Diatom Research
ISSN: 0269-249X (Print) 2159-8347 (Online) Journal homepage: www.tandfonline.com/journals/tdia20
Proposals for a terminology for diatom sexual
reproduction, auxospores and resting stages
Irena Kaczmarska, Aloisie Poulíčková, Shinya Sato, Mark B. Edlund,
Masahiko Idei, Tsuyoshi Watanabe & David G. Mann
To cite this article: Irena Kaczmarska, Aloisie Poulíčková, Shinya Sato, Mark B. Edlund,
Masahiko Idei, Tsuyoshi Watanabe & David G. Mann (2013) Proposals for a terminology for
diatom sexual reproduction, auxospores and resting stages, Diatom Research, 28:3, 263-294,
DOI: 10.1080/0269249X.2013.791344
To link to this article: https://doi.org/10.1080/0269249X.2013.791344
Published online: 13 May 2013.
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Diatom Research, 2013
Vol. 28, No. 3, 263–294, http://dx.doi.org/10.1080/0269249X.2013.791344
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
IRENA KACZMARSKA1∗ , ALOISIE POULÍČKOVÁ2 , SHINYA SATO3,4,5 , MARK B. EDLUND6 ,
MASAHIKO IDEI7 , TSUYOSHI WATANABE8 & DAVID G. MANN3
1 Department of Biology, Mount Allison University, Sackville, Canada
2 Department of Botany, Palacký University, Olomouc, Czech Republic
3 Royal Botanic Garden Edinburgh, Edinburgh, UK
4 Cardiff School of Biosciences, Cardiff University, Cardiff, UK
5 Graduate School of Science and Engineering, Yamaguchi University, Yamaguchi, Japan
6 St. Croix Watershed Research Station, Science Museum of Minnesota, St. Croix, MN, USA
7 Department of Biology, Bunkyo University, Koshigaya, Japan
8 Tohoku National Fisheries Research Institute, Fisheries Research Agency, Shiogama-shi, Japan
The past few decades have brought about a significant expansion in our understanding of the diatom life cycle, particularly its sexual
part. Presented here is a set of proposals for the terminology of processes and structures associated with sexual reproduction and for the
resting stages of diatoms, some of which have at times been confused with each other. The proposals fill the void present in widely used
publications offering standardized terminology related to diatom frustule micro-architecture.
Keywords: auxosporulation, diatoms, gametogenesis, life cycle, resting stages, sexual reproduction, terminology
1. Rationale
Several decades have passed since developments in electron microscopy began to reveal an unanticipated level of
micro-architectural complexity in the diatom frustule. Features such as rimoportulae and fultoportulae, which had
been detectable only as dots or spines under the light microscope, were revealed to have an intricate and characteristic
substructure, and much new detail was revealed in the striae,
areolae and raphe slits. Consequently, existing terms often
needed to be refined and many new ones invented. Faced
with the rapidly expanding vocabulary of diatom terms, a
small group got together in the 1970s to prepare a new,
standardized terminology focused on the diatom valve. The
result was the set of proposals by Anonymous (1975), von
Stosch (1975) and Ross et al. (1979). These papers have
served diatomists well but they contain little guidance about
the processes and structures present during the sexual phase
of the diatom life cycle, which until ca. 1980 were studied
largely using light microscopy.
In the second half of the 20th century, the most relevant papers on the diatom life cycle were issued by just two
researchers, L. Geitler (Vienna) and H.A. von Stosch (Marburg), together with their close colleagues, and almost all
papers were published in German. In the last two decades,
however, there has been a great increase in the number
and geographical origin of studies focused on the sexual
∗ Corresponding author. E-mail: iehrman@mta.ca
(Received 28 May 2012; accepted 18 March 2013)
© 2013 The International Society for Diatom Research
Published online 13 May 2013
phase, and in the level of detail at which reproductive structures could be observed. In these and other studies, electron
microscopy in particular, contributed to the understanding
of the diversity of structures (e.g., scales, plates) and possibly, the evolutionary relationships among the diatoms harbouring them. For example, based on auxospore development alone, von Stosch (1982) suggested close relationships
between some polar centrics and pennates, which was later
expanded and corroborated by molecular evidence (Medlin
& Kaczmarska 2004). Nonetheless, for many researchers,
the sexual phase of the diatom life cycle is probably still a
little mysterious and its terminology obscure.
At the 21st International Diatom Symposium held in
2010 in St. Paul, Minnesota, informal meetings were held
to discuss the possibility of preparing a terminology for
the structures and processes present during diatom sexual
reproduction. A working group was subsequently organized
(by IK) that has conducted its business largely by e-mail and
produced the present set of proposals, which expands on the
limited terminology provided by Ross et al. (1979).
2. Introduction
For many diatoms, sexuality is an obligatory life stage
because it is an integral part of the process by which cells
reverse the diminution of size, or size reduction, that occurs
264
Kaczmarska et al.
C
B
A
Fig. 1. A summary of the principal features of the life cycle of diatoms in three main variants, namely non-polar (A) and polar (B) centric
diatoms, and pennate diatoms (C). In gametangia, larger circles represent functional nuclei (light = diploid, dark = haploid) whereas
smaller circles represent pyknotic nuclei. F/− & M/+ symbolize female/male or non-motile/motile gametes respectively. (AP & IK
original; drawings are based on: for the non-polar centric Coscinodiscus granii after Schmid 1995 with the permission of Biopress Ltd.; for
the polar centric Lithodesmium undulatum redrawn after von Stosch 1982 with the permission of J. Cramer Publishing and after Manton
& von Stosch 1966 with the permission of Blackwell Science Ltd, UK; for a pennate Neidium sp. AP, original).
during the vegetative phase (Fig. 1). Size reduction comes
about because of the peculiar and unique method of diatom
cell division, in which new wall elements (valves and girdle
bands) are produced within existing wall elements inherited from the parent cell and are therefore smaller than
the parent wall elements. Diminution is reversed by size
restitution, which occurs by one of two methods: vegetative cell enlargement or auxosporulation, which are defined
below. Of the two, the more common is apparently auxosporulation and this usually, but not always, involves
sexual reproduction. Therefore, in one short-lived lifehistory stage, auxosporulation usually brings about both
genetic recombination and the reintroduction of large cells
to local populations of a species. The general outline of the
diatom life cycle has been detailed by Round et al. (1990),
Edlund & Stoermer (1997) and Chepurnov et al. (2004) to
name a few. The principal features of the sexual life cycle
are summarized for the three major variants in Fig. 1.
Our proposals begin with general terminology for the
life cycle events and the phenomenon of sexual reproduction and then proceed to details of the cells and structures
involved in fertilization and auxospore development (sections 3–9). Then our discussion ends with resting stages
(which are only rarely associated with auxosporulation) and
some special features of vegetative reproduction that are
often encountered during studies of the life cycle (section
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
10), such as the formation of internal valves and abrupt size
reduction, through which the size diminution is accelerated, bringing cells to the sex-inducible stage faster. Terms
appearing in bold type are formally defined at that point
in the proposals. These terms are the ones that are recommended to be used, while some other terms and synonyms
present in the literature are given in parentheses or discussed in the text. Indented entries deal with variants of
the entities defined in the main paragraph, or with phenomena or structures associated with these entities. In the
diagrams accompanying the terminology, diploid nuclei
are designated by open circles, haploid nuclei by filled
circles. Functional nuclei, either diploid or haploid, are
always shown larger than non-functional nuclei (‘pyknotic’
nuclei: section 4.5.11). Sections 6, 9 and 10 are divided
into thematic subsections with italicized headings, to aid
orientation.
In the examples provided here, whenever possible, the
names of diatom taxa are used as they currently appear
in AlgaeBase (Guiry & Guiry 2012; www.algaebase.org;
September 2011) because taxonomic reappraisal is not the
focus of our presentation. In cases in which the taxonomic
affiliation of a diatom has changed since the publication of
information relevant to this terminology, the name used by
the original author is shown as a synonym (in parentheses).
Most figures are adapted from earlier publications, but some
are original works by the authors. This is indicated in the
figure legend by the word ‘original’ following the author’s
initials.
3.
Life cycle
3.1. The life cycle of a diatom is the series of developmental changes through which a diatom passes from its
initial state to the same state in the next generation. Usually,
the life cycle comprises: (1) a period of vegetative, mitotic
cell division; and (2) a period of sexual reproduction preceding ‘auxosporulation’ (see section 3.3). The analogous
series of developmental changes in single cells, from one
mitotic cell division to the next, comprises the cell cycle of
a diatom. Three variants of the diatom life cycle are shown
in Fig. 1A–C.
Diatoms are diplonts, i.e., organisms that are diploid in
all stages of the life cycle except for the gametes, which are
haploid; individual gametes do not usually develop further
(but see ‘haploid parthenogenesis’ in section 5.4) and must
combine with another, sexually compatible gamete in order
to give rise to a new diploid individual.
3.2. An auxospore is a specialized cell that has the capacity of expanding in a highly controlled fashion, involving
the formation of unique wall elements (incunabula, perizonia: see sections 9.1 and 9.2) not found at any other stage
of the life cycle, to regenerate the characteristic size and
shape of a diatom. It is usually formed sexually, but occasionally apomictically or even vegetatively. Corresponding
to these two modes of formation, the auxospore is derived
265
from a zygote (sexual auxospore), or from a pseudozygote (see section 5.3) or unreduced vegetative cell (asexual
auxospores), respectively. Asexual auxospores are not synonymous with vegetatively enlarging cells (see section 3.5).
Although the transformation of the zygote, pseudozygote or
unreduced cell into an auxospore is probably a continuous
process, it is considered to be complete when the auxospore
begins to expand. The auxospore becomes ‘mature’ when
it has completed expansion and contains the initial cell (see
section 3.4). Auxospores are usually diploid, but haploid
or polyploid auxospores are also known to be formed, e.g.,
in Licmophora C. Agardh (Roshchin & Chepurnov 1994),
Craticula Grunow (Mann & Stickle 1991) and Pinnularia
Ehrenberg (Poulíčková et al. 2007, Poulíčková & Mann
2008). The fate of the auxospores with unusual numbers of
nuclei is poorly understood. Auxospores are not themselves
dormant resting stages and rarely develop into such stages
(see section 10.1). They are not dispersal units.
3.3. Auxosporulation refers to the whole process by which
an auxospore is formed, develops and, following expansion,
gives rise to new, enlarged initial cell(s). In most diatoms
that have been investigated, auxosporulation will not occur
if cell sizes exceed a critical size threshold (see section 3.6),
which differs from species to species. This is a permissive threshold and auxosporulation may not occur unless
other requirements are also met, such as particular physical or chemical conditions, cell densities or the presence of
compatible mates.
Just as auxosporulation is impossible for cells above a
certain critical size threshold, so it may also be impossible
below a second threshold (the lower sexual size threshold:
see section 3.6). In this case, the smallest cells continue to
divide and get smaller still but are unable to auxosporulate,
although they may be capable of vegetative cell enlargement, as in Achnanthes Bory de Saint-Vincent (Chepurnov
& Mann 1997). Diatoms for which there is a lower threshold for auxosporulation are said to have a closed life cycle,
those in which there is no lower threshold have an open life
cycle.
3.3.1. Uniparental auxosporulation is the formation of an auxospore from a single parental cell, following automixis (see section 5.2) or apomixis (see
section 5.3), or as a consequence of vegetative differentiation. Examples are Achnanthes brevipes var. intermedia (Kützing) Cleve (Roshchin & Chepurnov 1993),
Fragilaria capucina var. vaucheriae (Kützing) LangeBertalot (= Synedra vaucheriae: Geitler 1958), Reimeria sinuata (Gregory) Kociolek & Stoermer (= Cymbella sinuata: Geitler 1958), Sellaphora pupula (Kützing)
Mereschkowsky (Mann et al. 2004), Muelleria peraustralis
(W. West & G. S. West) Spaulding & Stoermer and Scoliopleura peisonis Grunow (Edlund & Spaulding 2006).
This is a broadly defined term that is particularly useful when there is insufficient cytological information to
determine whether the formation of the auxospore includes
meiosis.
