. E u s t i p Gardn. ex Champ. is a genus in the
angiosperm family Hamamelidaceae and is therefore unavailable. The adjectival
Eustigmatos ( ~uazzyyazoawell-equipped with an eyespot)was chosen instead.
Eustigmataceae plerumque sphaericae, membranis laevibus, ornamentis
carentibus.
Eustigmataceae with mostly spherical cells, cell wall smooth and unornamented.
T Y P E :Eustigmatosvischeri Hibberd.
Key to species
1.
1'.
of Eustigmatos
Cells mostly 7-9pm in diameter, cells larger than 20pm never
produced in culture . . . . . . . . . .
Eustigmatos vischeri
Cells mostly 9-18 pm in diameter, cells larger than 20 pm may or
may not be produced in culture . . . . . . . . . . . . 2
2. Cells mostly 9-18pm in diameter, but some 20-50pm cells
produced in culture
. . . . . . . . Eustigmatos magnus
2'. Cells mostly 11-15 pm in diameter, cells larger than 20 pm
rarelyproducedinculture . . . . . . . Eustigmatospolyphem
Eustigmatos vischeri'Hibberd, sp. nova
SYNONYM : Pleurochloris commutata sensu Vischer Ergebnisse der wissenschaftlichen
Untersuchungder Schweizerischen NationaLparks, I : 484 (1945),non Pascher (1925:46).
Cellulae solitariae, sphaericae, plerumque 7-9 pm diametro. Chloroplastus
singulus, lobatus, parietalis, pyrenoide polyedrica stipitata. In cellula matura et
vacuola contentis granularibus et globulus rubens adsunt. Reproductio aut per
zoosporas aut per autosporas effecta; autosporae duae vel quattuor, initio mutue
compressae in pariete cellulae maternae, itaque tetraedrae vel complanatae;
zoosporae lageniformes flagello singulo antico emergenti, stigmate prominenti
extra chloroplasti ad cellulae extremitatem anticam et chloroplasto singulo
pyrenoide carenti instructae.
Cells solitary, spherical, mostly 7-9 pm in diameter. Chloroplast single, lobed,
parietal, with a stalked polyhedral pyrenoid. A vacuole with granular contents
and a reddish globule developing. Reproduction either by production of 2 or 4
autospores, at first tetrahedral or flattened by mutual compression within the
mother cell wall, or by lageniform zoospores with a single anterior emergent
flagellum, prominent extraplastidial eyespot at the anterior extremity and a
single chloroplast lacking a pyrenoid.
TYPE: Fig. 1
The genus Pleurochloris originally included only P. commutata (Pascher, 19251,
which is therefore the type species of the genus. In 1945 Vischer isolated and
described a strain which he tentatively identified as P. commutata. However, recent
investigation of a descendant of that isolate (Hibberd & Leedale, 1972)showed it
to be quite different. Pascher described P. commutata as having spherical to ovoid
cells 3-7 pm in diameter with a single bowl-shaped chloroplast; its zoospores
were said to be very variable in shape, becoming amoeboid, containing a single
TAXONOMY O F EUSTIGMATOPHYCEAE
10s
contractile vacuole and one chloroplast without eyespot, and bearing 2 unequal
flagella, one slightly longer than the cell body and the other up to a quarter this
length. Vischer’s strain, in contrast, produces elongate lageniform zoospores
with a single emergent flagellum and a large anterior extraplastidial eyespot
(Hibberd & Leedale, 1972). This organism cannot be identified with any
previously described taxon and is therefore described here as a new species.
The taxonomic position of the genus Pleurochloris (governed by that of
P. commutata) is uncertain. It was originally placed in the Tribophyceae
(Xanthophyceae) (Pascher, 1925:1, but certain features such as the absence from
the zoospores of an intraplastidial eyespot, the presence of a single, parietal,
lobed chloroplast in the vegetative cells and the production of 2 or 4 autospores
which have their faces at first flattened by mutual compression in the mother cell
suggest that P. commutata might be a eustigmatophyte. On the other hand, two
important characters that would have confirmed this affinity are not illustrated
or described: no information is provided concerning the occurrence of a large
red extraplastidial eyespot at the anterior end of the zoospore nor for polyhedral
pyrenoids in the vegetative cell (which Pascher would have described as
“Eiweisskristalle”). However, even if P. commutata is eventually found to be a
eustigmatophyte it may be distinguished from presently recognized genera by the
combination of spherical cells which are always free-floating and biflagellate
zoospores. All other known spherical free-floating eustigmatophytes have
uniflagellate zoospores while the only other forms producing biflagellate
zoospores possess cells that may become attached by a stipe to the substrate.
Eustigmatos uischeri differs from E. magnus and E. polyphem in possessing
relatively small cells with a restricted size range. I t is represented in
culture collections by Vischer’s original isolate, by CCAP no. 860/lb, an
isolate from New Zealand soil, and by Innsbruck no. T8 (CCAP 860/7), originally
listed as Pleurochloris magna. Other strains which have been identified as this
species have been received from Dr E. A. Flint (nos 15, 16A, 19 from New Zealand
as ‘Polyedriella sp.’); from Dr P. A. Broady (isolate IA 29 from Iceland); and 2
isolates from Mr R. P. Adamson as Pleurochloris pyrenoidosa Pascher (CCAP 860/5,
860/6). With the exception of the latter these strains were isolated from soil
samples and E . uischeri thus appears to be a relatively common component of the
soil flora. The strains from M r Adamson were isolated during a survey of the
algae in swimming pools in the Phoenix, Arizona, metropolitan area, when it was
found that E . uischeri was the most common species, occurring in 67%of the pools
surveyed (Adamson 8c Sommerfeld, 1978). It forms such conspicuous growths on
the pool sides that it has acquired the common name of ‘mustard algae’. Inoculation from wind-blown soil during dust storms is possibly the reason for the
frequent occurrence of E . uischeri in the pools (R. P. Adamson, personal
communication).
Eustigmatos magnus (J. B. Petersen) Hibberd, comb. nova
SYNONYM: Pleurochloris magna
( 1932).
ILLUSTRATIONS Figs 2-4.
J . B. Petersen, Archiu f u r Protistenkunde, 76: 404
I t is clear from Petersen’s description of “albumen crystals” in the vegetative
cells and elongate, uniflagellate zoospores with a “refractive body” (eyespot) in
the anterior end, that Pleurochloris magna is a eustigmatophyte. I t cannot be placed
D. J. HIBBERD
104
in the genus Pleurochloris, for the reasons given above, and so it is transferred to
Eustigmatos because it produces only spherical or ovoid and never angled or
stellate cells. I t differs from E. uischeri in having generally a greater range of cell
size and from E. uischeri and E. polyphem in its potential for producing in culture a
proportion of very large cells.
Confusion over the identity of eustigmatophytes in culture collections is
particularly significant in the case of this species. As described above (Table 1) it
was discovered that all of the strains labelled “Pleurochloris magna” agreed with
both the original description and the still available ‘type’ strain of Vischeria
punctata. The isolate of P. magna believed to be shared by the various collections
was isolated by Vischer in 1941 (Geiger-Huber & Vischer, 1947). It is clear from
his description of this material (Vischer, 1945), that he had indeed obtained
P. magna sensu Petersen, for he recorded even greater dimensions for the very
large cells characteristic of the species than were noted by Petersen. Therefore,
Vischer’s strain must have been lost and replaced, in some unknown way, by a
strain of Vzscheria punctata which was isolated and described at the same time.
