Hydrobiologia 269/270 : 11-20, 1993 .
H . van Dam (ed.), Twelfth International Diatom Symposium .
© 1993 Kluwer Academic Publishers. Printed in Belgium .
11
Patterns of sexual reproduction in diatoms
D . G . Mann
Royal Botanic Garden, Edinburgh EH3 SLR, United Kingdom
Key words :
auxosporulation, evolution, sexual reproduction, taxonomic characters
Abstract
Sexual reproduction takes many forms within the diatoms . The variation has been classified by several
authors, but in most cases the distinctions between their main categories have depended on the number of gametes produced per gametangium (and thus on how many zygotes per pair of copulating cells),
and upon whether fusion is oogamous, anisogamous or isogamous . These classifications are not themselves an adequate basis for taxonomic comparison, which should be based on individual characteristics of the sexual process . Diatoms seem to be primitively oogamous . In araphid pennate diatoms and
some raphid diatoms the gametes and gametangia are morphologically alike but physiologically distinct ;
one gametangium produces active gametes and the other passive ones . This may be the primitive condition in pennate diatoms, providing a link to the oogamy of centrics via the morphological anisogamy
of Rhabdonema Kiitz .
Introduction
Diatoms are almost unique among algae in having a diplontic life cycle, the only other confirmed
example being Vaucheria D .C ., within the Xanthophyta (Al-Kubaisi & Schwantes, 1981) . The
basic plan of the life cycle, involving size reduction followed by auxosporulation, is common to
most diatoms. However, while the basic plan is
constant, the details are not . There is immense
variation in sexual reproduction and zygote development, and this is a rich source of taxonomic
characters (Mann, 1990a) . Thus Hasle et al.
(1983) stated that the formation of flagellate
sperm by members of the Cymatosiraceae was
one of the principal reasons for regarding them as
centric, rather than pennate diatoms . In addition,
recent revisions of raphid genera have been based
in part on sexual reproduction and auxospore
development (e .g . Mann, 1989, 1990b ; Mann &
Stickle, 1989, 1991, 1993) .
No complete review of auxosporulation in centric diatoms is available, but several tens of species have been studied in some detail (see Drebes,
1977). All are oogamous or have abandoned allogamy for automixis or apomixis . Within pennate diatoms there is much more variety and auxosporulation has been described, in varying
degrees of detail, from over 160 species (Geitler,
1936, 1973, 1984 ; Mann unpublished survey) .
Even by 1932, Geitler was able to list over 90
records and it had become important to have a
classification of the different types of auxosporulation in pennate diatoms, to facilitate comparison and discussion . The classification most often
used today (see Geitler, 1973 ; Round et al ., 1990)
is based on one developed by Hustedt (1930b),
who established four main categories, based on
12
the degree of reduction and simplification from
the "Normaltypus", which is clearly implied to be
the ancestral type ; in this two gametangia (mother
cells) copulate and produce two gametes apiece,
which then fuse to form two zygotes .
Here I discuss whether Hustedt's and other
classifications of auxosporulation types do identify the most important features of variation and
the extent to which they can be used in taxonomy .
The discussion is weighted towards pennate diatoms .
Historical review
The first attempt to classify patterns of auxosporulation, by Smith (1856), followed shortly
after the first descriptions of "conjugation" by
Thwaites (e .g. 1847), Griffith (1855), Carter
(1856) and Smith himself (1856) . He described
four types :
I . "two parent frustules and two sporangia [i .e .
auxospores] as the result of their conjugation"
II . "From the conjugation of two parent frustules . . . a single sporangium"
III . "The valves of a single frustule separate,
the contents ... increase in bulk, and finally
become condensed into a single sporangium"
IV. "From a single frustule . . . two sporangia
are produced" .
Klebahn (1896) distinguished five types of auxosporulation, again on the basis of the number of
vegetative cells (one or two) that participate in the
formation of the auxospores and the number of
auxospores (one or two) produced . Klebahn's
categories were :
I . "eine Mutterzelle bildet eine Auxospore"
II . "eine Mutterzelle bildet zwei Auxosporen"
III . "zwei Mutterzellen bilden zwei Auxosporen ... ohne Conjugation"
IV. "zwei Mutterzellen bilden eine Auxospore
durch Conjugation"
V . "die Tochterzellen zweier Mutterzellen
bilden durch Conjugation zwei Auxosporen ,
Of these, three were asexual (types I-III), while
types IV and V involved sexual fusion . Klebahn's
five types were listed by Hustedt (1930a, b),
though not in the original order and with an unexplained change to Klebahn's type III, making it
a sexual process .