266
Kaczmarska et al.
Fig. 2. Vegetative cell enlargement in Coscinodiscus wailesii represents an asexual means of restoring large size-class cells into the
population. The sequence of figures from left to right shows: a small vegetative cell; expansion of the protoplast; release of the protoplast
from the frustule; formation of the epivalve in the enlarged cell following acytokinetic mitosis and pyknosis of one of the sibling nuclei;
and completion of the vegetative cell enlargement with the production of a large cell/frustule after another acytokinetic mitosis and nuclear
pyknosis (MBE original; drawings are based after Nagai et al. 1995 with the permission of Allen Press Publishing Services).
3.3.2. Biparental auxosporulation is the formation of
one or two auxospores through the union of gametes derived
from two different parental cells. Biparental auxospores
result from allomixis (see section 5.1).
The occurrence of uni- or biparental auxosporulation is usually species-specific, but within a genus (e.g.,
Pinnularia and Neidium Pfitzer: Mann & Chepurnov
2005, Poulíčková et al. 2007, Poulíčková & Mann 2008,
Poulíčková 2008a) and sometimes even within a single
species (e.g., Cyclotella meneghiniana Kützing, Denticula tenuis Kützing: Iyengar & Subrahmanyan 1944, Geitler
1953, Mills & Kaczmarska 2006), both uni- and biparental
auxosporulation may sometimes occur.
3.3.3. Two- (or multi-) step auxosporulation is a process in which post-initial cells can undergo a further step of
successful auxosporulation without a significant intervening reduction in size. It has been documented, for example,
in Coscinodiscus granii Gough (Roshchin 1994) and Thalassiosira punctigera (Castracane) Hasle (Chepurnov et al.
2006). It is unclear whether the second (or third) steps
always occur through the same process as the first.
3.4. The initial cell is the first vegetative cell formed within
the mature auxospore, complete with a fully formed frustule (the initial frustule composed of the initial epitheca
and the initial hypotheca, each with an initial valve). Normally, each initial theca is produced following acytokinetic
mitosis (see section 10.3), which results in an initial cell
containing one diploid and up to two pyknotic nuclei (see
section 4.5.11). The initial epitheca and initial hypotheca
often differ morphologically from the thecae of normal
vegetative post-auxospore cells, because of their formation
within the auxospore rather than within another vegetative
cell. It is often convenient to refer to the first few mitotic
generations of cells produced by division of the initial cell
as post-initial cells.
3.5. Vegetative cell enlargement is the size restitution
through the partial or complete release of a vegetative
cell protoplast from its frustule, its subsequent expansion,
and the formation of a new frustule, as in Coscinodiscus
wailesii Gran & Angst (Nagai et al. 1995; Fig. 2), Achnanthes longipes C. Agardh, and other centric and pennate
species (von Stosch 1965, Roshchin & Chepurnov 1992).
The cell initiating vegetative enlargement is not differentiated from other vegetative cells (except that the cells are
usually in the later stages of size reduction and hence small)
and does not undergo meiosis in preparation for, or during,
enlargement. The characteristic incunabula or perizonia of
auxospores are absent and the enlarged cells produced by
vegetative enlargement may not expand to the same maximum size as the auxospores of the same species; they may
have modified frustule morphology relative to the parental
cells.
3.6. Although there is now evidence that diatom life cycles
are more flexible and varied (Schmid 1995) than was
thought or implied previously (e.g., in the accounts of the
life cycle by Drebes 1977a or Round et al. 1990), it seems
nevertheless to be true, especially in pennate diatoms, that
each species or even population exhibits fairly constant
ranges of size for different kinds of cells. This leads to
the concept of cardinal points in the diatom life history
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
(reviewed by Davidovich 2001, Edlund & Bixby 2001,
Chepurnov et al. 2004), which comprise: (1) the size of
the initial cells; (2) the size of the cells first capable of sexual size restitution [i.e., the position of the critical (upper)
sexual size threshold]; and (3) the size at which cells die,
because they have reached the minimum viable size. (4) A
fourth cardinal point exists in diatoms with a closed life
cycle, namely the size at which cells lose the capacity for
auxosporulation (the lower sexual size threshold).
4. Sexual reproduction: cell types and development
4.1. Sexual reproduction in diatoms refers to the whole
process of sexualization, the production of gametes (or
gametic nuclei) through the differentiation and development of gametangia, meiosis and subsequent fertilization
to produce zygotes (full sexuality, Fig. 1). In cases where
fertilization involves the fusion of nuclei derived from the
same gametangium, the diatom may be said to exhibit
reduced sexuality, as, for example, in autogamy.
4.2. A gamete is a haploid cell (or occasionally an unreduced diploid cell, if meiosis fails) that fuses with another
such cell during sexual reproduction, leading to fertilization. Diatoms produce several types of gametes.
4.2.1. Fusing gametes may be physiologically and
morphologically identical (isogametes), in which case fertilization (and therefore also sexual reproduction itself)
is isogamous, as in Eunotia tropica Hustedt (Idei in
Hori 1993) or Achnanthidium (= Achnanthes) minutissimum (Kützing) Czarnecki (Mizuno in Hori 1993). Or,
the gametes may be morphologically or physiologically
different (anisogametes), in which case fertilization is
morphologically or physiologically anisogamous, as in
Licmophora communis (Heiberg) Grunow or Tabularia
(Kützing) D.M. Williams & Round (Chepurnov & Mann
2004, Davidovich et al. 2011). The most extreme, differentiated form of anisogamous reproduction is oogamy, in
which a large egg cell is fertilized by a small uniflagellate sperm. Almost as extreme anisogamy occurs also
in a few pennate species. For example, in Rhabdonema
Kützing, one or two large, non-motile ‘eggs’ and small
non-flagellated but motile spermatia are produced (see
section 4.2.6). In those diatoms in which sexually compatible gametes resemble each other morphologically but
differ in their behaviour (e.g., one being motile while the
other is not), reproduction is said to be physiologically
anisogamous (Neidium, Sellaphora Mereschkovsky: Mann
1984, 1989b); it is recommended that such cases are always
referred to as ‘physiological anisogamy’ rather than simply
‘anisogamy’, to avoid the implication that gametes differ in
size or visible structure or are differentiated into sperm and
eggs.
4.2.2. In anisogamous diatoms, it is conventional to refer
to sometimes smaller, motile gametes as ‘male’gametes
and non-motile gametes as ‘female’gametes. In oogamous
diatoms, these terms are unlikely to cause any confusion
267
(the uniflagellate sperm, and the cells that produce them,
are ‘male’, and oogonia producing egg cells are ‘female’;
e.g., in Melosira varians C. Agardh: von Stosch 1951).
By extension, the amoeboid small spermatia in Rhabdonema adriaticum Kützing (von Stosch 1958), the swirling
and rotating gametes in Tabularia fasciculata (C. Agardh)
D.M. Williams & Round (Davidovich et al. 2010) and
Pseudostaurosira D.M. Williams & Round (Sato et al.
2011), and the motile gametes of Nitzschia longissima
(Brébisson) Ralfs (Davidovich et al. 2006) and Sellaphora
species (Mann 1989b) can also be termed ‘male’. For
the same diatoms, the ‘egg cells’ of the araphid pennates Rhabdonema, the non-motile gametes of Tabularia
and Pseudostaurosira, and the non-motile gametes of
Nitzschia longissima or Sellaphora can be termed ‘female’.
Further, if a gametangium (see section 4.4) produces only
motile gametes or only non-motile gametes, it is convenient to refer to them as ‘male’ or ‘female’ gametangia,
respectively.
Note that it is not implied that the ‘male’ gametes
of non-oogamous diatoms are homologous with sperm,
or that the ‘female’ gametes are homologous with egg
cells. It should be noted also that, using gamete size
alone as an indication of its sex or of the occurrence of
anisogamy is unreliable in pennate diatoms, since the size
of gametes depends on the size of the gametangium producing them (Davidovich 2001) and thus will vary over
the life cycle of a clone as the vegetative cells capable
of becoming gametangia diminish in size. Consequently,
motile ‘male’ gametes may sometimes be larger than the
passive gametes they fertilize, e.g., in Pseudostaurosira
(Sato et al. 2011).
4.2.3. In some cases (e.g., Pinnularia nodosa (Ehrenberg) W. Smith: Poulíčková & Mann 2008), cells are
encountered that are similar to gametes in their ploidy and
how they are formed, but that appear incapable of fusing with each other. These ‘pseudogametes’ may have no
function and may be teratological.
4.2.4. An egg is the large, immobile macrogamete of
oogamous diatoms, which may be enclosed, where only a
small part of the egg cell is exposed to allow fertilization
(e.g., Leptocylindrus danicus Cleve, Melosira moniliformis
(O.F. Müller) C. Agardh: French & Hargraves 1985, Idei &
Chihara 1992), or exposed, where the oogonium dehisces
to expose a large area for fertilization (e.g., Attheya decora
West: Drebes 1977b), or free, where the egg cell is liberated into the medium apparently rendering the entire cell
surface available for fertilization (e.g., Lithodesmium undulatum Ehrenberg, Ditylum brightwellii (West) Grunow:
Manton & von Stosch 1966, Koester et al. 2007;
Fig. 3).
4.2.5. Sperm are the anteriorly uniflagellate microgamete of oogamous diatoms (Fig. 4), e.g., Melosira varians (von Stosch 1951). Terms for sperm ultrastructure
(e.g., transitional fibres, mastigonemes) are not included
here: many are illustrated and recently reported for sperm
268
Kaczmarska et al.
Fig. 3. Oogonium with one egg nearly free and the other
still within the oogonial frustule in Lithodesmium undulatum,
redrawn after Manton & von Stosch (1966) with the permission
of Blackwell Science Ltd, UK.
Fig. 4. Opened mature spermatogonangium with uniflagellate sperm and frustule-less secondary spermatocytes in Lithodesmium undulatum, redrawn after Manton & von Stosch 1966
with the permission of Blackwell Science Ltd, UK.
ultrastructure in Thalassiosira Cleve and Melosira C.
Agardh (Idei et al. 2013).
4.2.6. A spermatium is a non-flagellate microgamete,
which may possess some capacity for movement, including amoeboid movement, as in Rhabdonema (von Stosch
1958), or more vigorous types of motion seen in some other
araphid species. For example, in two species of Tabularia
(T. tabulata (C. Agardh) Snoeijs and T. fasciculata), gamete
movements coincide with growth and retraction of cell
surface projections that are behaviourally and morphologically consistent with pseudopodia (Davidovich et al. 2010,
2011). In Pseudostaurosira trainorii E.A. Morales, motility
comprises amoeboid and/or spinning movements associated with the extrusion and retrieval of microtubule-based
threads (Sato et al. 2011).
4.3. A gametogonangium is a cell from which or in which
the gametangia are formed.
4.3.1. A spermatogonangium is a diploid cell that
undergoes successive depauperating mitotic cell divisions
(Fig. 4; see section 4.3.2). These divisions may be accompanied by the formation of reduced, more or less silicified
Fig. 5. Spermatogenesis (sensu lato) in Odontella. Maturing
spermatogonangium with four spermatogonia at varying stages
of development (two are in the primary spermatocyte stage and
two in the secondary spermatocyte stage); in Odontella granulata
spermatogonia carry vestigial valves, redrawn after von Stosch
(1958) with the permission of John Wiley & Sons Ltd.
or vestigial thecae (Melosira sp., Odontella [= Biddulphia] granulata (Roper) Ross: Drebes 1977a; Fig. 5) or
produce entirely valve-less spermatogonia (Coscinodiscus granii, Schmid 1995; Fig. 4) following respective
cytokineses. It may also involve acytokinetic mitoses, all
within the confines of the spermatogonangial frustule. Divisions within a spermatogonangium lead to the production
of spermatogonia (see section 4.4), which in diatoms usually undergo meiosis to produce sperm and therefore are
primary spermatocytes.