Thus the studies of Hibberd & Leedale (1970, 197 1, 1972)on the strain thought
to be P. magna were actually on V.punctata. During these investigations the
irregularly stellate or angled cells characteristic of V.punctata were seen
occasionally and it was thought that this might have been a feature of P. magna
overlooked by Petersen and Vischer. The true situation only became apparent
after a detailed comparative study of all eustigmatophycean strains in culture had
been made and when a new isolate, clearly identical with P. magna, was sent from
New Zealand to Cambridge by Dr E. A. Flint in 1974. Eustigmatos magnus is
presently represented in the culture only by CCAP 806/4 (Flint no. 32).
Eustigmatos polyphem (Pitschmann) Hibberd, comb. nova
SYNONYM :
Pleurochloris polyphem Pitschmann, Osterreichische botanische Zeitschrzjl,
116: 489 (1969).
While it seems sensible to retain E. vischeri and E. magnus as separate species,
the taxonomy of several strains in the Innsbruck collection is problematic. These
strains, listed as Pleurochloris polyphem (nos IB 207 (=CCAP 860/8), IB 208) and
P. mugna (nos. S2, V1, V2), have spherical cells which are mostly 10-1 1ym in diameter with a maximum of c. 15pm. Under identical conditions of culture most
cells of E. uischeri are 7-9pm in diameter while E. mugrzus produces many cells in
the size range 20-45pm. Although Pitschmann (1969) describes cells of up to
34pm in diameter for P . polyphem, study of the same isolate shows that they are
not typical of this strain. Thus, while the strains in question fall within the size
range given for the majority of cells of Pleurochloris mugna by Petersen ( 1932)they
rarely achieve the maximum of 2 1pm reported by him and certainly not the
diameters of 50pm recorded by Vischer, or the 45ym of the present study. For
these reasons it has been decided to retain P. polyphem as a separate species and
not to follow Ettl (1978) who places it in synonomy with P. magna. Pitschmann
differentiates P. polyphem from other species mainly on the basis of the size and
shape of the zoospores, but their appearance does not differ significantly from
that of the other species in the Eustigmataceae. For the reasons given above,
P. polyphem is referred to the genus Eustigmatos.
T A X O N O M Y OF EUSTIGMATOPHYCEAE
105
Vischeria Pascher
TYPE: V . stellata (Poulton) Pascher (lectotypified by Starmach, 1968: 155).
The genus Vischeria was established by Pascher (1937) for basically spherical
Tribophyceae in which the cell wall is typically raised into projections grading
from a small number of relatively large rounded swellings to a large number of
conical projections. In culture the great majority of cells may have completely
smooth, unornamented walls. Pascher considered Vischeria to be closely related to
Polyedriella, which contained species with polyhedral cells, and the difference between the projections of Vischeria and the ridges of Polyedriella was considered to
be only a matter of degree. The description of V . punctata by Vischer ( 1945) made
the distinction between the two genera even more blurred and recent studies of
the available strains have further demonstrated their basic similarity (Hibberd &
Leedale, 197 1). The limits of Vischeria are therefore slightly broadened to encompass all eustigmatophytes with isodiametric free-floating cells in which the cell
wall is elaborated into projections or ridges. Zoospores of all species are uniflagellate (but see below), elongate-lageniform and indistinguishable from those of
Eustigmatos.
Study of‘these taxa is complicated by the fact that they may produce completely
smooth cells which are also indistinguishable from species of Eustigmatos. However, there is hardly any gradation between the angled cell types and the form
of the typical cells thus remains a reliable character even though in cultures
dominated by smooth-walled cells they can sometimes be found only by careful
searching.
Kej to species ofvischeria
1.
1’.
Cells with wall projections relatively frequent in culture, spheriVischeria stellata
cal ; projections small, conical and evenly distributed
Cells with wall projections relatively infrequent in culture,
polyhedral
. . . . . . . . . . . . . . 2
2. Cells mostly 7-9 ym in diameter; polyhedral cells
infrequent in culture, irregularly pentagonal or hexagonal
in optical section, generally smaller than the spherical cells
in the same culture . . . . . . . . .
Vischeria punctata
2 ’ . Cells mostly 9-1 1 ym in diameter; polyhedral cells very rare
in culture, mostly very irregularly rhomboid or pentagonal
in optical section, similar in size to the spherical cells in the
same culture . . . . . . . . . . .
Vischeria heluetica
Vischeria stellata (R. Chodat ex Poulton) Pascher, Heterokonten. Rabenhorst’s K?yptogamen-flora uon Deutschland, osterreich und der Schweiz. Leipzig. Bd. 1I, Lit$ 41559
(1938).
SYNONYM : Chlorobotrys stellata R. Chodat ex Poulton, htude sur les Heterokontes These
no. 777 Universite‘ de Gentua, Geneva: 7 (1925).
ILLUSTRATIONS:Figs 6, 7 .
Vischeria stellata is distinguished from the two species described below by the
fact that the relatively large number of conical projections of the cell wall are so
regularly distributed that the cells do not depart significantly from an overall
D. J. HIBBERD
106
spherical shape. Poulton’s (1925, 1926) observations of zoospores with two unequal flagella cannot be reconciled with the later observations of Hibberd &
Leedale (1972) of only a single flagellum.
With regard to the identification of the Cambridge strain of this species as
Vischeria punctata (Table I ) , it is important to note that the culture of V . stellata
obtained from CCAP in 1965 and used by Hibberd & Leedale (1972)was found to
be identical with Chodat’s original isolate. However, in 1974 the strain listed as V .
stellata was found to be V . punctata and V . stellata is now represented at CCAP by a
duplicate of UTEX 312. Innsbruck isolate S1 (=CCAP 887/4), originally listed as
Pleurochloris magna, also appears to be V . stellata.
Vischeria punctata Vischer, Ergebrisse der wissenschaftlichen Untersuchung der
Schweizerischen Nationalpurks, 1: 492 ( 1945).
Vischeria stellata sensu Ettl, Xanthophyceae. I. Teil. Susswatserpora von
Mitteleuropa. Stuttgart Bd. 3: 204 (19781, pro parte.
SYNONYM :
ILLUSTRATIONS:
Figs 8 , g .
Vischer differentiated this species from V. stellata by the fact that cultures
contained a great majority of perfectly spherical cells and only a small
proportion of cells with their walls raised into projections, and that the latter
were somewhat polyhedral in shape with fewer and more irregularly disposed
projections. The present observations on these two species fully support these
distinctions and I do not concur with Ettl (1978) in including V .punctata within
V. stellata. In L‘.punctata the majority of angled cells are 6.25-7.5 km in diameter
and are thus significantly smaller than the spherical cells in the same culture. This
size difference further distinguishes V. punctata from both V. stellata and
V. heluetica in which the cells with projections are similar in size to the spherical
cells in the same culture. Vischer did not see the zoospores of V.punctata but
these are now known to be similar to those of the other large-celled free-floating
eustigmatophytes (Hibberd & Leedale, 1972). V.punctata is represented in culture
by Vischer’s original isolate and Innsbruck no. T10 (CCAP 887/3).