A further scheme was presented by Karsten
(1898, 1899), who recognized four types, which
correspond to Klebahn's, except that Klebahn's
type III is not recognized (several of Klebahn's
examples having been shown to be sexual) and all
are reordered (Karsten's type I = Klebahn's type
II ; 11= III & V ; III = IV ; IV = I) . Finally, Mereschkowsky (1903) produced yet another scheme,
very similar to Klebahn's, but with types III and
V transposed . In these classifications the order of
the different types is significant, since each author
made a conscious attempt to reflect possible evolutionary or biological trends .
The muddle created by Klebahn, Karsten and
Mereschkowsky was caused principally by erroneous interpretations of auxosporulation in centric diatoms and Rhabdonema . Thus, for instance,
between 1896 and 1904 small flagellate
"microspores" were observed in Coscinodiscus
Ehrenb ., Chaetoceros Ehrenb . and Rhizosolenia
Ehrenb . (summary by Fritsch, 1935), but it was
not until 1950 that it was finally established that
these cells are spermatozoids and that centric
diatoms are oogamous (Von Stosch, 1950 ; Fig . 1) .
Previously, auxosporulation in centric diatoms
was considered to be asexual (type I in Klebahn's
system) and sexual reproduction, if present at all,
was thought to involve copulation of the microspores (e .g . Kniep, 1928). The occurrence of
meiosis during the formation of diatom gametes,
though suspected, was not conclusively established until 1912 (by Karsten) . By 1930, however,
enough information was available from cytological and life cycle studies to enable correct interpretation of auxosporulation in pennate diatoms,
and Hustedt (1930b) put forward a new scheme
for these, as follows :
"I . Normaltypus . Zwei Mutterzellen bilden
durch paarweise Kopulation zwei Auxosporen
(a) Gameten anisogam [referring to dissimilarities in gamete behaviour rather than
size] . . .
13
la
1b
2
10
O
v
Figs 1-10.
Patterns of sexual reproduction in diatoms . Fig. 1 . Oogamy, as in the centric diatom Lithodesmium. A . Oogonium
liberating two eggs (N .B . in many other centric diatoms only one egg cell is produced per oogonium) . B . Male gametogenesis :
spermatogonia undergoing meiosis to produce flagellate sperm . Fig . 2. Modified oogamy (morphological anisogamy) in Rhabdonema arcuatum . The female gametangium produces two immobile egg cells ; the male gametangium produces two amoeboid
"sperm" and a residual body. Figs 3-7 . Allogamous reproduction in pennate diatoms, illustrating Geitler's (1973) principal categories. Figs 3-5 . Two gametes produced per gametangium (type I) . Fig. 3 . Physiological anisogamy : one active gamete per gametangium (type IA1) . Fig. 4 . Physiological anisogamy : both active gametes produced by the same gametangium (type IA2) . Fig . 5 .
Isogamy (types IB & IC) . Figs 6, 7 . One gamete produced per gametangium (type II) . Fig . 6 . Anisogamy (type IIB) . Fig . 7 . Isogamy
(type IIA) . Figs 8, 9 . Automixis (type III) . Fig . 8 . Paedogamy (type IIIA) . Fig . 9 . Autogamy (type IIIB) . Fig. 10 . Apomixis (type
IV) .Stipple : motile gametes . Heavy stipple : functional haploid gametic nuclei. Black : degenerating, non-functional nuclei . Open
circle (Figs lb, 10) : unreduced diploid nucleus or meiotic nucleus .
14
(b) Gameten isogam . . .
II . Reduzierter Typus A . Aus zwei Mutterzellen entsteht durch Kopulation eine Auxospore
(a) Gameten anisogam [again, referring to dissimilarities in gamete behaviour] . . .
(b) Gameten isogam . . .
III . Reduzierter Typus B . Autogame Auxosporenbildung
(a) Automixis . Zwei in einer Mutterzelle
entstandene Gameten verschmelzen zu
einer Zygote [ = paedogamy sensu Geitler,
1932, 1973] . . .
(b) Autogamie . ..
IV. Reduzierter Typus C . Apogame Auxosporenbildung
(a) Aus einer Zelle entstehen zwei Zygoten . . .