4.3.2. Depauperating cell divisions (these have sometimes, incorrectly, been called ‘depauperizing’ divisions,
e.g., Drebes 1977a) are successive differentiating steps
of mitosis and cytokinesis of the spermatogonangia that
are not accompanied by growth of the daughter cells, so
that the resulting cells become smaller and smaller until
primary spermatocytes are produced. Depauperating divisions occur during the spermatogenesis in centrics (e.g.,
Chaetoceros didymus Ehrenberg, Coscinodiscus granii:
von Stosch et al. 1973, Schmid 1995), and also during
the formation of the spermatia in the araphid pennate
Rhabdonema (von Stosch 1958; Fig. 6).
4.4. A gametangium is a cell that undergoes meiosis to
produce gametes. In oogamous diatoms, this term will
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
Fig. 6. Formation of spermatia and egg in Rhabdonema adriaticum (redrawn from von Stosch 1958 with the permission of
John Wiley & Sons Ltd). The residual body left after the spermatial maturation is omitted here (see schematic representation of the
process in Fig. 12, Level 3D).
usually be replaced by oogonium, for a cell in which one
(e.g., Chaetoceros diadema (Ehrenberg) Gran: French &
Hargraves 1985) or two egg cells (e.g., Odontella mobiliensis (Bailey) Grunow: von Stosch 1954) are produced
following meiosis, and spermatogonium for a cell that subsequently produces the sperm (or spermatia in the araphid
pennate Rhabdonema). In the many pennate diatoms that are
isogamous, there is no obvious or consistent differentiation
into different types of gametangia (see section 4.5.7).
4.5. Gametogenesis is the process by which gametes are
formed within a gametangium. Since diatoms are diplonts
(see section 3.1), gametogenesis always includes meiosis
but the process and the products differ between centric and
pennate species.
Two types of gametogenesis occur in centric diatoms:
spermatogenesis, in which sperm are formed via meiosis
from a primary spermatocyte (see sections 4.5.2–4.5.4)
and oogenesis, in which one or two eggs are produced via
meiosis from a primary oocyte (see section 4.5.6).
4.5.1. By analogy with the development of chytrid fungi
(Webster & Weber 2007, p. 128), the production of gametes
by a gametangium (centric or pennate) can be said to be
holocarpic if the whole of the gametangial protoplast is
converted into gametes, and eucarpic if part of the gametangial protoplast is excluded as a residual cell or residual body
(see sections 4.5.9 and 4.5.10).
4.5.2. Spermatogenesis is strictly the process in oogamous diatoms by which a diploid primary spermatocyte
undergoes meiosis to produce sperm, but the term can also
be applied more loosely to the whole process by which
spermatogonangia give rise to sperm (e.g., Actinocyclus
sp., Coscinodiscus granii: Idei in Hori 1993, Schmid 1995;
Fig. 7A–D).
4.5.3. In hologenous spermatogenesis, the whole of
the primary spermatocyte is partitioned among the four
sperm, e.g., Attheya decora (Drebes 1977b; Fig. 7A), i.e., it
269
is holocarpic. Generally, the primary spermatocyte divides
to form two haploid secondary spermatocytes (Figs 5,
7A–B) at the end of meiosis I (sometimes referred to as
proto-gametes, as in Lithodesmium undulatum, Manton
& von Stosch 1966), and these secondary spermatocytes
then divide to produce two haploid spermatids, which
differentiate into sperm, e.g., Attheya decora (Drebes
1977b).
4.5.4. In merogenous spermatogenesis, the spermatids
bud off from the spermatocyte(s) after meiosis II, leaving
one or two residual bodies (see section 4.5.10) (Fig. 7B–C),
so that the development is eucarpic. In merogenous species,
the sperm often lack chloroplasts because these are segregated into the residual bodies. Examples are Actinocyclus
sp. (Idei in Hori 1993, Idei et al. 2012; Fig. 7C) and Pleurosira laevis (Ehrenberg) Compère (= Biddulphia laevis:
Heath & Darley 1972; Fig. 7B).
4.5.5. A plasmodium is a mass of protoplasm containing several nuclei resulting from acytokinetic nuclear
divisions in the spermatogonangium, e.g., during spermatogenesis in Guinardia flaccida (Castracane) H. Peragallo
(Fig. 7D) or Pleurosira laevis (Heath & Darley 1972). The
plasmodium acts as the spermatocyte, cleaving off sperm. It
is suggested that in diatoms this term should only be applied
to cells with four or more functional nuclei.
4.5.6. Oogenesis is the process by which an egg cell
is formed within an oogonium by oogamous diatoms
(Figs 8A–C, 9–11, 12C). Within each oogonium is one
oocyte, a cell whose nucleus will enter meiosis. The number
of eggs produced within an oogonium is either one (e.g.,
Melosira moniliformis, Rhabdonema adriaticum, Odontella rhombus (Ehrenberg) Kützing: von Stosch 1956, 1958,
Migita 1967; Fig. 8C) or two (Attheya decora: Drebes
1977b). Oogenesis varies in whether or not a cytokinesis
takes place in the oogonium, the equality of the cytokinesis if present, and the fate of the haploid nuclei. Variants
include: (1) an equal cytokinesis following meiosis I with
degeneration of one nucleus in each cell after meiosis II
(Fig. 8A) to produce two eggs, e.g., in O. mobiliensis or
O. granulata (von Stosch 1954, 1958; Fig. 9); (2) an unequal
cytokinesis following meiosis I, producing a residual cell
(see section 4.5.9), which does not develop further, and
a cell that undergoes meiosis II with degeneration of one
nucleus, e.g., in O. rhombus or Cerataulus smithii Ralfs ex
Pritchard (von Stosch 1956; Fig. 10) or Rhabdonema adriaticum (von Stosch 1958; Fig. 6); and (3) no cytokinesis
with degeneration of a nucleus after each of meiosis I and
II, e.g., in Melosira varians (von Stosch 1954) or Bacteriastrum hyalinum Lauder (Drebes 1972) (see Figs 8C,
11, respectively). Types 1 and 3 are holocarpic, type 2 is
eucarpic.
4.5.7. Pennate gametogenesis: in most pennate species
examined, the gametogenesis occurs after pairing of
sexualized vegetative cells; after meiosis, one or two
iso- or anisogametes (see section 4.2.1) are produced per
gametangium (Fig. 12A–D)
270
Kaczmarska et al.
Fig. 7. Schematic representation of the types of spermatogenesis reported in centric diatoms. Level 1, depauperating (A–C) and acytokinetic (D) mitoses; level 2, meiosis I and the secondary spermatocytes; level 3, meiosis II and mature sperm cells, residual bodies and
gametic nuclei in plasmodium. Four variants (A–D) of the process are indicated vertically, including sperm from equal meiosis I and II in
column A; the sperm separate from two-nucleated cells; B–C sperm separate from two- or four-nucleated cells following meiosis II and
the detachment from residual bodies (irregularly shaped cells); D represents an acytokinetic development of the spermatogonangium in
Guinardia flaccida as described in Hoppenrath et al. (2009), resulting in the formation of a plasmodial primary spermatocyte (for simplicity
the plasmodium is shown as containing only two diploid nuclei). Two- and four-nucleated cells are not illustrated. IK, original.
4.5.8. Gamete rearrangement: in pennate species,
cytokinesis (after meiosis I) proceeds in the median valvar
plane of the gametangium, as during mitotic cell division.
However, the daughter protoplasts sometimes slide over
each other (rearrange) to move from their initial parallel
positions beneath each valve to lie one towards each pole
of the gametangium, as in Caloneis silicula (Ehrenberg)
Cleve (Mann 1989a) and Pinnularia cf. gibba Ehrenberg
(Poulíčková et al. 2007).
4.5.9. Residual cells (= polar body; = supernumerary
cell pro parte) are sometimes cut off during gametogenesis
and other divisions. They are small cells, containing one
or more nuclei (haploid or diploid) and a small amount of
cytoplasm, e.g., in Cerataulus smithii or O. rhombus (von
Stosch 1956; Figs 6, 9) or Eunotia bilunaris (Ehrenberg)
Schaarschmidt (Mann et al. 2003; Figs 12D, 23). Whether
residual cells perform any function in gametogenesis other
than being receptacles for superfluous protoplast and nuclei
is currently unclear. It has been suggested that they may in
some cases facilitate plasmogamy through their expansion
(e.g., in Sellaphora: Mann 1989b). Residual cells are also
formed, with diploid nuclei, during the vegetative phase of
the life cycle (see section 10).
4.5.10. A residual body is a cell produced by a
gametangium that does not function as a gamete and
contains no nucleus, unlike residual cells, but sometimes
contains chloroplasts (e.g., in merogenous spermatogenesis of centric diatoms and some pennate species such as
Rhabdonema: von Stosch 1958).
4.5.11. Pyknosis: during gametogenesis, diatom nuclei
are often destroyed as part of normal development. Degenerating nuclei were first observed when stained with dyes
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
271
Fig. 8. Variations of oogenesis in centric diatoms. Gametangium (normally containing only one primary oocyte), meiosis I and its
products, the secondary oocytes, and meiosis II and mature gametes are illustrated horizontally. Columns A–C illustrate variants of the
process resulting in different number of eggs, with the irregular cell outline for the residual cell. IK, original.
like carmine, safranin and haematoxylin, where they appear
as strongly staining, dense bodies. For this reason they were
termed pyknotic nuclei (the Greek origin indicates thickening, compaction) and it is suggested retaining this term.
Pyknotic nuclei are also found after acytokinetic mitotic
divisions of auxospores (see section 3.4) and vegetative
cells (see section 10.3).
5. Types of sexual reproduction
5.1. Allomixis refers to a fully sexual mode of reproduction,
in which fertilization occurs between gametes derived from
different individual cells (Figs 13–14). Such organisms may
be either outbreeding or inbreeding, but diatoms are termed
allomictic whether or not the gametes are derived from cells
of different clones or from cells of the same clone, as long as
the compatible gametes are produced by different individual
cells. The fusion of gametes in allomictic diatoms is referred
to as allogamy and the terms allomictic and allogamous
can often be used interchangeably. By definition, allomictic
diatoms exhibit biparental auxosporulation.
5.1.1. Gametangiogamy refers to the type of sexual
reproduction observed in many allomictic pennate diatoms,
in which the primary step in sexual reproduction is pairing
and recognition between the gamete-producing cells (the
gametangia), rather than between the gametes themselves.
5.2. Automixis refers to a form of reduced sexuality and genetic recombination in which the fertilization
occurs between gametes or haploid nuclei derived from
the same cell. Automixis is an extreme form of inbreeding in diatoms; at the other end of the spectrum of
breeding behaviour is extreme outbreeding, comprising
matings between genealogically distant cells. Automictic
diatoms exhibit uniparental auxosporulation, as do apomictic diatoms. Two kinds of automixis are recognized:
paedogamy and autogamy.
5.2.1. Paedogamy is a fusion of two gametes within
a single gametangium; for this to be possible, cytokinesis must occur within the gametangium during meiosis and
this apparently always occurs at meiosis I. Examples are
Neidium cf. ampliatum (Ehrenberg) Krammer (Poulíčková
2008a; Fig. 15) and Nitzschia fonticola (Grunow) Grunow
(Trobajo et al. 2006).
5.2.2. Autogamy is a fusion of two gametic (haploid) nuclei within an undivided cell after meiosis II. The
fusing nuclei may be any nuclei from among the four products of meiosis II, as in Cyclotella meneghiniana (Iyengar
& Subrahmanyan 1944; Fig. 16) or Pinnularia nodosa
(Poulíčková & Mann 2008); alternatively, the fusing nuclei
may be two sister nuclei from meiosis II, when one of
the nuclei degenerates after meiosis I, as in Thalassiosira
angulata (Gregory) Hasle (Mills & Kaczmarska 2006;
Fig. 17). The genetic consequences of these two types of
autogamy are different.