Vischeria helveticu (Vischer & Pascher) Hibberd, comb. nova
Polyedriella helvetica Vischer 8c Pascher in Pascher, Heterokonten.
Rabenhorst’s Kvptogamen Flora von Deutschland Osterreich und der Schweiz. Leipzig
Bd. 11, Le$ 4 : 570 (1938).
SYNONYM:
ILLUSTRATION:
Fig. 10.
The genus Polyedriella originally included only P. irregularis Pascher (Pascher,
1930) and this is therefore the type species. The form of its zoospores is unknown
and the vegetative cells show no features indicating a position in the
Eustigmatophyceae; therefore, it cannot be stated to which class the generic
name Polyedriella belongs. Pascher ( 1938) considered P. heluetica to be closely
related to Vischeria, differing from the various species of this genus known to him
only in the smaller number of cells with wall projections and polyhedral shape.
Vischer (1945), in describing V.punctata, pointed out that this species was
intermediate in cell form between Vischeria stellata and Polyedriella heluetica on the
one hand and the perfectly spherical Pleurochloris species on the other and so
P. heluetica is here placed in the genus Vischeria. The cells of V. helvetica are slightly
T A X 0 N 0 M'k' 0 F E USTI G M A T 0 P HY C EAE
107
larger than those of' V . punctata and V . stellata under the same conditions of
culture but are most easily distinguished by the fact that the pyrenoid is particularly well-differentiated. The pyrenoid in V . heluetica is also generally larger
(diameter 4.5-5pm) than in V. punctata and V . stellata (diameter c. 3.5pm).
Vischeria helvetica is represented in culture only by Chodat's original isolate.
Pseudocharaciopsidaceae
PseudocharaciopsidaceaeLee 8c Bold ex Hibberd, familia nova
Pseudocharaciopsidaceae Lee 8c Bold, Phycologtcal Studies X I I . Austin :
University of Texas: 69 (19741, nomen nudum.
Eustigmatophyceae unicellulares cellulis stipitatis. Zoosporae flagellis duobus
emergentibus instructae.
Unicellular Eustigmatophyceae with stipitate cells. Zoospores with two emergent
flagella.
TYPE: Pseudocharaciopsis Lee &Bold.
The name Pseudocharaciopsidaceae Lee 8c Bold was published without a
description or discussion of familial limits to include only the monospecific
genus Pseudocharaciopsis. It is here established, with the necessary diagnosis, for all
eustigmatophytes capable of producing a stipe and discoid attachment structure.
The zoospores of the two known species with vegetative cells of this type differ
from those in the Eustigmataceae in having a Golgi body and 2 emergent flagella,
the shorter of which is characteristically very narrow for the greater part of its
length, with only 2 component microtubules. This combination of characters
suggests that the species described below may form the basis of a natural group.
SYNONYM :
Pseudocharaciopsis Lee 8c Bold, Phycological Studies XII. Austin: University of Texas :
69 (1974).
TYPE: P . texensis Lee 8c Bold.
The genus Pseudocharaciopsis was established to include forms possessing
vegetative cells which closely resemble cells of species of the tribophycean genus
Characiopsis B o d , which, in turn, resemble species in the chlorophycean
genus Characium Braun. The species described by Lee 8c Bold clearly belongs to
the Eustigmatophyceae on the basis of the structure of both its motile and
vegetative cells. In the original diagnosis these authors include the character of
stalked pyrenoids but the circumscription of the genus is modified here to
include stipitate species producing biflagellate zoospores, whether or not they
possess stalked pyrenoids. This concept may need further modification with the
discovery of new forms but, as discussed below, any other course would be
inadvisable at the present time.
The naming of a eustigmatophycean genus with cells resembling those of
species of Characiopsis is complicated by doubt about the identity of the type
species of Characiopsis. Silva (1979) has pointed out that Borzi (1895) originally
indicated Characium minutum Braun as holotype of the genus Characiopsis. (The
later lectotypification by Loeblich ( 1967) who selected Characiopsis pyrformis
(Braun) Borzi was unnecessary.) However, Lemmermann ( 19151, having seen
Braun's original specimens of Characium minutum, became convinced that the alga
named Characiopsis minuta by Borzi represented a different species and he named
it Characiopsis borziana. I t is not clear from the I.C.B.N. (1979)whether Characiopsis
108
D. J. HIBBERD
TAXONOMY O F EUSTIGMATOPHYCEAE
109
minuta (Braun) Borzi or CharaciopJis borziana Lemmermann should be considered
as the type of the genus. Silva (1979) regards Characiopsis borziana as the type,
being of the opinion that a genus should be typified with material at hand
whether or not the author misidentified the type with a previously described
species. This is the position adopted here. This selection is supported by the
implied intention of Art. 10.1 of the I.C.B.N. that “the type of a name o f a genus
. . . . is a species”-rather than the name of a species.
The situation is further complicated by doubt about the affinity of Characiopsis
borziana. Borzi ( 1895) described the zoospores as apparently possessing a single
chloroplast, prominent, slightly lateral eyespot and single terminal flagellum.
These features may be interpreted as belonging to tribophycean zoospores (which
in a minority of species do possess only a single chloroplast) in which a
second flagellum was not detected. This is possible because in some species, the
second flagellum is too short to be seen clearly using the light microscope. This
interpretation is supported by the presence of several chloroplasts in the
vegetative cells, a situation more characteristic of the Tribophyceae than the
Eustigmatophyceae. O n the other hand, Borzi may have been describing
eustigmatophycean zoospores, all of which characteristically possess a single
chloroplast, a prominent extraplastidial eyespot at their anterior extremity and
mostly only a single terminal flagellum; the second very narrow flagellum found
in zoospores of stipitate eustigmatophycean species is too narrow to be visible
using the light microscope and normal methods of observation; if present in the
zoospores of C. borziana, it would almost certainly not have been detected.
However, the eyespot in C. borziana is clearly described by Borzi and illustrated in
every figure as occupying a lateral position, as is typical of the Tribophyceae
where the intraplastidial eyespot underlies the proximal end of the short
posteriorly directed flagellum. Unfortunately, it is not clear from Borzi’s figures
whether the eyespot is intraplastidial or not. I t appears to be separate from the
chloroplast in most illustrations ([Borzi, 1895, Tav. XLV), but in some cases the
shading of the chloroplast extends towards it in a way suggesting that it might
really be enclosed within a narrow chloroplast lobe. Thus, owing to the lateral
position of the eyepost and the inconclusive nature of the remainder of the
evidence, C. borziana is here retained as a species in the Tribophyceae. If a reinvestigation of a new isolate showed C. borziana to be a eustigmatophyte, and
thus congeneric with species of Pseudocharaciopsis, the transfer of the name
Characiopsis from the Tribophyceae to the Eustigmatophyceae could be prevented
either by conserving Characiopsis with an altered type or by proposing the name as
a nomen rejciendum on the grounds that it had been widely and persistently used
for a taxon not including its type (Art. 69); a new name would then be needed to
replace Characzopsis in the Tribophyceae.
With regard to C. minuta, the second possible type of Characiopsis, it is shown
below that this species is undoubtedly a eustigmatophyte. If it should be decided
at a future date that C. minuta is the type of Characiopsis then the transfer of that
Figures 1-10, Fig. 1 . Eustigmatos uischen, CCAP 860/la, x 1500. Figs 2-4. Eustigmatos magna, CCAP
860/4. Fig. 2 . Normal vegetative cells, each with a prominent vacuole (V), x 1500. Fig. 3. Zoospore.