(b) Aus je einer Zelle entsteht eine Zygote . . ."
Of these, only Type IVa (corresponding to
Klebahn's type II) is now redundant, having been
founded principally for Rhabdonema, where the
existence of small amoeboid gametes and oogamy
was then unknown (Von Stosch, 1958 ; Fig . 2) .
Hustedt's scheme was adopted with little change
by Geitler (1932), who subsequently subdivided
the main categories on the basis of gamete behaviour (e .g . whether there is rearrangement of
the gametes within the gametangium before plasmogamy), the presence of particular copulation
structures, pairing configurations, and the orientation of the expanding auxospores relative to the
gametangia (Geitler, 1973) .
Thus, from 1856 onwards, the principal basis
for classifying patterns of auxosporulation has
been the number of auxospores produced per
mother cell, which in turn is determined by
whether sexual fusion occurs and, if it does, by
the number of gametes produced per gametangium . Other characteristics, such as whether
sexual fusion is isogamous or anisogamous, have
been of secondary importance . Does this classification truly identify the most fundamental aspects of variation in auxosporulation? Some scientists have apparently assumed that it does . In
a cladistic and phenetic analysis of monoraphid
diatoms, Kociolek & Stoermer (1986) considered
sexual reproduction as a single character with
two states, corresponding to Geitler's (and hence
Hustedt's) types I and II ; this places the emphasis on the number of gametes produced per gametangium, rather than on any other aspects of
auxosporulation .
Evolution of auxosporulation patterns
Although there can be little hope of obtaining
direct evidence from fossils, some plausible conclusions can be reached about the evolution of
sexual behaviour . Primitive diatoms must have
had a flagellate stage in the life cycle, since extant
centric diatoms have flagellate sperm and it is
inconceivable that eukaryotic flagella have arisen
several times, through evolutionary convergence .
We cannot be certain that the flagellate stages of
primitive diatoms were gametes, but the fact that
flagella are found today only on sperm and that
flagellate sperm are produced by centric diatoms
as diverse as Melosira C .A . Ag ., Biddulphia S .F .
Gray, Chaetoceros, Rhizosolenia, and the Cymatosiraceae (Drebes, 1977 ; Hasle et al., 1983) is
strong circumstantial evidence that they were . For
similar reasons, it is likely that primitive diatoms
were oogamous diplonts, like present day centric
diatoms . This conclusion is consistent with the
earlier appearance of centric diatoms in the fossil record (Tappan, 1980).
If these conclusions are accepted, then further
suggestions can be made about the evolution of
sexual behaviour in diatoms . First, oogamy has
been replaced by morphological isogamy during
the evolution of the pennate diatoms, with the
loss of all traces of flagella (I regard the report of
Subba Rao et al., 1991 as non-proven : see Fryxell
et al., 1991 ; Rosowski et al ., 1992). This is a remarkable exception to the generally accepted rule
that isogamy is the primitive condition in eukaryotes, while oogamy has arisen many times polyphyletically (e .g . see Wiese et al ., 1979). However,
the morphological isogamy found in most pennate diatoms is quite unlike the isogamy of other
15
13
14
Figs 11-17. Camera lucida drawings of live cells . Scale bars= 20 µm (the left-hand bar refers to Figs 11-15) . Figs 11, 12 . Amphora cf. laevissima ; A & B show different focal planes, one for each gametangium . Fig . 11 . 11 .40 h : each gametangium contains
two gametes . Fig . 12 . 12 .30 h : the two gametes from the lower gametangium (B) have moved towards the gametes in the upper
gametangium (A) and fused with them, producing two zygotes, each with two chloroplasts . Figs 13-15 . Biremis sp . Figs 13, 14 .
Gametangia before (Fig. 13) and after (Fig. 14) rearrangement of the two gametes (in each figure the other gametangium of the
pair is not shown but lay beneath that illustrated) . Fig . 15 . Gametangial frustule (forced apart) and expanding auxospore ; siliceous
caps (e .g . arrow) cover the ends of the auxospore. Figs 16, 17 . Neidium ampliatum . Fig . 16 . Gametangium (the other member of
the pair lay beneath that illustrated) containing two rearranged gametes . Fig. 17 . Gametangial frustule (forced apart) and fully
expanded auxospore, containing the young epivalve (right) ; siliceous caps cover the ends of the auxospore (e .g . arrow).