5.3. Apomixis refers to auxosporulation in which the
formation of the auxospore resembles that seen in alloand automictic auxosporulation, but in which meiosis is
replaced by pseudomeiosis (a process involving stages
resembling meiotic prophase, but without reduction in
ploidy), followed by a mitotic division, or by differentiation of a pseudozygote (a cell resembling the zygote of
related allomictic or automictic species) from a diploid vegetative cell. Examples are Cocconeis placentula Ehrenberg
(Geitler 1927a, b, 1973), Achnanthes cf. subsessilis Kützing (Sabbe et al. 2004) and Eunotia sp. (Chepurnov et al.
2004).
272
Kaczmarska et al.
Fig. 10. Mature oogonium with egg and residual cell in Cerataulus smithii, redrawn after von Stosch (1956) with the permission of Springer Publishing.
Fig. 9. Mature oogonium with two eggs in Odontella granulata,
redrawn after von Stosch (1958) with the permission of John Wiley
& Sons Ltd.
5.4. Haploid parthenogenesis is the development of
an unfused gamete into an auxospore and subsequently
an initial cell, which may divide to produce a clonal
lineage of (at least initially) haploid cells. A number of examples (listed by Chepurnov et al. 2004) are
known from cultures and laboratory populations but it
is unknown whether the phenomenon occurs in natural
populations.
6. Sexuality of allomictic diatoms
General terminology
The following section has caused us more difficulty than
any other and represents a consensus terminology. Although
many of the phenomena dealt with have been known for
a long time, they have been described in a variety of
ways, which are not always easily reconciled. Furthermore, the genetic and physiological bases of many of
these phenomena are little known. Accordingly, supplied
here is a limited set of terms, which will probably not
cover all the possibilities diatoms exhibit, dealing with
the characteristics for which there are most data, such as
the morphology and behaviour of sex cells and sexualized
clones. Consequently, the definitions and the summary presented in Table 1 can be expected to need modification and
amplification in the future, to transcend what is essentially
a phenotype-based terminology.
In the following paragraphs overarching concepts are
presented first, including the mating system (hetero- versus homothally, mating types), and then discussion of
terms to describe the sexuality of individual cells and
clones. With respect to the latter, the focus is on visible
(primarily morphological or behavioural) characteristics.
According to these, four sex phenotypes can be distinguished in diatom cells and clones: ‘male’ (= motile),
‘female’ (= non-motile), hermaphrodite (expressing both
male and female characteristics), and genderless (not clearly
either male or female). ‘Male’ and ‘female’ are used in
a conventional sense, reflecting the sexual differentiation
of gametes, gametangia and gametophytes in multicellular
‘higher’ organisms possessing motile sperm or dispersed
pollen (male gametophytes) and immobile egg cells or
embryo sacs in female gametophytes; in diatoms, the naming reflects differences in motility, and sometimes also in
morphology. Accordingly, ‘genderless’ cells and clones are
those found in isogamous diatoms (exclusively among pennate diatoms), where all gametes are moderately motile
and there is no phenotypic distinction into male or female,
e.g., in Eunotia Ehrenberg and some Amphora Ehrenberg ex Kützing (Geitler 1969). Genderless and cosexual
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
Fig. 11. Mature oogonium with single egg carrying one gametic
and two pyknotic nuclei in Bacteriastrum hyalinum, redrawn
after Drebes (1972) with the permission of Schweizerbart Science
Publishers (www.schweizerbart.de).
cells (see sections 6.7 and 6.10) and clones may nevertheless be differentiated biochemically (see explanatory
note under section 6.8). In diatoms exhibiting physiological anisogamy, motile but non-flagellate male gametes are
sometimes referred to as ‘active’ (‘+’) and the non-motile
females as ‘passive’ (‘−’). However, it is probably best to
avoid the implication that the females are inactive, since
it is quite likely that they secrete pheromones to orient the
movement of the males (cf. Sato et al. 2011). There are
some inconsistencies between what is proposed here and the
terminology adopted previously (e.g., Chepurnov & Mann
1997; see section 6.16).
It should be noted that the classification of diatoms
into heterothallic and homothallic is largely independent
of the classification of gametes and clones into unisexual, male, female, cosexual, etc.: one deals with the
mating system, the other with visible sexual differentiation. For example, among heterothallic diatoms, both
mating types of Nitzschia palea (Kützing) W.Smith produce
only cosexual gametangia (Trobajo et al. 2009) and both
mating types of Amphora copulata (Kützing) Schoeman
273
& R.E.M.Archibald produce only genderless gametangia
(Mann & Poulíčková 2010), whereas each mating type of
Pseudo-nitzschia multiseries (Hasle) Hasle (Davidovich &
Bates 1998) and Sellaphora capitata D.G. Mann & S.M.
McDonald (Mann et al. 1999) expresses a different sex, male
or female. Among homothallic diatoms, many centrics and
Sellaphora bisexualis D.G. Mann & K.M. Evans (Mann
et al. 2009) produce male and female unisexual cells
within a single clone, but in other cases, all gametangia of all clones are apparently alike, being cosexual
(Gomphonema parvulum (Kützing) Kützing: Geitler 1932)
or genderless (Cocconeis scutellum Ehrenberg: Mizuno
1987).
6.1. Sexual potential: the intrinsic capacity of cells to
develop particular sexual structures, sexual identity and
behaviour, according to their mating type or sex. The
potential is realized when sexualization (see section 6.2)
is induced by internal and/or external factors.
6.2. Sexualization is the initiation of the process by which
cells realize their sexual potential and begin gametogenesis.
6.3. Mating system: the pattern of mating and sexual
interactions between individuals of a population (clonal or
natural), including the balance between inbreeding and outbreeding, and whether clones are differentiated into different
sexes or mating types.
6.4. Homothally refers to mating systems in which pairing
cells or gametes can be derived from the same or different
clones, i.e., sexual reproduction can occur intraclonally as
well as interclonally and clones are self-fertile. The term
was originally introduced for fungi, referring to organisms
in which individual thalli (mycelia) or clones can complete
the sexual cycle on their own (Whitehouse 1949, Moore &
Novak Frazer 2002).
Many centric diatoms appear to be homothallic (in a
single clone some individual cells sexualize into oogonia, others into spermatangia) and can self-fertilize, at least
in vitro (e.g., Chaetoceros didymus: von Stosch et al. 1973),
as can some pennates (e.g., Pseudo-nitzschia brasiliana
Lundholm, Hasle & G.A. Fryxell: Quijano-Scheggia et al.
2009). However, little is known about how homothallic
diatoms mate in nature, i.e., when and/or if a number of
homothallic clones of the same species sexualize at the same
time and interbreed. At least some clones of homothallic
centric species exhibit strategies that will result in outcrossing, e.g., a size-dependent propensity to produce, at
times, only oogonia or only spermatangia (as in sequential
hermaphrodites: see section 6.11.2), or different external
requirements for induction of male and female gametogenesis (e.g., Lithodesmium undulatum: Manton & von Stosch
1966), which may be clone specific.
6.5. Heterothally refers to mating systems in which clones
have dissimilar sexual potentials (identities) and are differentiated into two or more sexes or mating types. In these,
successful syngamy generally occurs only between members of different clones having opposite but complementary
274
Kaczmarska et al.
Fig. 12. Schematic representation of variants of gametogenesis in pennate diatoms. Level 1, transformation of sexualized cells into
gametangia (containing primary meiocytes), which may involve prior depauperating mitoses (thus far known only in Rhabdonema);
level 2, meiosis I and the secondary meiocytes; level 3, meiosis II and mature gametes. A–B, the main variants of gamete formation; C–D,
the gametogeneses in Rhabdonema. (C, ‘oogenesis’; D, spermatiogenesis); the unequal secondary meiocyte at 2C indicates the production
of a residual cell while the body with an irregular outline (3D) represents the residual body produced during the production of merogenous
spermatium. *Case of unequal meiosis I with the production of a residual cell and only one functional gamete in Eunotia bilunaris, cf.
Fig. 23. IK, original.
sexes or mating types. In strictly heterothallic diatoms,
each clone is fully self-sterile, e.g., Pseudo-nitzschia multiseries (Davidovich & Bates 1998, even after years in monoclonal cultures), but in other cases the different mating types
or sexes may show some capacity for intraclonal reproduction. Heterothally was first applied in fungi where sexual
reproduction occurs through the interaction of two different, compatible thalli (mycelia) or clones (e.g., Whitehouse
1949, Hawksworth et al. 1995).
6.5.1. In heterothallic diatoms, clones of the same sexual
potential are referred to as having the same mating type and
in strictly heterothallic species, successful sexual reproduction can only occur between cells of opposite or compatible
mating type. In some species, the mating types differ in the
kinds of gametes they produce. For example, the gametes
produced by one of the mating types of Sellaphora capitata,
Nitzschia longissima or Tabularia fasciculata are motile
(Mann et al. 2004, Davidovich et al. 2006, 2010), whereas
the gametes produced by the other mating type are nonmotile. In this case, the mating type in which the gametangia
produce motile gametes can be thought of as ‘male’, while
the other is ‘female’. In other cases, the mating types cannot
be distinguished on the basis of the form or visible behaviour
of the gametes, but in at least one case they are separable
instead according to the motility of the gametangia (Gillard
et al. 2013).
6.5.2. A system for naming mating types in individual diatom species has been proposed by Chepurnov et al.
(2005), similar to that used in other algae to designate sexcompatible mating types (e.g., mt+ and mt–, as in Lewin
1954, albeit that the system was used there for the gametangia and gametes of green algae, which are haploid). An
acronym is formed from a few letters of the genus and
species names, followed by a suffix to differentiate the two
(or more) mating types: + or − where the mating types differ in the activity of the gametes they produce (+ motile, −
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
275
Fig. 14. Allogamic pair producing isogametes in a nitzschioid
diatom. IK, original.
Fig. 13. Allogamic pair producing anisogametes in a nitzschioid
diatom. IK, original.
non-motile); a number, if the gametangia are not obviously differentiated (as in some Eunotia or Amphora); or
some other symbol that has a meaning in relation to the
characteristics of mating. For example, in the heterothallic,
morphologically isogamous diatom Pseudo-nitzschia pungens (Grunow ex Cleve) Hasle, one mating type produces
motile gametes and is designated PNp+ , whereas the other
produces non-motile gametes and is designated PNp− .
Phenotypic expression of sexuality in allomictic diatom
cells and clones
Expression of sexuality in individual cells
6.6. Unisexual cells are cells expressing only one sex,
‘male’ (or ‘+’) or ‘female’ (or ‘−’) and hence producing
only one type of gamete, either ‘male’ (motile) or ‘female’
(non-motile). For example, some cells of centric diatoms
only produce small, flagellated sperm and others only produce large and non-motile eggs. Similarly, some cells of
Pseudo-nitzschia multiseries produce two motile ‘male’
gametes, while others produce two non-motile ‘female’
gametes. However, although each sexualized cell is unisexual in centric diatoms, the clones producing them may
be polysexual (as in Chaetoceros didymus, Attheya decora, Odontella longicruris (Greville) Hoban: von Stosch
et al. 1973, Drebes 1977b, Hoban 2008). By contrast, in
the heterothallic Pseudo-nitzschia multiseries (Davidovich
& Bates 1998), each sex (producing either male or female
gametangia) is expressed in a genetically different clone
(= unisexual clone, see section 6.9).
6.7. Cosexual cells exhibit a type of hermaphroditism
in which each cell expresses the characteristics of two
sexes equally, by producing two gametes in the same
gametangium, one of which is motile (‘male’), the
276
Kaczmarska et al.
Fig. 15. Paedogamy in Neidium cf. ampliatum after meiosis II
(upper) and plasmogamy (lower). AP, original.
Fig. 16. Autogamy in Cyclotella meneghiniana, after meiosis II
(left, pyknotic nucleus produced following meiosis I) and after
karyogamy (right). IK, original.
Fig. 17. Autogamy in Thalassiosira angulata, following meiosis II (left) and after karyogamy (right). IK, original.
other non-motile (‘female’). Examples are Nitzschia recta
Hantzsch (Mann 1986), N. palea (Trobajo et al. 2009),
Gomphonema Ehrenberg or Cymbella C. Agardh (Geitler
1932, 1973), in which gametes are exchanged between
paired gametangia.