C, Chloroplast; E, eyespot; F, flagellum. Phase-contrast, x 1500. Fig. 4. V e v large vegetative cell. V,
Vacuole. x 1000. Fig. 5 . Eustzgmatospolyphem, Innsbruck IB 207. P, Pyrenoid; V, vacuole, x 1500. Figs
6, 7 . Vzschena stellala, UTEX 312, x 1500. Figs 8, 9. Vzscheriapunctata. Fig. 8. PRA A316, x 1500. Fig. 9.
UTEX 153, x 1500. Fig. 10. Vzscheria heluetica, CCAP 861/1. Arrowhead indicates a polyhedral cell
with two projections visible. P, Pyrenoid, x 1500.
8
110
D. J. HIBBERD
generic name from Tribophyceae to Eustigmatophyceae could be prevented in
the manner described for C. borziana.
Key to species of Pseudocharaciopsis
1. Cells all narrowly ellipsoid with acute apex, the chloroplast
normally single and with a spherical stalked pyrenoid
. . . . . . . . . . . . . .
Pseudocharaciopsis minuta
1'. Cells extremely variable in shape and size, none of the several
. . . . . Pseudocharaciopsis ovalis
chloroplasts bearing a pyrenoid
Pseudochuraciopsis minuta (Braun) Hibberd, comb. nova
SYNONYMS: Characium minutum Braun, in Kiitzing Species Algarum, Leipzig : 892
( 1849).
Characium minutum Braun. Algarum unicellulariumgenera nova et minus cognita, praemissis observationibus de algis unicelluluribus in genere. Leipzig: 46 ( 1855).
Characiopsis minuta (Braun) Borzi, Studi Algologici Fmc. 11. Palermo: 152 (18951,
quoad basionym, excluso descriptione.
Pseudocharaciopsis texensis Lee 8c Bold, British Phycological Journal, 8: 32 ( 1973).
ILLUSTRATIONS: Figs 11-13.
A cytological and ultrastructural investigation by Lee 8c Bold ( 1973)of both the
vegetative cells and zoospores of a new isolate of a stipitate yellow-green alga
clearly showed that it belonged in the Eustigmatophyceae. The alga was erected
as the type species of the new genus Pseudocharaciopsis since it was said to have
been previously undescribed, though no evidence for this was given. Comparison
of cultures of the strain studied by Lee 8c Bold with previous descriptions of
species of Characiopsis show that it can be identified as Characiopsis minuta (Braun)
Borzi. The cell shape is characteristic and distinct from all other Characiopsis
species with the possible exception of C. acuta Borzi and C . subulata Borzi, which
have respectively longer and shorter stipes than C. minuta. The size range
measured here in actively growing cultures-( 12)20(34)x (3)5(10) pm-agrees
well with that described by Braun-(5)16.5-20(25) x 5 pm and subsequently by
Hermann ( 1863)(as Churucium ambiguum Hermann and C.tenue Hermann), Borge
(18961, West (1904) (as Characium subulatum A. Braun), Lemmermann (19151,
Pascher (1938)and Margalef (1944, 1948);senescent cultures of P. minuta characteristically produce a proportion of very large cells, 35-60pm long and 10-20pm
wide. Pascher (1938) describes this species as a very widespread, though easily
overlooked, form with a very wide ecological distribution, commonly appearing
in large numbers. It therefore seems likely that it might have been rediscovered
during Lee & Bold's wide-ranging investigation of Churacium-likeforms. Of the
authors listed above, only Margalef (1944) illustrates the pyrenoid but this is
easily overlooked if only bright-field optics are used. Pyrenoids would, in any
case, have been expected to be absent from C. minuta since this character was
considered to distinguish species of Characiopsis from those of Characium, the latter
genus of chlorophycean algae possessing easily demonstrable pyrenoids surrounded by starch grains. Even the very large polyhedral pyrenoids in the Eustigmataceae remained unrecognized in most species; once having been precisely
described, they are now easily seen using the light microscope.
Pseudocharadopsis ovalis (Chodat) Hibberd, comb. nova
ovalis Chodat, In Materiaux pour la Flore Cryptogamique Suzsse 4
(2). Berne: 182 (1913).
SYNONYMS : Monodus
TAXONOMY OF EUSTIGMATOPHYCEAE
Ill
Characiopsis ovalis (Chodat)Chodat ex Poulton, ktude sue les Heterokontes. These no.
777, Universite' de Gentve. Geneva: 32 (1925).
ILLUSTRATIONS:
Figs 14, 1 7 .
The CCAP strain no. 882/1 was originally deposited under the name
Ellipsoidion oocystoides Pascher. It was subsequently identified as E . acuminatum
Pascher in publications on its cytology and ultrastructure (Hibberd & Leedale,
1970, 197 1 , 1972) as it appeared to resemble that species more in its overall
shape. During these investigations it was also found that a proportion of the cells
of this species could become attached to the bottom of the culture flasks by
means of a short stipe and discoid holdfast (Hibberd & Leedale, 19721, a feature
not characteristic of species in the genus Ellipsoidion; a wide variability in cell
shape and size was also noted. After further study it is now apparent that strain
882/1 closely resembles the species described by Poulton (1925) as Characiopsis
ovalis. This description was based upon a strain originally isolated by R. Chodat
(no. 107) and described by him as Monodus ovalis (Chodat, 1913); the isolate was
presumably lost before 1947 since it does not appear in the list of strains held at
the University of Basle at that date (Geiger-Huber & Vischer, 1947).
In its external form, strain 882/ 1 most strikingly resembles C. ovalis in showing
the same extreme range of variation in cell shape, size and presence or absence of
a stipe and holdfast. This range of variation is unusual in cultured material and
was stressed by Poulton (1925) as the most obvious character of C. ovalis. The
a pearance of the cell contents also agrees in general with Poulton's description,
t e strongest points of similarity being the presence of 2 to several chloroplasts
and the occurrence of a single large lipoidal droplet varying in colour from red
to brown. While the zoospores of strain 882/1 resemble those described for
C. ovalis in possessing a large red eyespot at their anterior extremity and only a
single chloroplast, the second flagellum is neither as long nor as obvious as that
described by Poulton. On the other hand, the observations of Poulton (1925) on
zoospores belonging to the tribophycean genera Botrydiopsis, Heterococcus and
Tribonema and those on vischeria stellata described above appear inaccurate and
enigmatic in the light of more recent studies. For this reason no particular weight
is attached to this apparent difference in zoospore flagellation and strain 882/1 is
identified as Characiopsis ovalis (Chodat)Chodat ex Poulton.
As discussed above, it has been decided that the name Characiopsis be used for a
genus of Tribophyceae and that C . borziana should be the type species. Strain
882/1, a eustigmatophyte, clearly cannot be retained in Characiopsis. I t is here
placed in the genus Pseudocharaciopsis since it is capable of producing cells with a
stipe and attaching disc and has zoospores with an almost identical structure to
those of P. minuta, despite the fact that the chloroplasts in the vegetative cells do
not appear to possess stalked pyrenoids (Hibberd, 1980). This step requires
modification of the original circumscription of the genus but it would be
premature to set up a new genus solely on the basis of the presence or absence of
pyrenoids, a remarkably capricious character in the majority of the other classes
of algae.