algae . There the gametes are small and highly
mobile ; in pennate diatoms, they are at least half
the size of the vegetative cells and, although the
gametes retain some limited power of autonomous movement, it is the gametangia that copulate . The gametangia are brought together, either
through passive transport of the gametangia (as
in Synedra Ehrenb . or Licmophora C.A . Ag . : Geitler, 1939a, b; Mann, 1982), or through active
movement (as in raphid diatoms) . Recent analyses of the adaptive significance of isogamy,
anisogamy and oogamy (e .g . Cox & Sethian,
1984, 1985), which suggest that isogamy should
be associated with small gametes and zygotes,
16
apply where the gametes are released and are
alone responsible for effecting copulation and
sexual fusion . In pennate diatoms, and also in
desmids, it is the gametangia, not the gametes,
that initially copulate . Here variation in gamete
behaviour (physiological anisogamy versus
isogamy) is unlikely to have the same significance
as in algae where the gametes are released . Furthermore, in diatoms where the gametangia copulate, flagella are probably made redundant by the
short distance the gametes have to travel to effect
fertilization .
Given that it is the gametangia rather than the
gametes that copulate, there is no longer any advantage in producing any more gametes per copulating pair of gametangia than are necessary to
produce the final number of zygotes, nor any advantage in morphological anisogamy (Cox & Sethian, 1984, 1985) . In turn, given a set initial
amount of cytoplasm (containing organelles, reserve material, etc) derived from the gametangia,
the number of zygotes produced will reflect a selective trade-off between numbers and size . The
number of zygotes obviously limits the number of
potential offspring, while zygote size is likely to be
highly correlated with the fitness of the offspring
- especially since the first phase of zygote development is not vegetative growth and division but
a massive expansion in volume, accompanied by
the formation of a silicified perizonium, considerable rearrangement of cell organelles and cytoskeleton, two successive acytokinetic mitoses,
and the synthesis of a complete new frustule .
The critical question to be answered, therefore,
concerning the change in sexual behaviour between the centric and pennate diatoms, is not why
oogamy gave way to morphological isogamy but
why there was a transfer of function (Corner,
1958) from gametes to gametangia, so that the
gametangia became responsible for copulation .
Although raphid diatoms (and also some araphid
and centric diatoms : Pickett-Heaps et al., 1991)
are motile, this does not in itself explain why
copulation has become a function of the gametangia and why all diatoms do not produce eggs
and flagellate sperm . A partial explanation may
be as follows:
In the benthic habitats where most pennate
diatoms occur, cell densities are often high and
sexualized diploid cells will encounter each other
more frequently than would usually occur in the
plankton, either through chance contact following
passive transport by water currents or through
active movement . For sexualized cells that find a
mate, wastage of gametes is clearly minimal . If
sexualized cells of pennate diatoms are not irreversibly committed to meiosis (and my unpublished observations show that cells that have
paired do sometimes revert to the vegetative
state), cells that fail to find a mate could abandon
development as gametangia and resume vegetative growth, giving them another chance to complete sexual reproduction successfully, when inductive conditions recur . In centric diatoms, there
is no opportunity for reversion, since the cells that
copulate or fail to copulate are already fully committed: they have undergone meiosis and are haploid .
An alternative explanation is given by PickettHeaps et al. (1990), who suggest that the switch
to the production of amoeboid gametes within a
mucilage envelope reflects adaptation to a terrestrial environment .
The taxonomic significance of auxosporulation
patterns in pennate diatoms
The above discussion provides a necessary background for considering whether the Hustedtian
classification of auxosporulation patterns in pennate diatoms, as modified by Geitler, identifies
the most important characteristics of auxosporulation and ranks them correctly in a hierarchy .
First, consider the primary division made by
Hustedt, based on the degree of reduction from
the "Normaltypus" (type I), in which two copulating gametangia produce two zygotes . It seems
very likely that type I (Figs 3-5) is indeed the
primitive state for pennate diatoms, because it
involves both meiosis and sex, which must be
primitive in diatoms (since they are common to
most groups of eukaryotes), and because it is ontogenetically simpler than type II auxosporulation
17
(Figs 6-7), where more meiotic products are destroyed in each gametangium . Type II is then a
reduced form, in which increased fitness of the
zygotes must compensate for the halved number
of offspring . Types III (Figs 8-9) and IV (Fig . 10)
represent abandonment of sex in favour of automixis (type III), where lines will be completely
inbred, or apomixis (Type IV) . A further type of
behaviour exists, in which auxospores are never
formed and sexual reproduction never occurs, because the diatom avoids size reduction ; examples
include Caloneis amphisbaena (Bory) Cleve
(Mann, in preparation) and probably some populations of Craticula ambigua (Ehrenb .) D .G.