6.8. Genderless cells are cells whose gametes express
no differential morphological or behavioural characteristics during their sexual interactions with other sexualized
cells: there is no difference in motility or consistent difference in size and hence no possible classification into ‘male’
or ‘female’. Examples are in Eunotia and some Amphora
(Geitler 1969, 1973).
Note: the designation as ‘genderless’ refers to a lack
of morphological and behavioural differentiation; it does
not necessarily mean that there are no biochemical differences (cryptic sexual differentiation) between the gametangia and gametes. For example, although the gametes
of Amphora copulata are apparently all alike (Mann &
Poulíčková 2010), this species displays heterothally, implying a biochemical differentiation between the gametangia
and gametes. The same applies to ‘cosexual’ cells: although
all cosexual gametangia of Nitzschia palea are visibly
alike, each producing one ‘male’ and one ‘female’ gamete
(Trobajo et al. 2009), this does not mean that there is no
sexual differentiation between them, since this species is
heterothallic.
Expression of sexuality in clones (summary comparison
shown in Table 1)
6.9. A unisexual clone is one producing unisexual cells of
only one type during the whole sexual phase of the life cycle.
There are therefore two types of unisexual clone: ‘male’
and ‘female’ clones. Clones of Sellaphora capitata (Mann
et al. 1999) or Pseudo-nitzschia delicatissima (Cleve) Heiden (Amato et al. 2007) seem to be predominantly or wholly
unisexual.
6.10. Cosexual clones consist entirely of cosexual cells (see
section 6.7).
6.11. Polysexual clones are ones in which different individual cells express different sex phenotypes (‘male’ and
‘female’, possibly even cosexual) either simultaneously or
at different times during the life cycle. These clones can also
be referred to as hermaphrodite. A variety of combinations
of sex–phenotype occur in polysexual clones. The same
expression of sexuality may continue throughout the entire
reproductive phase of a clone (constant hermaphrodites:
these are also therefore simultaneous hermaphrodites, see
section 6.11.1), or the sex may be labile (inconstant
hermaphrodites), changing with time, progression through
the life cycle and cell size (in sequential hermaphrodites, see
section 6.11.2), the sex of available mates, or environmental conditions (e.g., Lithodesmium undulatum: von Stosch
1954).
A wide range of hermaphroditism is also common
among individuals of flowering plants and readers may find
it helpful to refer to reviews of angiosperm reproductive
terminology in, for example, Richards (1986), Klinkhamer
et al. (1997), Barrett (2002), de Jong & Klinkhamer (2005)
and Harder & Barrett (2006).
Table 1.
Summary of combinations of mating systems and different types of visible (morphological or behavioural) sex expression in diatoms.
Mating
system
Separate
mating
type
Heterothallic
yes
Variant
Clone
1
Genderless
Sex of
gametangia within
a clone
Example
Notes:
2
Cosexual
all
3
Polysexual
+
Uncertain
no
7
Genderless
5
Uni- and
polysexual
(‘facultative
andromixis’)
6
Uni- and
polysexual
(‘subdioecy’)
all
all or all
or +
a few
all
Amphora
Nitzschia
No example Pseudocopulata
palea
yet known
nitzschia
(Mann &
(Trobajo
multiPoulíčková et al. 2009)
series
2010)
(Davidovich &
Bates
1998)
, male; , female;
?
4
Unisexual
or all
Homothallic
or all
or +
a few
8
Cosexual
all
9
10
11
Polysexual
Constant
Inconstant hermaphrodite
hermaphrodite Labile
Sequential
hermaphrodite hermaphrodite
+
and/or
→
+
→
Nitzschia
Coscinodiscus Navicula cryp- Gomphonema Sellaphora
Lithodesmium Melosira
longissima
granii
tocephala
parvulum
bisexualis
undulatum
varians (von
(Davidovich
(Drebes
(Poulíčková
(Geitler
(Mann et al.
(von Stosch
Stosch 1956)
et al. 2006)
1968)
& Mann
1932)
2009)
1954)
2006)
, cosexual; , genderless (i.e., gametes undifferentiated both morphologically and behaviourally, sexual reproduction therefore being isogamous).
278
Kaczmarska et al.
6.11.1. A simultaneous hermaphrodite is a constant
hermaphrodite clone in which, concurrently, some sexualized cells produce ‘+’ (or ‘male’) gametes, whereas other
cells produce ‘−’ (or ‘female’) gametes. An example is Sellaphora bisexualis (Mann et al. 2009) and probably many
centric diatoms. Cosexual clones are also simultaneous
hermaphrodites.
6.11.2. A sequential hermaphrodite clone is one
whose cells express one sex within part of the life cycle
(and cell size range), after which they switch to produce
cells of a different sex. For example, some centric diatoms
pass through a unisexual phase, when the clonal cells produce only oogonia, then a bisexual phase when oogonia
and spermatangia are produced concurrently, and finally
the alternate unisexual phase, when cells in the clone
produce only spermatangia (e.g., Odontella rhombus or
Melosira varians: von Stosch 1956).
Further explanatory comments, including discussion of
other terms sometimes used in diatoms and their
relationships to those defined in sections 6.1–6.11
6.12. Clones in which all gametangia are always genderless, whatever the stage of the life cycle or circumstances
or environmental conditions, could be referred to as ‘genderless clones’. However, this term is likely often to be
superfluous, since it is as convenient to say that the clones
are ‘isogamous’ (see section 4.2.1)
6.13. ‘Monoecy’ is sometimes applied to sexual reproduction in diatoms. In seed plants, monoecy refers to a condition
in which the flowers or cones are unisexual but are borne
on the same plant, which is therefore hermaphrodite. By
analogy, treating a diatom clone as equivalent to an individual seed plant, most centric diatoms could be said to
be monoecious, since the sperm and eggs are produced
by different cells of a clone; they are also homothallic
and self-fertile, at least in vitro. Another diatom that could
be termed monoecious is the homothallic pennate diatom
Sellaphora bisexualis, because each clone produces both
male and female gametangia (Mann et al. 2009). However,
monoecy and homothallism are not necessarily correlated.
It is conceivable that a diatom could be heterothallic but
also monoecious. Such a diatom would be self-sterile (intraclonal reproduction would be impossible) despite producing
gametes of opposite sex, and fertilization would occur only
between compatible gametes of opposite sex from different
clones (as in outbreeding monoecious flowering plants).
However, no heterothallic monoecious diatoms have yet
been discovered.
6.14. Another term drawn from higher plants and sometimes applied to diatoms is ‘dioecy’. Higher plants in which
male flowers or organs are borne on separate plants from
the female flowers or organs are referred to as exhibiting
dioecy. Hence, the term can be applied to diatoms consisting of unisexual clones (in the sense defined above,
see section 6.9). Examples would be several species of
Pseudo-nitzschia H. Peragallo (Amato et al. 2005), some
clones of Tabularia fasciculata (Davidovich et al. 2010),
or Sellaphora capitata (Mann 1989b). In all of these, each
clone produces gametangia and gametes of only one type,
either male or female.
6.15. ‘Subdioecy’ has been used to refer to the condition reported in the centric diatom Coscinodiscus granii,
in which some clones were unisexual, but a few oogonia
were occasionally formed in ‘male’ clones (Drebes 1968).
Other clones of the same species isolated later from the
same area of the North Sea were polysexual (Drebes 1974),
as was another clone isolated from this area more recently
(Schmid 1995). No centric diatom has yet been discovered
that is fully and strictly heterothallic (dioecious).
6.15.1. A similar phenomenon to ‘subdioecy’ occurs
also among pennate diatoms, since in a few species it
has been reported that some ‘male’ clones produce a few
female gametangia, allowing limited intraclonal reproduction; all other clones are purely male or female. Such
clones producing mostly male gametangia but also small
numbers of females can be termed ‘subandroecious’. This
phenomenon has also been referred to as ‘facultative
andromixis’ (because only ‘male’ clones demonstrated such
sex inconstancy; Davidovich et al. 2006). It remains unclear
whether this is a constitutive property of all cells within such
clones, or reflects a breakdown of self-incompatibility in
some cells. Examples are Nitzschia longissima (Davidovich
et al. 2006) and some ‘male’ clones of Tabularia fasciculata (Davidovich et al. 2010 and references therein). If the
alternative also occurs (where some female clones but no
male clones produce gametangia of the opposite sex), the
labile female clones could be termed ‘subgynoecious’.
6.16. Note: ‘unisexual’, ‘bisexual’ and ‘monoecious’
are used in different senses than Chepurnov & Mann
(1997), who designated clones of Achnanthes longipes as
‘unisexual-1’, ‘unisexual-2, ‘bisexual’ and ‘monoecious’
on the basis of the presence and intensity of mating in
pairwise combinations of clones. In this species, there are
no obvious differences among gametangia or gametes in
morphological or behavioural characteristics: all gametangia are ‘genderless’ in our terminology. ‘Unisexual-1’ and
‘unisexual-2’ clones of A. longipes were able to mate vigorously with each other but displayed very limited ability
to reproduce intraclonally, so that, if these had been the
only kinds of clones within A. longipes, the species could
have been classified in our terminology as heterothallic, producing genderless gametangia. However, the existence of
two other types of clone negates this classification. ‘Bisexual’ clones of A. longipes are able to mate vigorously with
both ‘unisexual-1’ or ‘unisexual-2’ clones, but are unable to
mate intraclonally, whereas ‘monoecious’ clones can mate
freely either intraclonally or with any of the three other
types of clone. Such examples are not fully understood
and may be rare, but they illustrate that our current proposals are incomplete and will need to be revised in due
course.
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
Fig. 18. Lateral pairing between two chains of cells in
Pseudo-nitzschia pungens, schematic representation of gametangia shown at two slightly different times after meiosis II (upper,
immediately after meiosis II; lower, during degeneration of the
pyknotic nuclei). IK, original.
7. Copulation and fertilization
In oogamous diatoms, the gametangia are not physically
linked in any way and sperm are released free into the
environment and swim to the egg cells to fertilize them
(e.g., French & Hargraves 1985). In some anisogamous pennate diatoms too, gametes can be produced without a 1:1
pairing between gametangia (e.g., araphid Tabularia and
Pseudostaurosira trainorii: Davidovich et al. 2010, 2011,
Sato et al. 2011). In other anisogamous and isogamous
pennate diatoms, however, the gametangia become paired
through passive or active movement of vegetative or sexualized cells (as in raphid pennates), and various structures
may be produced to facilitate fertilization. These structures
are related to the fact that the gametes of anisogamous and
isogamous pennate diatoms lack flagella and generally have
no or limited capacity for autonomous motility.
7.1. Pairing is the process, prior to gametogenesis, by which
two or more sexualized cells become closely associated or
come into contact with each other, probably guided by sex
pheromones (Sato et al. 2011, Gillard et al. 2013). There
appear to be two variants: distance pairing (e.g., Eunotia bilunaris, Mann et al. 2003), where the gametangia are
not, or do not need to be, in contact at any time during gametogenesis, and contact pairing, where cells must contact
each other before gametogenesis will proceed (e.g., in Navicula Bory de Saint-Vincent: Poulíčková & Mann 2006).
During contact pairing, which apparently occurs only in
pennate diatoms (although there is insufficient information
to be sure), cells commonly adopt characteristic positions in
relation to each other. Thus, pairing may be lateral (often
but not always girdle-to-girdle, Fig. 18), as in Navicula,
Luticola D.G. Mann and Neidium (Mann & Chepurnov
2005, Poulíčková & Mann 2006, Poulíčková 2008a, b), or
apical, as in surirelloid diatoms, e.g., Cymatopleura solea
(Brébisson) W. Smith (Mann 1987; Fig. 19). In heteropolar diatoms exhibiting lateral pairing, the gametangia may
be parallel, e.g., they have the same orientation (basepole opposite base-pole, head-pole opposite head-pole), or
antiparallel, if they have opposite orientations (base-poles
opposite head-poles) as in Gomphonema (Geitler 1973;
Fig. 20).