K
Chlorobotryaceae
Chlorobotryaceae Pascher (as Chlorobotrydaceae Pascher).
TYPE:
Chlorobotrys Bohlin.
D. J . HIBBERD
112
Figures 11- 1 7 . Figs 11-13. Pseudocharaciofsis rninuta. Fig. 11. Group of cells mutually attached at their
proximal ends. P, pyrenoid. Phase-contrast, x 1500. Figs 12, 13. Two relatively large cells
photographed using a dark-blue filter to show the shape of the single chloroplast (C). P, Pyrenoid,
x 1500. Figs 14-17. Pseudocharaciopsis ovalis. Fig. 14. Small cell with apapilla (arrowhead)but no stipe.
Phase-contrast, x 1500. Fig. 15. Small cell with both a papilla and a stipe(s1. Phase-contrast, x 1500.
Fig. 16. Large cell with several chloroplasts (C),a single large lipoidal globule (L) but no apical
papilla, x 1500. Fig. 17. Three large cells each with a stipe and foot (F), apical papilla and refractile
lipoidal globule (L). Anoptral phase-contrast, x 1500.
Chlorobotrys Bohlin
(W.West) Bohlin.
The genus as originally described included only C. regularis which is therefore
the type species. Since C. regularis has been shown to be a eustigmatophyte (see
below), Chlorobotrys becomes a genus in the Eustigmatophyceae. It has been
decided to place C. regularis in a separate family since the cells differ from those
of other eustigmatophytes in possessing a smooth, thin,but flexible, cell wall and
in being surrounded (both as individuals and when in groups) by layers of
mucilage. Motile cells have never been found, a feature so far shared only with
members of the family Monodopsidaceae (see below). However, species in the
Monodopsidaceae have very much smaller cells than C. regularis and are not
surrounded by layers of mucilage.
TYPE: C. regularis
TAXONOMY OF EUSTIGMATOPHYCEAE
113
Chlorobotvs regularis (W. West) Bohlin, Bihang till K. Svenska vetenskapsakademiens
handlingar, 27, Afd. 111 (4): 34 (1901).
SYNONYM :
Chlorococcum regulare W. West, Journal of the Royal Microscopical Society,
1892: 737 (1892).
Chlorobotrys regularis can be identified as a member of the Eustigmatophyceae
on the basis of both the ultrastructure of its vegetative cells (Hibberd, 1974) and
chloroplast pigment composition (Whittle, 1976). Chlorobotrys polychloris Pascher
may be a form of C. regularis with a. more divided chloroplast (Hibberd, 1974).
Monodopsidaceae
Monodopsidaceae Hibberd, familia nova
Eustigmatophyceae unicellulares numquam a f i a e , cellulis sphaericis, vel
ovoideis vel ellipticis vel cylindricis, minus quam 10 pm diametro. Zoosporae
nullae.
Unicellular free-floating Eustigmatophyceae with spherical, ovoid, elliptical or
cylindrical cells less than 10 pm in diameter. Zoospores never produced.
TYPE:
Monodopsis Hibberd.
The separation of this family into two genera largely on the basis of size is
somewhat artificial but is necessitated by the lack of comparative ultrastructural
studies. Nevertheless this decision is supported by the following facts : Monodopsis
subterranea is a soil alga whereas the two smaller species here placed in the genus
Nannochloropsis are euryhaline, both occurring in coastal rock pools and one
additionally inthe open sea; in M . subterranea the pyrenoid is deeply embedded in
the chloroplast and terminal with respect to the whole cell (Hibberd, 1969, 1980)
while in Nannochloropsis species it apparently bulges from the face of the
chloroplast (Antia et al., 19751, and division in M . subterranea is oblique whereas
in Nannochloropsis species it is transverse.
1.
1I .
Key to the genera
Forms greater than 5 pm in maximum dimension
Forms less than 5 pm in maximum dimension
. . .
. .
I
M onodopsis
Nannochloropsis
Monodopsis Hibberd, genus novum
The name Monodus was derived by Chodat (1913:185) from povoa
and ddovo -“Monodus
~ovo6ova(qui n’a q’une dent)”. The correct form of the
new compound is therefore Mondontopsis of which the name Monodopsis represents
a shortened form.
DERIVATION:
Monodopsidaceae dimensione maxima plus quam 5 pm.
Monodopsidaceae greater than 5 pm in maximum dimension.
TYPE:
Monodopsis subterranea (J.B. Petersen) Hibberd.
Monodopsis subtmuneu (J. B. Petersen) Hibberd, comb. nova
SYNONYM:
(1932).
Monodus subterraneus J. B. Petersen Archiv f u r Protistenkunde, 76: 406
114
D. J. HIBBERD
The strain maintained at Cambridge as no. 848/1 was isolated from a rock in a
stream near Marion, Connecticut, U.S.A. by Professor R. A. Lewin. There is no
reason to doubt its identification as Monodus subterruneus. The chloroplast
pigment composition of this strain has been found to be typical of the
Eustigmatophyceae (Whittle 8c Casselton, 1975) and preliminary structural investigation (Hibberd, 1969, 1980) shows certain features such as absence of a
girdle lamella from the chloroplast and presence of a highly characteristic type of
storage vesicle which confirms its position in this class.
The type of the genus Monodus is M . ovalis Chodat, which was transferred to
Characiopsis by Poulton ( 1925) and is here combined into Pseudochuraciopsis.
However, the name Monodus has continued to be widely used since 1925 (Silva,
1979) and has now been proposed for conservation with the altered type
M . acuminutus Chodat (Silva, 1980). Since the affinities of M . ucuminutus are
unknown, Monodus remains for the present a genus in the Tribophyceae.
NunnocMoroj~sisHibberd, genus novum
Nannochlorid - and so the correct form
of the new name is Nannochloridopsis. Nunnochloropsis represents a shortened form
of this name.
DERIVATION : The stem of Nunnochloris is
Monodopsidaceae dimensione maxima minus quam 5 pm.
Monodopsidaceae less than 5 pm in maximum dimension.
TYPE:
Nunnochloropsis oculutu (Droop)Hibberd.
The taxonomy of very small (less than 5 pm), greenish coloured algae which
apparently do not produce motile reproductive stages is confused and unstable.
The major groups which must be considered when assigning an organism of this
type are the Chlorophyceae, Tribophyceae and Eustigmatophyceae; in the cases
of some of the older descriptions, the Nostocophyceae (= Cyanophyceae) must
also be considered. However, even this basic classification is not possible using
light microscopy alone and it is this limitation that has mainly led to the present
confusion. Most algae of this general form are named as species of the
chlorophycean genus Nunnochloris Naumann, which was established for
unicellular algae possessing a single parietal chloroplast, a hyaline structureless
cell wall lacking surrounding mucilage, and reproducing only by transverse
division into two equal parts (Naumann, 1921). The genus originally included
only N . bacillaris and N . coccoides, both species occurring in artificially enriched
freshwater habitats. Pennington (1941) referred a similar minute form, also
found in artificially enriched freshwater, to the new genus and species Diogenes
rotundus. Fritsch (1949) noted the similarity between this form and species of
Nannochloris and transferred it into that genus. More recently several marine
species have been referred to the genus. Butcher (1952) described N . maculatus
and N . atomus from British coastal waters and Droop (1955) described N . oculata
from brackish supralittoral rock pools. 0ther unnamed species of Nunnochloris
from marine habitats are listed by both CCAP and UTEX. Bourrelly (1972)places
all the marine species of Nannochloris in the genus Diogenes, apparently
considering the possibility that the two species described by Naumann may have
been blue-green algae.