Mann (Mann, 1988 ; Mann & Stickle, 1991) .
However, the four types do not represent a
simple evolutionary progression . For instance,
paedogamy - fusion of sister gametes within a
single gametangium (Fig . 8 ; Geitler's type IIIA) is less likely to be derived from type II allogamy
than from type I . For derivation from type I, the
only change required is a breakdown of the self
incompatibility mechanism that prevents the two
gametes of a single gametangium from fusing
(usually accompanied by loss of pairing between
gametangia : Geitler, 1973) . Thus it is not surprising that the examples of paedogamy listed by Geitler (1973, 1979) - two Gomphonema angustatum
(Kiltz .) Rabenh. races, G . constrictum var. capitatum (Ehrenb .) Cleve, Cymbella aspera (Ehrenb .)
Cleve, Amphora "normani-veneta ", Epithemia turgida (Ehrenb .) Kdtz . and Nitzschia `frustulum var.
perpusilla" - are all closely related to species
within the same genus that exhibit type I auxosporulation .
For diatoms with type II auxosporulation a
change to any form of automixis is more complex,
involving not only a breakdown of self incompatibility mechanisms but also the survival of an extra
haploid nucleus, which had previously been destroyed . Nevertheless, it can happen . In the Sellaphoraceae (sensu Round et al., 1990), a series can
be traced from type IA auxosporulation (Fig . 3)
in Fallacia Stickle & D .G . Mann, to type IIB
(Fig . 6) in most Sellaphora Mereschk ., to type III
(probably IIIB) in one deme of S. pupula (Kiitz .)
Mereschk . (Mann, in preparation) .
Thus, although Hustedt's four main categories
do reflect important evolutionary changes, the
variation pattern indicates that these changes
have occurred several times quite independently,
and that some changes are probably easier than
others .
Next, consider the second most important criterion in the Hustedt-Geitler system : whether
sexual fusion is isogamous or anisogamous . The
anisogamy here is not a matter of size - except
in Rhabdonema and Grammatophora Ehrenb . but a difference in the behaviour of the fusing
gametes, one remaining still while the other moves
to effect plasmogamy. Among type I diatoms with
anisogamy there are two main variants . In the
first (Geitler's type IA1 ; Fig. 3), each gametangium produces an active gamete and a passive
one ; this type is widespread, occurring, for instance in species of Gomphonema Ehrenb ., Cymbella C.A. Ag., Achnanthidium Kiitz ., Frustulia
Rabenh ., Nitzschia Hass . and Lyrella Karayeva
(Geitler, 1973 ; Mann, 1986 ; Mann & Stickle,
1993). In the second (Geitler's type IA2 ; Fig . 4),
one gametangia produces both of the active gametes and the other both of the passive gametes .
A priori, type IA2 might be expected to be
primitive in pennate diatoms, since the gametangia are differentiated into "male" (i .e . producing
the active "male" gametes) and "female", as in
centric diatoms (Figs 1, 4) . The araphid pennate
genera Rhabdonema and Grammatophora (Von
Stosch, 1958 ; Magne-Simon, 1960, 1962) exhibit
what appears to be an even more primitive type,
in which the gametes differ in size as well as behaviour, the active, amoeboid males being smaller
than the passive females (Fig . 2) ; this behaviour
seems to be transitional between type IA2 and the
oogamy of centric diatoms . The pattern of variation supports the idea that type IA2 is primitive,
since it is found in several araphid pennate genera (Diatoma Bory, Licmophora, Synedra : Geitler,
1973 ; Mann, 1982), while other forms of type I
allogamous auxosporulation are restricted to
raphid diatoms (a possible exception is Meridion
C.A. Ag . : Geitler, 1973) . This suggestion assumes, of course, that raphid pennate diatoms
have been derived from araphid pennate ances-
18
tors, which seems reasonable given the occurrence in both of gametangial pairing and a sternum as the pattern centre, and the ontogeny of
the raphe system, which suggests derivation from
an araphid state (Mann, 1984a) .