7.2. Copulation is the process by which paired gametangia
achieve the spatial interrelationship and physical environment for fertilization to occur. Copulation, so defined,
279
Fig. 19. Apical pairing in Cymatopleura solea, after Mann
(1987) with the permission of Biopress Ltd.
Fig. 20. Antiparallel position of laterally paired gametangia in
Gomphonema constrictum var. capitatum, redrawn after Geitler
(1973) with the permission of Springer Publishing.
is restricted to pennate diatoms. Copulation may be
free, where mating individuals do not produce detectable
mucilaginous envelopes, e.g., Pseudo-nitzschia multiseries
(Davidovich & Bates 1998) or Navicula (Poulíčková &
Mann 2006), or involve the formation of special copulation
structures (see below and Mann 2011).
7.2.1. The copulation envelope is a translucent mass
of mucilage produced by and surrounding the gametangia.
Some are diffuse (watery and visible only with differential
interference contrast illumination or after staining), as in
280
Kaczmarska et al.
Fig. 21. Copulation envelope in Gomphonema olivaceum,
redrawn after Geitler (1932) with the permission of Elsevier.
Pinnularia (Poulíčková et al. 2007) or Luticola (Poulíčková
2008b), while others are compact capsules (dense and
clearly visible in LM) as in Placoneis gastrum (Ehrenberg) Mereschkovsky (Mann & Stickle 1995). Compact
copulation envelopes can be divided into structured and
unstructured variants, according to whether the capsule
is homogeneous or differentiated into two or more layers
(Fig. 21).
7.2.2. The copulation aperture is a localized opening
formed between two gametangia to facilitate plasmogamy,
as in Sellaphora (Mann 1989b). Analogous apertures may
be present in centric diatoms to allow access of sperm to
the egg cell, e.g., in Isthmia nervosa Kützing (Steele 1963)
or Coscinodiscus granii (Schmid 1995).
7.2.3. Copulation tubes are formed by the fusion of two
copulation papillae that grow out from the girdle region of
paired gametangia, through which the gametes move to fertilize each other, e.g., Nitzschia recta (Mann 1986; Fig. 22)
and Eunotia (Mann et al. 2003; Fig. 23).
7.3. Pseudocopulation is a process resembling the copulation of biparental sexual reproduction, but where each of the
paired cells reproduces uniparentally, through automixis.
7.4. Fertilization or syngamy is the union of gametes to
produce a zygote, comprising plasmogamy and karyogamy
(see sections 7.4.1 and 7.4.2). Fertilization usually involves
some movement of one or both gametes. In some cases
Fig. 22. Copulation tube in Nitzschia recta, drawn after Mann
(1986) with the permission of Biopress Ltd. One gametangium
already with pyknotic nuclei, while the other just completed
meiosis II.
Fig. 23. Copulation papillae in Eunotia bilunaris, inferred after
Mann et al. (2003) with the permission of John Wiley & Sons Ltd.
Note the single functional gamete and a nucleated residual cell in
each gametangium.
this may be passive displacement, but often one or both
gametes are motile, i.e., their motion is autonomous, involving flagella, pseudopodia or amoeboid movements. In some
diatoms, the two sets of fusing gametes behave as a coordinated pair within a confined space, e.g., in Neidium (Mann
1984). In a few diatoms, the fertilization seems to be effected
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
by a swelling of the gametes, e.g., in Craticula Grunow
(Mann & Stickle 1991). In two species of Tabularia male
gametes demonstrate mobility outside the paternal thecae
which involves swirling and forward movement (Davidovich et al. 2010); the mechanism of this motility, seen also
in Pseudostaurosira, is not fully understood (Davidovich
et al. 2011, Sato et al. 2011).
7.4.1. Plasmogamy is the fusion of cells, here of two
gamete cells.
7.4.2. Karyogamy is the fusion of two or more
(gametic) nuclei (contributed either by different gametes
from different gametangia, or from the same gametangium).
7.4.3. In physiologically anisogamous pennate diatoms
producing two gametes per gametangium, there are two
main patterns of behaviour concerning the direction of
gamete fusion (plasmogamy). One is the cis-type, in
which the gametangia are unisexual, both gametes of one
gametangium being motile, whereas the gametes of the
other gametangium are non-motile, as in Mastogloia smithii
Thwaites (Stickle 1986) and Pseudo-nitzschia (Davidovich
& Bates 1998); both zygotes therefore lie within only one
of the gametangia (the ‘female’). The other is the transtype, in which each gametangium produces one motile and
one non-motile gamete (i.e., the gametangia are cosexual);
each motile gamete migrates to the partner gametangium to
copulate with the non-motile gamete resulting in one auxospore developing within each gametangium (e.g., Gomphonema and Neidium: Geitler 1932, Mann 1984). By
definition, cosexual gametangia exhibit a trans-activity of
their gametes.
7.5. A zygote is a cell produced by the fusion of gametes,
irrespective of the timing of karyogamy. In many diatoms,
karyogamy is delayed relative to plasmogamy, so that the
gametic nuclei remain separate in the zygote and even in the
auxospore (expanding stage of the zygote) derived from it.
The auxosporulation of such diatoms can therefore be said
to include a dikaryotic phase.
8. Auxospore types and expansion
Anonymous (1975) and Ross et al. (1979) listed the following types of auxospores, categorized according to their
orientation with respect to the parental cell from which the
auxospore developed.
8.1. A free auxospore has no contact with parental thecae,
e.g., Ditylum brightwellii (Koester et al. 2007) because the
eggs are liberated from the maternal frustule to freely float
in the environment.
8.2. A terminal auxospore is positioned at the end of one
theca of the parent cell, as in Proboscia alata (Brightwell)
Sundström (Cupp 1943) or Leptocylindrus danicus (French
& Hargraves 1985; Fig. 24)
8.3. A lateral auxospore emerges from the girdle area
of the parent cell and expands away from it, as in
Bacteriastrum hyalinum (Drebes 1972) or Rhizosolenia imbricata Brightwell (Hoppenrath et al. 2009; Fig. 25).
281
Fig. 24. A mature terminal auxospore in Leptocylindrus danicus with a resting spore within the auxospore walls, based on
P. Hargraves unpublished material, with author’s permission. IK,
original.
Fig. 25. A young, lateral auxospore in Rhizosolenia imbricata, after Hoppenrath et al. (2009) with the permission of
Schweizerbart Science Publishers (www.schweizerbart.de).
8.4. An intercalary auxospore is flanked by parental thecae, which remain attached during, and sometimes after,
auxospore enlargement, e.g., Thalassiosira angulata (Mills
& Kaczmarska 2006; Fig. 26).
8.5. A semi-intercalary auxospore is flanked on one
side by a parental theca and on the other by a twin
282
Kaczmarska et al.
Fig. 26. An older, intercalary auxospore in Thalassiosira angulata covered with scales (note that the pattern of scale organization
is exaggerated). IK, original.
Fig. 27. Two young, globular, semi-intercalary auxospores in
Odontella regia (a schematic composite of description by von
Stosch 1982 and Hoppenrath et al. 2009). IK, original.
auxospore derived from the same gametangium, e.g., Rhabdonema arcuatum (Lyngbye) Kützing (Karsten 1899) or
Odontella regia (Schultze) Simonsen (von Stosch 1982,
Hoppenrath et al. 2009; Fig. 27).
8.6. Isometric expansion is equal in all directions and
results in auxospores becoming spherical, or bubble-like
at maturity; common in non-polar centrics (and thalassiosiroids) with circular valve outlines (e.g., Fig. 1A;
Coscinodiscus granii: Schmid 1995).
8.7. An anisometric auxospore expands mostly in one or
few directions. Anisometric expansion may be multipolar,
bipolar or unipolar.
8.7.1. Multipolar expansion proceeds in three or more
directions (but all in the same plane), resulting in triangular,
square or star-like shapes at maturity (Fig. 1B; Lithodesmium undulatum: von Stosch 1982).
8.7.2. Bipolar expansion proceeds in two (opposite)
directions resulting in elongate cells; these are usually
isopolar (Fig. 1C; e.g., Neidium sp.: Poulíčková 2008b) but
sometimes expansion at one pole exceeds that at the other,
producing heteropolarity.
8.7.3. A unipolar auxospore expands in only one
direction, again resulting in elongate cells that may or may
not be heteropolar (e.g., Cymatopleura solea: Mann 1987).
9. Auxospore envelope and wall components
Soon after their formation, zygotes (or their equivalents
in diatoms that reproduce apomictically) probably always
form a thin organic wall outside the cell membrane. Little
is known about this structure, which is called the primary
zygote wall. Elements of the gamete envelopes, if any are
present, may also be incorporated into this primary wall.
During maturation, the zygote expands, as an auxospore,
and other organic and silica elements are often added to
the primary zygote wall. The primary zygote wall and parts
that are subsequently added to the zygote wall (secondary
elements) prior to its expansion as an auxospore compose the ‘incunabula’ (see section 9.1: literally ‘swaddling
clothes’ or cradle). Subsequently, the incunabula may be
ruptured and their function in protecting and constraining
the shape of the zygote is taken over (in some centric and
most pennate diatoms) by a new structural component of the
auxospore wall, the ‘perizonium’ (see section 9.2), which
is initially formed underneath the incunabula. As the auxospore expands, the incunabula may be retained as caps or
they may be incorporated into the auxospore wall as its outer
layers. The auxospore wall contains organic components as
well as, or instead of, silicified elements. Together, the silicified and organic components of the auxospore wall help to
control and accommodate directional expansion of the auxospore, building up the shapes of the vegetative cells of the
next generation (von Stosch 1982, Medlin & Kaczmarska
2004). In contrast to polar centric and pennate diatoms, in
some centric (mostly non-polar) diatoms there is no clear
distinction between the components added to the wall by
the early zygote (or even the gametes and oogonium) and
those added by the auxospore (e.g., Kaczmarska et al. 2000,
Idei et al. 2012).
9.1. Incunabula are the organic and inorganic components
(including silicified elements) of the auxospore wall that
are produced by the zygote, prior to its expansion as an
auxospore (equivalent of the primary auxospore wall in
Kaczmarska et al. 2000, 2001 and Medlin & Kaczmarska
2004). Incunabula may continue to surround the auxospore
(including the perizonium when present) as it expands;
alternatively, parts may be separated into cap-like structures covering the auxospore poles. Silicified incunabular
elements are classified as described below.
9.1.1. Scales (= incunabular scales) are flat disc-shaped
elements, usually with a ring-like pattern centre (an annulus), inside of which are randomly arranged pores, and
which subtend a radiating system of secondary ribs that
often branch dichotomously. The ribs are often masked by
further silica deposition, but radial markings may still be
recognizable. Diverse morphologies have been reported,
including simple scales (e.g., Melosira nummuloides C.
Agardh: Round et al. 1990; Fig. 28), which are circular or elliptical; distorted scales with highly irregular
outlines and random perforations (in Isthmia A. Agardh:
M. Idei, unpubl. obs.); slit scales, which bear a slit
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
Fig. 28. Incunabular scale in Melosira nummuloides, after
Round et al. (1990, fig. 64d) with the permission of Cambridge
University Press.
within the area circumscribed by the annulus (in Coscinodiscus granii: Schmid 1995, fig. 2); dendroid scales
(dendroid spine scales), which consist of a tree of dichotomously branching spines arising from a basal disk (e.g.,
Odontella aurita (Lyngbe) C. Agardh: von Stosch 1982,
fig. 11h); and spinescent scales in Triceratium antediluvianum (Ehrenberg) Grunow, with bushy developments of
spines (von Stosch 1982, fig. 13b). Scales are present in
most centric auxospores observed so far and have also been
reported in some pennates, e.g., Grammatophora marina
(Lyngbe) Kützing (Sato et al. 2008b), Tabularia parva
(Kützing) D.M. Williams & Round (Sato et al. 2008c),
Gephyria media Arnott (Sato et al. 2004), Pseudostriatella oceanica S. Sato, Mann & L.K. Medlin (Sato
et al. 2008a), Nitzschia longissima (Kaczmarska et al.