TAXONOMY OF EUSTICMATOPHYCEAE
115
The inadequacy of the present taxonomy of these small green forms is
illustrated by the recent findings of Antia et al. (1975) who, on the basis of
chloroplast pigment composition and ultrastructure, found CCAP strain no.
251/lb, listed as N . coccoides, to be a member of the Chlorophyceae, while the
‘type’ strain of N . oculata (CCAP no. 849/1) was identified as a member of the
Eustigmatophyceae. Application of the name Nannochloris depends on the
affinities of the type species. Naumann (1921)did not designate either of the two
species he described as the type and none has apparently been chosen since.
CCAP strain no. 251/lb, presently listed as N . coccoides, fits Naumann’s
description of this species, the normally sub-spherical cells being 2.5-4 pm in
diameter, containing a single parietal chloroplast and apparently reproducing by
transverse division. The early stages of division are unequal, resembling
budding, but since division always appears to result ultimately in the production
of two daughter cells of equal size, no particular weight is attached to this
character, particularly in the light of the brevity of Naumann’s original
description. Since this strain has been shown to be a member of the
Chlorophyceae N . coccoides Naumann is here designated as the lectotype species of
the genus Nannochloris Naumann, 1921. The new genus Nannochloropsis is established for eustigmatophycean species of very small size, the best known of which
is presently classified as a species of Nannochloris, N . oculata Droop.
While only two species of Nannochloropsis can be named at the present time, it is
probable that the marine forms known as clone ‘GSB Sticho’ (Ryther, 1954;
Yentsch 8c Guillard, 1969; Norgird et al., 1974)and clone ‘Tunis’ (Norgard, Svec,
Liaaen-.Tensen & Guillard, 1974) also belong in Nannochloropsis. Both of these
isolates have been identified as eustigmatophytes on the basis of their chloroplast
pigment composition (Norgard et al., 1974)but they have not yet been sufficiently
characterized morphologically tci place them in the present taxonomy. The
species described as Diogenes rotundus by Pennington may also be a
eustigmatophyte since it apparently contains no chlorophyll b (Pennington,
1941). In addition, current studies on a number of unnamed ‘Nannochloris’strains
show that some, which cannot be identified as N. oculata, like that species do not
contain chlorophyll b (Dr M. Turner, personal communication) and therefore
possibly represent further species of Nannochloropsis. However, the majority
including N . atomus (CCAP no. 2.51/4b),N. maculata (CCAP 251/3), N . sarnzensis
nom. prov. (CCAP 251/2), N . sp. (CCAP 251/5), N . coccoides (CCAP 251/la) and
CCAP 251/6, presently listed as N . oculata, do possess chlorophyll b (Dr M.
Turner, personal communication). They are probably correctly placed in the
genus Nannochloris, although the taxonomy of this group at the specific level is in
need of revision.
of Nannochloropsis
pm in diameter
. . .
Key to species
1.
1’.
Cells subspherical, 2-4
Cells cylindrical, 3-4 x 1.5- 1.7 pm
.
.
.
.
Nannochloropsis oculata
Nannochloropsis salina
Nunnochloropsis oculdu (Droop) Hibberd, comb. nova
SYNONYM : Nannochloris oculata Droop, Journal o f the Marine Biologtcal Association o f
the United Kingdom, 3 4 : 235 (1955).
Droop only tentatively referred this organism to the genus Nannochloris since a
delicate external membrane was present at certain stages of the life cycle and the
D. J. HIBBERD
1 I6
cells also possessed a “pale circular stigma”. As discussed above, the ‘type’ strain
of this species has been found to be a eustigmatophyte (Antia et al., 1975)and so
it cannot be retained in the chlorophycean genus Nannochloris.
Nannochloris salina Hibberd, sp. nova
Monallantus salina Bourrelly, Bulletin d u Laboratoire Maritime de Dinard,
43: 114 (1958), nomen nudum.
SYNONYM :
Cellulae cylindricae, rectae vel leviter reniformes, 3-4 pm x 1.5-1.7 pm, extremis
rotundatis, plerumque granulo refractivo ad quoque extremum ; vagina
gelatinosa nulla.
Cells cylindrical, straight or slightly reniform, with rounded ends, 3-4
pm x 1.5-1.7 pm, mostly with a refringent granule at each end; gelatinous sheath
lacking.
TYPE:
Bourrelly, Bulletin d u LaboratoireMaritime de Dinard, 43:Fig. 5 ( 1958).
This minute alga, originally found in large numbers in supralittoral pools, was
tentatively identified as a member of the Tribophyceae on the basis of the yellowgreen colour of its chloroplasts, absence of starch and free-living unicellular
habit. It was described as Monallantus salina by Bourrelly (1958) but this
publication was invalid since it was not accompanied by a Latin description. An
alga subsequently isolated by Maestrini from the Gulf of Marseille and identified
as M . salina by Bourrelly (in Berland et al., 1970) has been found to have a
chloroplast pigment composition typical of the Eustigmatophyceae (Antia et al.,
1975). It also has certain ultrastructural features that are in agreement with this
placement (Antia et al., 19751, such as absence of a chloroplast girdle lamella,
absence of starch and the presence of vesicles with finely lamellate contents.
Monallantus breuicylindrus Pascher was designated lectotype of Monallantus by
Loeblich ( 1967). Although the zoospores of M . breuicylindrus apparently do not
possess an intraplastidial eyespot positioned close to the point of insertion of
the shorter flagellum of the heterokont pair as do M.gracilis Pascher and
M . pyeniger Pascher (Pascher, 1937), characters which would unequivocally
demonstrate a position in the Tribophyceae, they nevertheless possess all the
other attributes of a typical tribophycean zoospore such as two unequal flagella,
two chloroplasts, an anterior contractile vacuole and a broadly ovoid shape. For
these reasons the name Monallantus is retained for a genus in the Tribophyceae.
DISCUSSION
I t is intended that this taxonomic study of the Eustigmatophyceae shall serve
as a foundation for future studies on the group and help to eliminate confusion
over the naming of strains used for experimental work. Changes will be
inevitable as new species are added but the family classification appears to be
natural: ellipsoid cell shape and stipitate habit is linked with the production of
biflagellate zoospores in the Pseudocharaciopsidaceae, isodiametric cells and
free-floating habit with uniflagellate zoospores in the Eustigmataceae, while
Chlorobotlys regularis has a unique type of vegetative cell and no zoospores. The
greatest uncertainty remains with the taxonomy of the small forms classified in
TAXONOMY O F EUSTIGMATOPHYCEAE
117
the Monodopsidaceae since these are difficult to fix for EM and have relatively
few characters.
In this laboratory further work is in progress on the isolates discussed above
and on others. These forms appear to be ecologically important, occurring in
large numbers in enriched waters, both fresh and marine. Such occurrences are
probably under-reported because of the difficulty of identifying the species
concerned, even at the class level..