Did ancestral raphid diatoms also have type
IA2 auxosporulation? The evidence is ambiguous . Geitler (1973) lists Craticula (=Navicula)
halophila (Grun .) D .G. Mann as having type IA2
auxosporulation, based on Subrahmanyan
(1947) . However, though admirable in most respects, Subrahmanyan's report is unconvincing
about the occurrence of behavioural anisogamy .
Fusion seems in fact to be isogamous, as in Craticula cuspidata (Ki tz .) D .G. Mann (Stickle,
1986 ; Mann & Stickle, 1991) . Clear examples of
type IA2 auxosporulation are found in Mastogloia
smithii Thwaites (Stickle, 1986) and M. binotata
(Grun .) Cleve (reinterpretation of Buffham's 1892
illustrations), and also some species of Amphora
Ehrenb . (Figs 11, 12) . At present it is impossible
to judge whether these represent rare survivals of
a primitive trait or convergent evolution . Even so,
the variation pattern suggests that the difference
between type IA1 and IA2 auxosporulation is at
least as important as that between IA and IB .
Furthermore, during evolutionary reduction to
type II auxosporulation, where only one gamete
is produced per gametangium, type IA1 could
give rise to IIA or IIB, depending upon which
gametes are suppressed : if to IIB, it would be
indistinguishable from reduced IA2 ; if to IIA, it
would be indistinguishable from reduced IB (see
Figs 3-7) .
Thus, there is no clear evidence that Hustedt's
hierarchical classification of the different types of
auxosporulation does identify and correctly rank
the most important features of variation . For
taxonomic purposes, therefore, each aspect of
auxosporulation should be assessed independently, alongside cell wall, protoplast or other
characters . To use Hustedt's or Geitler's categories as a basis for taxonomic analysis is dangerous .
To illustrate this, consider Neidium Pfitzer and
Biremis D .G . Mann & E.J . Cox . Auxosporulation in Neidium was described in detail by Mann
(1984b), while Biremis will be covered in a forthcoming article (Mann, in preparation) ; representative stages are shown in Figs 13-17 . Both genera exhibit type IAl auxosporulation (Fig . 3) .
Thus, if one were to assess auxosporulation characteristics in the same way as Kociolek & Stoermer (1986), Neidium and Biremis would be
scored simply as "type I" ; hence they would be
recorded as differing from e .g . Cocconeis Ehrenb .
(since this has type II auxosporulation ; Geitler
1973) but not from Mastogloia Thwaites, even
though Mastogloia has the unusual and perhaps
primitive characteristic that both active gametes
are produced by the same gametangium (Fig . 4) .
Closer analysis reveals that Neidium and Biremis
share the following character states : gametangia
not obviously differentiated into donor and recipient; mucilage capsule around gametangia diffuse ; gametangia remaining closely associated
throughout gamete formation and plasmogamy ;
two gametes produced per gametangium (Figs 13,
14, 16) ; gametes becoming rearranged within each
gametangium after formation, to lie one on either
side of the median transapical plane (Figs 13, 14) ;
one passive and one active gamete produced per
gametangium ; mature zygotes ellipsoidal ; auxospore expansion parallel to the apical axes of the
gametangia (Figs 15, 17) ; auxospore poles with
siliceous caps (Figs 15, 17 ; not yet reported from
any other diatoms) ; primary transverse perizonial
band little broader than the other transverse
bands . Many of these character states are found
in several or many other groups of raphid diatoms
but none is universal . In any wide-ranging cladistic or phenetic analysis of raphid diatoms, failure
to treat these features as separate characters will
bias the outcome of parsimony analysis (cladistics) or clustering (phenetics) . Classifications of
auxosporulation patterns have great value in facilitating discussion, but should not be used as a
basis for taxonomy .
Acknowledgements
This work was supported by SERC GR/C/68484
and the Royal Society . Thank you too to Jeremy
19
Pickett-Heaps, Stephen Droop, my wife and an
anonymous referee for comments on the manuscript .
ichs and der Schweiz . In Dr L . Rabenhorsts KryptogamenFlora von Deutschland, Osterreich and der Schweiz, 7 (1) .
Akademische Verlagsgesellschaft, Leipzig . 921 pp .
Hustedt, F ., 1930b . Bacillariophyta (Diatomeae) . In A . Pascher (ed .) Die Si sswasser-Flora Mitteleuropas, 10, 2nd
edn . G . Fischer, Jena . 466 pp .
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