2007), Sellaphora marvanii Poulicková & D.G. Mann
(Mann et al. 2011), Amphora commutata Grunow (S. Sato,
unpubl. obs.), and Diploneis Ehrenberg ex Cleve (M. Idei,
unpubl. obs.). Various other types of scales can be found
in Round et al. (1990, fig. 63) or von Stosch (1982,
figs 1c, 13b). However, no scales have been detected in
some centric auxospores, e.g., Stephanodiscus Ehrenberg
(Round 1982).
9.1.2. Strips (= incunabular strips) bear no perforations
or fringes and are thinner and narrower than the perizonial
bands. They are wound around the zygote and auxospore in
a somewhat irregular manner and, particularly in the early
stages of auxospore expansion, they overlap one another
to make multiple layers. This contrasts with the perizonial
band series, which are always exactly arranged in relation to
the axis of auxospore expansion and show minimal overlap
of their margins. Incunabular strips have been found in polar
centric and raphid pennate diatoms, e.g., Hydrosera whampoensis (A.F. Schwarz) Deby (M. Idei, unpubl.), Pinnularia
cf. gibba (Poulíčková et al. 2007) and Nitzschia fonticola
(Trobajo et al. 2006; Fig. 29).
9.1.3. Plates (= incunabular plates) are structures such
as in Neidium, where, in a typical form, the zygote is almost
completely enclosed by a few large, flat, siliceous lateral
283
Fig. 29. Irregularly spiral incunabular strips in Nitzschia fonticola, after Trobajo et al. (2006) with the permission of John Wiley
& Sons Ltd.
Fig. 30. Incunabular plates consisting of helmet and lateral
plates in Neidium cf. ampliatum, after Mann & Poulíčková (2009)
with the permission of Czech Phycological Society.
plates and two polar caps (Mann & Chepurnov 2005),
which are here renamed as helmet plates to distinguish
them from the incunabular caps defined below (Mann &
Poulíčková 2009; Fig. 30).
9.1.4. Caps (= incunabular caps) are present in pennate diatoms, where the incunabula often split in half at the
equator of the auxospore as it begins to expand and each half
remains attached to one end of the auxospore as an incunabular cap (Gephyria Arnott, Pseudo-nitzschia, Nitzschia
Hassall, Navicula, Luticola, Neidium: Kaczmarska et al.
2000, 2007, Sato et al. 2004, Poulíčková & Mann 2006,
Poulíčková 2008b, Mann & Poulíčková 2009). These have
sometimes been referred to as ‘perizonial caps’, ‘polar caps’
or ‘apical caps’, but it is now clear that they are developmentally and structurally separate from the perizonium and it
is recommended that the term ‘perizonial caps’ be reserved
for the structural cap element of the perizonium present at
the primary poles of Surirellaceae (see section 9.2.1).
284
Kaczmarska et al.
Fig. 31. A set of transverse perizonial bands converging into
a suture in Rhoicosphenia curvata, after Mann (1982) with the
permission of John Wiley & Sons Ltd.
Fig. 32. Fine structure of a transverse perizonial band with an
axial rib and lateral fimbriae. Proximal fimbriae may be reduced
or absent, as in Gephyria media, after Sato et al. (2004) with the
permission of John Wiley & Sons Ltd.
Fig. 33. Longitudinal perizonial bands in Rhoicosphenia curvata, after Mann (1982) with the permission of John Wiley &
Sons Ltd.
Fig. 34. Schematic representation of auxospore wall elements
and their spatial relationships in Pinnularia major, after Ishii et al.
(2008) with the authors’ permission.
Fig. 35. Cross-section of an idealized and hypothetical mature
auxospore illustrating the spatial relationship between wall components and the initial frustule. Individual components of the wall
are based on the following species: spirally arranged incunabular
strips as in Nitzschia, after Trobajo et al. (2006) with the permission of John Wiley & Sons Ltd.; transverse perizonial bands and
suture as in Rhoicosphenia, after Round et al. (1990) with the
permission of Cambridge University Press; and primary and secondary bands of longitudinal perizonium as in Achnanthes, after
Toyoda et al. (2006) with the permission of John Wiley & Sons
Ltd. TW, original.
9.2. The perizonium is a part of the auxospore wall comprising silica bands or rings, hoops and strips (Figs 31–33)
that is formed underneath the incunabula as the auxospore
expands, apparently to control polarity and shape of the
growing auxospore and hence also the species-specific
shape of the initial cell. Spatial relations among these elements of the auxospore wall are illustrated in Figs 34 and
35. The perizonium usually comprises two types of bands
– the transverse and longitudinal perizonial series, here
referred to as the ‘transverse perizonium’ (see section 9.2.1;
Figs 31–32, 34–35) and the longitudinal perizonium (see
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
section 9.2.2; Figs 33–35). However, either the transverse
or longitudinal series may be absent, e.g., in Achnanthes
(Toyoda et al. 2005, 2006) and Pseudo-nitzschia multiseries (Kaczmarska et al. 2000). Each series usually consists
of several elements. Each perizonium, transverse or longitudinal, consists of a primary band (primary transverse
perizonial band, primary longitudinal perizonial band),
which is symmetrical with respect to its axial rib. The
primary band is flanked on both sides by a series of secondary bands which are asymmetrical with respect to their
axial ribs, having fimbria shorter or less developed on the
proximal side to auxospore mid-section.
Perizonial bands overlap each other from the primary
band outwards. The subsequently formed bands flanking
the primary band may all be similar and form a single series
of secondary bands (secondary transverse series, secondary
longitudinal series), or be further differentiated into secondary and tertiary bands, as in Rhoicosphenia Grunow
(Mann 1982) and may subtly differ in structure.
Explanatory remarks concerning the use of
‘properizonium’ and ‘perizonium’
The term properizonium (in German, Präperizonium, translated as ‘pre-perizonium’ in Drebes 1972), was originally
coined by von Stosch & Kowallik (1969, p. 469) for
the system of silicified bands in the auxospore walls of
some polar centric diatoms: ‘Das Perizonium ist eine von
der ursprünglichen Zygotenhülle unabhängige Struktur aus
teleskopartig ineinandergeschobenen kolbenringähnlichen
Kieselelementen, das Präperizonium ähnlich konstruiert,
aber mit der ursprünglichen durch rundliche Schuppen
armierten Zygotenhülle verwachsen’ (The perizonium is a
structure independent from the original zygote wall, formed
of ring-like silica elements that overlap each other as in
a telescope. The properizonium is similarly constructed,
but is knit together inseparably with the original zygote
wall, which is reinforced by rounded scales [our ‘incunabula’]). However, differentiating the properizonia from the
perizonia is questionable for two reasons. First, in some
centric auxospores, e.g., Lampriscus shadboltianum (Greville) Peragallo, L. orbiculatum (Shadbolt) Peragallo &
Peragallo and Trigonium Cleve (Idei & Nagumo 2004, M.
Idei, unpubl.), the incunabula are clearly separate from and
morphologically unlike the ‘properizonia’ illustrated for
other multipolar centrics by von Stosch (1982). Second,
the properizonia and perizonia share a similar morphology
(being composed of organized series of bands) and function (constraining auxospore expansion prior to initial cell
formation, von Stosch 1982, Medlin & Kaczmarska 2004).
Therefore, in order to avoid terminological redundancy, it is
proposed to unify the properizonia and perizonia and refer
to all systems of bands and hoops that are produced by the
expanding auxospore as ‘perizonia’.
9.2.1. The transverse perizonium is a system of silica
bands (Figs 31–32, 34–35) in the auxospore wall – either
285
split or closed rings – oriented perpendicular to the axis
of auxospore expansion. Where most or all of the transverse perizonial bands are split rings, their open ends are
usually aligned with each other along one side of the
auxospore to form a suture (Fig. 34); in such cases, the
primary transverse perizonial band is often a closed
ring, even if all other transverse bands are split or open
(e.g., Rhoicosphenia curvata Kützing: Mann 1982). In
other diatoms (e.g., Lithodesmium Ehrenberg, Chaetoceros
Ehrenberg and Pseudostriatella S. Sato, Mann & L.K.
Medlin: von Stosch 1982, Sato et al. 2008a), the complex
topology of the transverse perizonial bands leaves one side
of the auxospore free of perizonial bands. This leads to the
formation of a clear area of varying width along that side
of the auxospore. Such a clear area may be referred to as
a pseudosuture (Sato et al. 2008a, figs 48, 54). The side
bearing the suture or pseudosuture is defined as the ventral side of the auxospore. The initial epivalve is usually
formed on the opposite or dorsal side of the auxospore.
In Surirellaceae, the auxospore expansion is unipolar. The
primary transverse band is replaced here by a perizonial
cap at one end of the auxospore (Mann 2000, M. Idei,
unpubl.). The transverse perizonium is then formed by
adding secondary bands outwards from this end towards the
opposite end of the auxospore (Mann 1987, figs 34–35).
9.2.2. The longitudinal perizonium is a system of long,
silica bands oriented parallel to the axis of expansion of
the auxospore. Longitudinal perizonial bands usually lie
beneath the suture or pseudosuture of the transverse perizonium, except in some species that are known to form
only a longitudinal perizonium (e.g., Achnanthes: Toyoda
et al. 2005, 2006). In some longitudinal perizonia (e.g.,
Gephyria, Grammatophora Ehrenberg), the bands are a set
of irregular, sprawly bars (Sato et al. 2004, fig. 5i, j) in
which the usual differentiation into bifacial primary and
unifacial secondary bands are not found (Sato et al. 2004,
2008b). In other diatoms (e.g., Rhoicosphenia curvata, Tabularia parva: Mann 1982, Sato et al. 2008c), the structure of
the longitudinal perizonia is substantially the same in that
sides of the primary formed band (primary longitudinal
perizonial band) are flanked by two or more subsequently
formed bands (secondary longitudinal perizonial bands),
whereby each element is overlapped by its more central
neighbour, similar to the transverse series.
9.3. The term epizonium was used by von Stosch (1982) to
refer to structures that are ‘interspersed between the scale
layer [incunabula in our terminology] and the much more
symmetrical prozonium [perizonium in our terminology]’.
It is unclear what these structures are and further research
is needed before the term can be clearly defined.
10. Resting stages and vegetative reproduction
Some diatoms have specialized cells that are produced
via modified mitosis, physiological or cytological processes that help the diatoms perennate, resist or survive
286
Kaczmarska et al.
unfavourable conditions. Two types of resting stages are
known among diatoms: resting spores (see section 10.1)
and resting cells (see section 10.2). While in the resting
stage, these cells are thought to be incapable of size restitution except in species that produce resting spores within the
auxospore (e.g., Leptocylindricus danicus: Fig. 24; French
& Hargraves 1985).
Terms associated with the normal mitotic cell cycle
dominating diatom life history (e.g., protoplast reorganization, chloroplast and nuclear behaviour and division, valve
morphogenesis) are not presented here. For this, readers are
referred to Pickett-Heaps et al. (1984, 1990), Round et al.
(1990) and references therein.
10.1. Resting spores are specialized cells produced in
groups of four, two or one through various ontogenetic
processes, including acytokinetic mitoses, and equal and
unequal mitoses (sometimes resulting in the formation of
incomplete or vestigial valves) during the vegetative portion
of the life history (Fig. 36). Resting spores are especially
common in neritic marine centric diatoms (Chaetoceros,
Stephanopyxis (Ehrenberg) Ehrenberg, Detonula F. Schütt
ex De Toni: von Stosch 1967), but are also known to occur in
some freshwater centrics (Aulacoseira Thwaites, Urosolenia Round & Crawford, Acanthoceras Honigmann: Edlund
& Stoermer 1993, 1997, Edlund et al. 1996) and have been
reported in a few pennate taxa including Eunotia soleirolii
(Kützing) Rabenhorst (von Stosch & Fecher 1979) and
Craticula cuspidata (Kützing) D.G. Mann (Schmid 1979).