ACKNOWLEDGEMENTS
I am particularly grateful to Mr T. Christensen and Dr P. C. Silva for their
invaluable advice on problems of nomenclature and for critically reading the
manuscript of this paper. Advice on nomenclature has also been provided by Mr
R. D. Meikle, Mr R. Ross, Mr P. D. Sell and Dr F. K. Kupicha. Diagnoses of the
new taxa were translated into Latin by Mr Christensen and Dr Kupicha. Mr R. P.
Adamson and Dr P. A. Broady kindly provided cultures of their own isolates.
Bibliographical help was provided by Mrs J. A. Moore.
REFERENCES
ADAMSON, R. P. & SOMMERFELD, M. R., 1978. Survey of swimming pool algae of the Phoenix, Arizona,
metropolitan area.Journa1 ofPhycology, 1 4 : 519-521.
ANTIA, N . J., BISALPUTRA, T., CHENG,J. Y. & KALLEY, J. P., 1975. Pigment and cytological evidence for
reclassification of Nannochloris oculata and Monallantus salina in the Eustigmatophyceae. Journal of Phycology,
I / : 339-343.
BASLEROVA, M. & DVOMKOVA, J., 1962. Algarum, hepaticarum, muscorumque in culturis collectto. Prague:
Czechoslovak Academy of Science.
BERLAND, B. R., BONIN, D. J., DAUMAS, R. A,, LABORDE, P. L. & MAESTRINI, S. Y., 1970. Variations d u
comportement physiologique d e I’algur Monallantus salina (xanthophycke) e n culture. Marine Biology, 7:
82-92.
BISCHOFF, H. W. & BOLD, H . C., 1963. Some soil algae from Enchanted Rock and related algal species. In
Phycological Studies I V (University ofTexas Publication No. 63 18).Austin: University ofTexas.
BOHLIN, K., 1901. Etude sur la Bore algologique d’eau douce des Aqores. Bihang till K . Suenska
uetenskapsakademiens handlingar, 27, Afd. III, No. 4 : 1-85.
BORGE, O., 1896. Australische Siisswasserchlorophyceen. Bihang till K . Suenska uetenskapsakademiens handlingar,
22, Afd. ( I f , A‘o. 9: 1-32.
BORZI, A,, 1895. Studi Algologici. Fasc. 11. Palermo: A. Reber.
BOURRELLY, P., 1958. Note systematique sur quelques algues microscopiques des cuvettes supra-littorales
d e la region de Dinard. Bulletin d u Laboratoire Maritime de Dinard, 43: 11 1-1 18.
BOURRELLY, P., 1972. Les algues d’eau douce. Initiation d. la systematique. Tome I : Les Algues Vertes. Paris: N.
Boubke & Cie.
BRAUN, A., 1855. Algarum unicellularium genera nova et minus cognita, praemissis obseruationibus de algis unicellularibus
i n genere. Leipzig: Engelmann.
BUTCHER, R. W., 1952. Contributions to o u r knowledge of the smaller marine algae.Journa1 o f t h r Marine
Biological Association ofthe United Kingdom, 3 1 : 175- 19 1.
CASTAGNE, J . L. M., 185 1. Catalogue des plantes gui croissent naturellement aux environs de Marseille. Supplement.
Aix: Nicot et Pardigon.
CHODAT, R. H., 19 13. Monographie d’algues e n culture pure. In Matrriauxpour la Flore Cryptogamique Suisre, 4 ,
Fasc. 2. Bern: K. J . Wyss.
CHRISTENSEN, T., 1962. Alger. In T. Mi. Bocher, M. Lange & T. Ssrensen (Eds), Botanik, 2 lSytematik
Botanik), 2: 1-178. Copenhagen: Munksgaard.
CHRISTENSEN, T., 1978. Annotations to a textbook of phycology. Botanisk Tidssknft, 73: 65-70.
DROOP, M. R., 1955. Some new supra-littoral protista. Journal ofthe Marine Biologzcal Association ofthe United
Kingdom, 3 4 : 233-245.
ETTL, H., 1978. In H. Ettl, J . Gerloff & H . Heynig (Eds),Xanthophyceae. 1.Teil. Sksswasserflora uon Mitteleuropa,
Bd. 3. Stuttgart & New York: Gustav Fischer.
FOTT, B., 1974. The phylogeny of eukaryotic algae. Taxon, 23: 446-46 1.
FRITSCH, F. E., 1935. The Structure and Reproduction of the Algae. Vol. I . Cambridge: Cambridge University
Press.
118
D. J. HIBBERD
FRITSCH, F. E., 1949. Contributions to our knowledge ofBritish algae. Hydrobiologia, 1 : 115-125.
GARTNER, G., 1976. Verzeichnis der Algenkulturen a m Institut fur Botanische Systematik und Geobotanik
der Universitat Innsbruck. Bericht des Natunuissenrchqftlich-medizinischenVereins in Innsbmck, 63: 67-89.
GEIGER-HUBER, M. & VISCHER, W., 1947. Mimeographed list ofspecies ofpure cultures ofdgae at the Botanical
Institute ofthe Uniuersity ofBasel.
GEORGE, E., 1976. Culture Centre ofAlgae and Protozoa, List ofstrains, 3rd Edn., 1976. Natural Environment
Research Council.
HERMANN, J., 1863. Ueber die bei Naumann aufgefundenen Arten des Genus Characium. In L. Rabenhorst
(Ed.), Beitrirge zur niihrenKenntniss und Verbreitung der Algen. He@ I . Leipzig: Eduard Kummer.
HIBBERD, D. J., 1969. Cytological Studies on the Coccoid Xanthophyceae. Ph.D. Thesis, University of Leeds.
HIBBERD, D. J., 1972. Chrysophyta: definition and interpretation. British PhycologicalJournal, 7: 281 (abstract).
HIBBERD, D. J., 1974. Observations o n the cytology and ultrastructure of Chlorobotrys regularis (West) Bohlin
with special reference to its position in the Eustigmatophyceae. British PhycologicalJournal, 9 ; 37-46.
HIBBERD, D. J., 1976. The ultrastructure and taxonomy of the Chrysophyceae and Prymnesiophyceae
(Haptophyceae): a survey with some new observations o n the ultrastructure of the Chrysophyceae. Botanical
J o u m l ofthe Linnean Society, 72: 55-80.
HIBBERD, D. J., 1980. Eustigmatophyceae. In E. R. Cox (Ed.), Phytoflagellates: F a n and Function: 319-334. New
York: Elsevier North Holland.
HIBBERD, D. J. & LEEDALE, G. F., 1970. Eustigmatophyceae-a new algal class with unique organization of
the motile cell. Nature, London, 225: 758-760.
HIBBERD, D. J. & LEEDALE, G. F., 197 1. A new algal class-the Eustigmatophyceae. Tauon, 20:523-525.
HIBBERD, D. J. & LEEDALE, G. F., 1972. Observations o n the cytology and ultrastructure of the new algal
class, Eustigmatophyceae. Annals ofBotany, 36: 49-1 1.
VAN DEN HOEK, C., 1978. Algen. Evuhrung in die Phycologie. Stuttgart: Georg Thieme Verlag.
KOCH, W., 1964. Verzeichnis der Sammlung von Algenkulturen um Pflanzenphysiologischen Institut der
UniversiCit Gottingen. Archiufur Mikrobiologie, 47: 402-432.