Spores are morphologically differentiated from vegetative cells and often have heavily silicified cell walls with
modified morphology. Spores have recognizable and often
differing epi- and hypospore valves, rarely with girdle elements. Resting spores are thought to provide a measure of
dormancy or grazing resistance (von Stosch & Fecher 1979,
Hargraves & French 1983, Itakura et al. 1999), require special conditions to germinate (von Stosch & Fecher 1979)
and are rarely produced within the sexual auxospore, e.g.,
Leptocylindricus danicus (Fig. 24; French & Hargraves
1985) and Cerataulina pelagica (Cleve) Hendey (Saunders
1968).
Because true auxospores rarely function as resting
stages, the term auxospore is an unfortunate misnomer, in
that it is not a resistant dispersal unit or a dormant stage as
is the case in some other algae. The term auxospore became
accepted before the function of auxospores was understood
and is too well established now to change it.
The types of resting spores listed below and illustrated
in Fig. 36 are modified from von Stosch (1967), Syvertsen
(1979) and Round et al. (1990), and they reflect only the
relationship between the mature spore and the spore parent cell and not always the ontogeny of spore production
(see von Stosch 1967 and references therein). Some species
are known to produce several spore types (e.g., Thalassiosira nordenskioeldii Cleve: Round et al. 1990, fig. 43).
10.1.1. Exogenous resting spores: groups of two or four
mature resting spores, produced by normal mitoses, that
Fig. 36. Resting spore types and their genesis. Thick-walled
spore types are determined by their relation to the spore parent cell and compared with the products of normal vegetative
reproduction. Top to bottom: a vegetative cell undergoing normal vegetative divisions and resulting progeny; production of two
exogenous resting spores; two semi-endogenous spores are each
partially enclosed by a parental theca and a residual cell with a
vestigial valve; a single endogenous resting spore surrounded by
the parental frustule and two residual cells with vestigial valves,
adapted after Round et al. (1990) with the permission of Cambridge University Press, and based in part on Thalassiosira, after
Syvertsen (1979) with the permission of Schweizerbart Science
Publishers (www.schweizerbart.de).
are not enclosed in the parent frustule (e.g., Detonula confervacea (Cleve) Gran, Thalassiosira nordenskioeldii,
T. antarctica Comber: von Stosch 1967, Syvertsen 1979).
10.1.2. Endogenous resting spores: a single or pair of
mature resting spores whose epi- and hypovalves are produced by unequal or acytokinetic mitoses; spores remain
completely enclosed in the parent frustule (e.g., Chaetoceros socialis Lauder, Urosolenia eriensis (H.L. Smith)
Round & Crawford, Acanthoceras zachariasii (Brun)
Simonsen, Aulacoseira skvortzowii M.B. Edlund, E.F. Stoermer & C.M. Taylor: von Stosch 1967, Syvertsen 1979,
Edlund & Stoermer 1993, Edlund et al. 1996, McQuoid &
Hobson 1996).
10.1.3. Semi-endogenous resting spores: mature spore
hypovalves of a spore pair remain enclosed in half of the
parent frustule, with the spore epivalve exposed to the
environment. Spore hypovalves are produced by unequal or
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
287
Fig. 37. A chain of vegetative (upper) and resting (lower) Aulacoseira cells illustrating the difference between protoplast organizations
in the two cell types. MBE, original.
acytokinetic mitoses (e.g., Stephanopyxis turris (Greville)
Ralfs, Ditylum brightwelli, Aulacoseira italica (Ehrenberg)
Simonsen: von Stosch 1967, Edlund et al. 1996).
10.2. Resting cells are physiologically and cytologically
modified cells characterized by metabolic/photosynthetic
dormancy and a centrally condensed protoplast (Fig. 37),
usually with unmodified or only slightly modified valve
morphology (e.g., thicker valves in some Aulacoseira
species: Jewson et al. 2008). Resting cells function
as a perennation strategy and are especially common
among freshwater plankton including centric and araphid
taxa (Sicko-Goad et al. 1989, Jewson 1992). Heavily
silicified winter stages in Eucampia antarctica (Ehrenberg) A. Mann are metabolically active, as indicated by
their mitotic divisions in this and other species (Fryxell & Prasad 1990, von Quillfeldt 2001) and may represent yet another form of survival strategy (seasonal
stages).
Other terms often used especially (but not exclusively) in
relation to the vegetative phase of the life cycle
10.3. Acytokinetic mitosis: a mitotic nuclear division that
is not followed by complete cell division or cytokinesis; each acytokinetic mitosis is followed by the production of only one valve following vegetative enlargement
(Fig. 2) or internal valve (Figs 38–39) or spore valve
(Fig. 36) production and degeneration of one of the two
nuclei, which becomes pyknotic. Acytokinetic mitoses
occur also during some gametogeneses (see section 4.5)
and precede production of initial epi- and hypovalves (see
section 3.4).
10.4. Unequal cytokinesis: a mitotic cell division that
unequally cleaves the mother cell to produce two diploid
sibling cells of unequal size. Unequal cytokineses are common in the production of resting spores (Fig. 36) and internal
valves (Figs 38–39). They also occur during gametogenesis,
e.g., at meiosis I in some diatoms (e.g., Cerataulus smithii,
Sellaphora: von Stosch 1956, Mann 1989b).
Fig. 38. Types of internal valve formation in Hantzschia
amphioxys (upper centre). Normal mitosis produces typical vegetative cells (upper right); two unequal mitoses produce a single
resting internal cell surrounded by heavily silicified internal valves
and enclosed between two residual cells with lightly silicified vestigial valves and small amounts of cytoplasm (upper left, lower
left); unequal mitosis may also result in a residual cell(s) with little
more than a nucleus and a parental valve (lower centre); an acytokinetic division results in a single internal spore containing both
resulting nuclei, one being pyknotic (lower right). MBE original,
adapted after Round et al. (1990) with the permission of Cambridge University Press, and Geitler (1980) with the permission
of Springer Publishing.
10.5. Internal valves are one or more morphologically
differentiated valves produced within vegetative cells following mitosis and unequal cytokineses or acytokinetic
288
Kaczmarska et al.
Fig. 40. Supernumerary valves in resting spores of
Melosira dickiei, showing normal vegetative valves (upper
left), while the lower left and the right frustule in surface view
illustrate resting spores with supernumerary valves, adapted after
van Heurck (1880–1885).
Fig. 39. Internal valve formation in Meridion circulare, cytology
following Geitler (1971). Vegetative valve (upper left); normal
mitotic cell division with resulting two vegetative cells (upper
right); the lower panel shows that the internal valve production in
Meridion involves first a mitosis to produce two acostate internal
valves, followed by an unequal mitosis that results in two internal cells surrounded by heavily silicified internal valves with a
small amount of cytoplasm segregated between two residual cells
each with a pyknotic nucleus and sometimes a vestigial valve (not
shown). MBE, original.
mitoses (Figs 38–39). Internal valves may serve as structures resistant to osmotic stress or desiccation and are often
more thickly silicified and have modified ornamentation
compared with vegetative valves. Cells encased in such
internal valves may be considered endogeneous resting
spores if they act as dormancy stages and require special
conditions to germinate (von Stosch & Fecher 1979, Round
et al. 1990). Internal valves are known from many genera including Melosira (Houk et al. 2010), Eunotia (von
Stosch & Fecher 1979), Fragilariforma D.M. Williams &
Round (M. Edlund, unpubl.), Meridion C. Agardh (Geitler
1971, Kingston 2003; Fig. 39), Achnanthes (Geitler 1980),
Entomoneis Ehrenberg (as Amphiprora: Geitler 1970),
Gomphonema (Kociolek & Stoermer 1991), Hantzschia
Grunow (Geitler 1980) and Pinnularia (Edlund & Stoermer
1997).
10.6. Supernumerary valves are structures known from
a few species producing multiple series of internal
valves, which are termed supernumerary valves, e.g.,
Melosira dickiei (Thwaites) Kützing (Houk et al. 2010;
Fig. 40) and Eunotia serpentina Ehrenberg (Hustedt
1927–1966). Supernumerary valves are not associated with
sexual reproduction and are thought to be produced within
the original vegetative frustule following multiple acytokinetic divisions.
10.7. The craticular plate (= craticular valve, craticula)
is an endogenously produced ‘roughly structured silica
scaffold’ (Schmid 1979) that lies internal to a normally
structured valve and seems usually to be produced in
response to osmotic stress. In the genus Craticula, the
craticular valve may in turn be external to a third type
of modified valve, the ‘heribaudii’ valve. The valves and
craticular plate (Fig. 41) together likely provide a measure
of protection from desiccation (Schmid 1979). The craticula
and ‘heribaudii’ valves are morphologically very different
from most internal valves and from the post-sexual initial
valves produced within an auxospore.
10.8. Abrupt (or rapid) size reduction is a sudden
decrease in valve size following (usually) a series of
asymmetrical mitotic divisions (with non-planar or oblique
cleavage) to produce significantly smaller cell lines, as in
the araphid pennates Asterionella Hassall, Ulnaria (Kützing) P. Compère [= Synedra] and Tabularia (Nipkow 1927,
Locker 1950, Roessler 1988, Kling 1993, Davidovich et al.
2010; Fig. 42), and in the raphid pennate Pseudo-nitzschia
(Chepurnov et al. 2005). This process may be adaptive in
bringing cells more rapidly into the inducible size range for
sexual reproduction or conferring an advantage in nutrient
uptake (Kling 1993), because of the change in the surface
area:volume ratio, and is probably more common than the
few reports suggest.
Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages
289
Fig. 41. Valve types and craticular plates within a resting spore of Craticula cuspidata. Left to right: vegetative valve; craticula or craticular
plate; ‘heribaudii’ valve (recognized as ‘var. heribaudii’ in older classifications); a complete resting spore encased in an envelope of sand
and detritus cemented by dried jelly-like compounds, illustrating the spatial relationship among the spore components. MBE, original; the
drawing on the extreme right is redrawn after Schmid (1979) with the permission of Springer Publishing.
major lineages of diatoms, such as the Rhaphoneidaceae–
Plagiogrammaceae–Asterionellopsis clade (Medlin et al.
2008, Ashworth et al. 2012). Further, with a few rare
exceptions (e.g., Sellaphora), very few species have been
systematically investigated over the duration of their sex life
and mated with a wide enough range of partners to consider
observed behaviours constant and sex linked. We are also,
only now, just beginning to learn how many loci may be
involved in sex determination in diatoms (Vanstechelman
et al. 2013), or what conditions modulate their expression
[cell-life stage (Armbrust & Galindo 2001), type of mate
or environment, etc.]. Therefore, we emphasize that the
current proposals will almost certainly be expanded and
amplified as new discoveries add to a better understanding
of the fascinating field of diatom reproductive biology. The
goal of this proposal is to help to generate more interest
in this field and to facilitate communication of these new
findings.
Fig. 42. Multiple size-classes of cells in a single colony of
Ulnaria ulna following two instances of mitotic abrupt size reduction. MBE, original based on Roessler (1988) with the permission
of Allen Press Publishing Services.
11. Concluding remarks
In closing, we wish to point out that although great progress
has been made since the 1980s, our understanding of
diatom life cycles is still meagre and patchy. For example, to date, there are no reports of auxosporulation in some
Acknowledgements
The authors are grateful to Oriha Ishii (Tokyo University for
Marine Science and Technology) for allowing us access to her
poster presented at the 20th International Diatom Symposium and
for sharing her unpublished observations. We thank K. Sabbe
and two anonymous reviewers for many helpful formative comments. J.M. Ehrman provided computer graphics expertise for
some figures but the majority were drawn by T. Watanabe. This
work was supported by project 206/08/0389 of the Grant Agency
of the Czech Republic and by project PrF/2013/003 of the
Internal Grant Agency of the Palacký University to AP and a
Postdoctoral Fellowship for Research Abroad from the Japan
Society for the Promotion of Science to SS Funding for MBE
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Kaczmarska et al.
was provided in part by the National Science Foundation (DEB0919095, 0743364); any opinions, findings, and conclusions or
recommendations expressed are those of the authors and do not
necessarily reflect the views of the NSF. Funding for IK was provided by a Natural Sciences and Engineering Research Council of
Canada (NSERC) Discovery Grant.
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