KUTZING, F. T., 1849. Species Algarum. Leipzig: F. A. Brockhaus.
LEE, K. W. & BOLD, H. C., 1973. Pseudochamciopsis texensis gen. et sp. nov., a new member o f the
Eustigmatophyceae. British PhycologicalJournal, 8: 3 1-3 7.
LEE, K. W. & BOLD, H. C., 1974. Characium and some Characium-like algae. Phycological Studies X I I (University of
Texas Publication No. 7403). Austin: University of Texas.
LEEDALE, G. F., in press. Algal classes: delimitation, interrelationships and phylogeny. Proceedings of the 2nd
Intenational Symposium on the Tauonomy @Algae, Madras, 1974.
LEMMERMANN, E., 19 15. Algologische Beitrage. XII. Die Gattung Characiopsis Borzi. Abhandlungen
herausgegeben uom NaturwksmchaJlichen Verein zu Bremen, 2,:249-267.
LOEBLICH, A. R., 111, 1967. Notes on the divisions Chlorophyta, Chrysophyta, Pyrrhophyta and Xanthophyta
and the family Paramastigaceae. Taxon, 16: 230-236.
LOEBLICH, A. R. & LOEBLICH, L. A., 1978. Division Eustigmatophyta. In A. I. Laskin & H. A. Lechevalier
(Eds), CRC Handbook of Minobiology, 2nd Ed. Vol. II. Fungi, Algae, Protozoa and Viruses, 481-487. West Palm
Beach, Florida: CRC Press.
LUTHER, A., 1899. Ueber Chlorosacm eine neue Gattung der Siisswasseralgen, nebst einigen Bemerkungen zur
Systematik venvandter Algen. Bihang till K. Sumka uetenskapsakademiens handlingar, 24, Afd. I I I , No. 13: 1-22.
MARGALEF, R., 1944. Datos para la flora algologica d e nuestras aguas dukes. Publicaciones del Instituto Botcinico
de Barcelona, 4(1): 1-130.
MARGALEF, R., 1948. Materiales para una flora d e las algas del N.E. d e Espaiia. 11, Chrysophyceae,
Heterocontae, Dinophyceae, Eugleninea. Collectanea Botanica, 2:99-130.
MARGULIS, L., 1974. The classification and evolution of prokaryotes and eukaryotes. In R. C. King (Ed.),
Handbook ofGenetirs, I : 1-41. New York: Plenum Press.
NAUMANN, E., 1921. Notizen zur Systematik der Siisswasseralgen. Arkiu f6r Botanik, 16(2): 1-19.
NORGARD, S., SVEC, W. A., LIUEN-JENSEN, S . , JENSEN, A. & GUILLARD, R. R. L., 1974. Chloroplast
pigments and algal systematics. Biochemical Systematics and Ecology, :3-6.
OLTMANNS, F., 1904. Morphologie und Biologie der Algen. Band 1.Jena: Gustav Fischer.
PASCHER, A., 1912. Zur Gliederung der Heterokonten. Hedwigia, 53: 6-22.
PASCHER, A,, 19 15. Uber Halosphaera. Bericht der Deutschen botanischen Gesellsch& 33: 488492.
PASCHER, A,, 1925. Heterokontae. In A. Pascher (Ed.), Die Siisswasser-Flora Deutschlands, Osterreichs und der
Schweiz. Hefl 11. Jena: Gustav Fischer.
PASCHER, A,, 1930. Zur kenntnis der heterokonten Algen. Archiufur Protistenkunde, 71: 3 11-358.
PASCHER, A,, 1937-1939. Heterokonten. In L. Rabenhorst's Kryptogamen-Flora uon Deutschland, Osterreich und der
Schweiz. Aufl. 2. Band X I . Leipzig: Akad. Verlagsges. (Lief: 1: 1-160, 1937; Lief: 2: 161-320, 1937; Lief: 3:
321-480, 1937; Lief: 4: 481-640, 1938; Lief: 5: 641-832, 1938; Lief: 6: 833-1092, 1939).
PENNINGTON, W., 1941. Diogaes rotundus, gen. et sp. nov.-a new alga from experimental tubs. Journal of
Botany, 79: 83-85.
PETERSEN, J. B., 1932. Einige neue Erdalgen. Archiufur Protistenkunde, 76395-408.
PITSCHMANN, H., 1969. Zwei neue Heterokonten (Pleurochlorispolyphem und Heterococcus clauatus) aus Boden
der alpinen Stufe des Mt. Kenya. Osterreichische botanische Zeitschri& 116: 48-91,
TAXONOMY OF EUSTIGMATOPHYCEAE
119
POULTON, E. IM.,
1925. Etude J U T les Heterokontes. These no. 777, Uniuersitd de Genive. Geneva: lmprimerie Jent
Socikte Anonyme. [Bulletin de la Sociitdbota,nique de Geniue, Ser. 2, 17: 33-121, 19261.
POULTON, E. M . , 1926. Studies o n the Heterokontae. N e w Phytologist, 25:309-337.
RYTHER, J . H., 1954. The ecology of phytoplankton blooms in Moriches Bay a nd Great South Bay, Long
Island, New York. Biological Bulletin. Marine Biological Laboratory, Woods Hole, Massachusetts, 106: 198-209.
SILVA, P. C., 1979. Review of the taxonomic history and nomenclature of the yellow-green algae. Archiufer
Protistenkunde, 121: 20-63.
SILVA, P. C., 1980. Remarks o n algal nomenclature VI. Taxon, 29: 121-145.
STARMACH, K., 1968. Chrysophyta 111. Xanthophyceae. R6znowiciowe. I n K. Starmach (Ed.) Flora
stodkowodnapolksi. Tom. 7 . Warszawa & Krak6w: Panstwowe Wydawnictwo Naukowe.
STARR, R. C., 1978. The culture collection ofalgae at the University ofTexas at Austin. Journal OfPhycologv, 14,
Supplement: 47- 100.
VISCHER, W., 1945. Heterokonten aus alpinen boden, speziell dem schweizerischen nationalpark. Ergebnzsse
der wissenschaftlichen Untersuchung der Schweizrischen Nationalparks, I :48 1-5 10.
WEST, G. S., 1904. A Treatise on the British Freshwater Algae. Cambridge: Cambridge University Press.
WEST, W., 1892. Algae of the English Lake District.Jouma1 ofthe Royal Microscopical Society, 1892: 7 13-748.
WHITTLE, S. J ., 1976. The major chloroplast pigments of Chlorobotrys regularis (West) Bohlin
(Eustigmatophyceae) and Ophiocytium m a p Naegeli (Xanthophyceae). Bntish Phycological Journal, 1 I :
1 1 1-1 14.
WHITTLE, S. J . & CASSELTON, P. J., 1969. The chloroplast pigments of some green and yellow-green algae.
British Phycologtcal Journal, 4 : 55-64.
WHITTLE, S. J . & CASSELTON, P. J., 1975. The chloroplast pigments of the algal classes Eustigmatophyceae
and Xanthophvceae. I. Eustigmatophyceae. British PhycologicalJournal, 10: 179-19 1.
YENTSCH, C. S. & GUILLARD, R. R. L., 1969. The absorption of chlorophyll-b in uivo. Phytochemistry and
Photobzologv, 9 335-388.