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Rivulariaceae

Chapter · January 2012

DOI: 10.13140/2.1.2976.3361

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 Rivulariaceae
22
Brian A. Whitton and Pilar Mateo

Contents 22.7 Geological Record and Environmental Change ............ 584

Summary...................................................................................... 561 22.8 Discussion .......................................................................... 585
22.1 Introduction ................................................................ 562 References .................................................................................... 586
22.2 Morphology................................................................. 562
22.2.1 Morphology and Classical Taxonomy ......................... 562
22.2.2 Range of Form ............................................................. 563
22.2.2.1 Tapering and Hairs ....................................................... 563 Summary
22.2.2.2 Heterocyst .................................................................... 564
22.2.2.3 Hormogonia ................................................................. 565 The Rivulariaceae are treated here as all the cyanobacteria
22.2.2.4 Akinete ......................................................................... 566
which have trichomes with a marked taper and a basal
22.2.2.5 Colony, Trichomes and Sheath..................................... 567
heterocyst for much of their growth cycle. Molecular
22.3 Molecular Perspective on Taxonomy........................ 568 sequencing of Calothrix and Rivularia shows that these are
22.3.1 Status of Classical Genera............................................ 568
22.3.2 Molecular Diversity Within Form-Genera ................... 569 heterogeneous and this probably also applies to Dichothrix
and Gloeotrichia. The unispecific Isactis has received little
22.4 Physiology ................................................................... 570
study, but is morphologically close to some Calothrix. These
22.4.1 Carbon and Nitrogen .................................................... 570
22.4.2 Phosphorus ................................................................... 571 should all be treated as form-genera for ecological descrip-
22.4.3 Molecules with Possible Ecological Effects ................ 574 tive purposes until more sequencing studies have been made.
22.5 Overview of the Genera ............................................. 574 Sacconema and Gardnerula are not considered distinct
22.5.1 Introduction .................................................................. 574 enough to be treated as distinct genera. Colony formation
22.5.2 Calothrix ...................................................................... 575 occurs by aggregation of hormogonia and this may lead to
22.5.3 Rivularia, Dichothrix and Isactis ................................. 576 the inclusion of more than one genotype.
22.5.4 Gloeotrichia ................................................................. 578
The group as a whole occurs in environments with
22.6 Interactions with Other Organisms.......................... 581 highly variable P concentrations, usually short periods of
22.6.1 Free-Living Phototrophs .............................................. 581
22.6.2 Symbiotic Associations ................................................ 582
relatively high ambient P followed by much longer periods
22.6.3 Animals ........................................................................ 582 of low P; a few possible exceptions are discussed. Typically
22.6.3.1 Introduction .................................................................. 582 organic P exceeds inorganic P and the Rivulariaceae as a
22.6.3.2 Destruction of Whole Filaments .................................. 583 whole are especially efficient at using organic phosphates.
22.6.3.3 Partial Destruction of Filaments .................................. 583
22.6.3.4 Avoiding the Grazers.................................................... 583
N2 fixation in Rivulariaceae is highest during the period
22.6.4 Bacteria and Fungi ....................................................... 584 of high P. In the case of Gloeotrichia echinulata, which
sometimes forms blooms in lakes, P acquisition takes place
mainly while the organism is growing near the sediments.
Its competitive success is favoured by a combination of
B.A. Whitton (*) P-rich sediments and relatively low P concentrations in
School of Biological and Biomedical Sciences, Durham University, the water.
Durham DH1 3LE, UK
Long colourless multicellular hairs are formed by many
e-mail: [email protected]
species, including all those with distinct hemispherical and
P. Mateo
spherical colonies. The hairs not only enhance the surface
Departamento de Biologia, Facultad de Ciencias,
Universidad Autonoma de Madrid, 28049 Madrid, Spain area for phosphatase activities, but also aid P acquisition
e-mail: [email protected] from environments where the ambient P concentration is

B.A. Whitton (ed.), Ecology of Cyanobacteria II: Their Diversity in Space and Time, 561
DOI 10.1007/978-94-007-3855-3_22, © Springer Science+Business Media B.V. 2012
562 B.A. Whitton and P. Mateo

mostly low, but with occasional much higher pulses. Although

most phosphatase activities take place at the cell surface,
some activity often occurs in sheaths and probably also
inside the cytoplasmic membrane of older hair cells, sug-
gesting that organic phosphates can sometimes pass through
the membrane.
Sufficient is known about the relationship between
morphology and the environment in the Rivulariaceae to
make them excellent environmental indicators. Many of
the morphological characters used for classical taxonomic
descriptions are expressed only when the organisms are
P-limited, but some culture collections and many experi-
mental studies have used media with very high P concen-
trations, making past interpretation of results doubtful, if
not wrong.
Fig. 22.1 Young planktonic colonies of Gloeotrichia echinulata
(Photo P.V. York, with permission)

22.1 Introduction

A number of general accounts of blue-green algae in the 22.2 Morphology

nineteenth century grouped genera with obviously tapered
trichomes into the family Rivulariaceae, with Rivularia 22.2.1 Morphology and Classical Taxonomy
haematites the type species. Geitler (1932) summarized the
earlier information, while Desikachary (1959) provided a The most widely accepted heterocystous genera of Rivula-
succinct definition; “Trichomes with a single row of cells, riaceae in classical floras (i.e. those based on International
apices generally attenuated or tapering in hair, unbranched or Code of Botanical Nomenclature) have trichomes with a
false-branched, sometimes with a distinct intercalary meri- basal heterocyst, a distinct taper to the trichome and a
stematic zone and trichothallic growth; hair with elongated sheath enclosing everything but the heterocyst. Calothrix
more or less vacuolated cells; heterocysts present or absent, includes all the forms growing as individual filaments or
when present basal, intercalary heterocysts also present in ill-defined colonies. Four genera form distinct colonies,
some; hormogonia present, akinetes present or absent, when with Gloeotrichia separated by its ability to form akinetes.
present single or in series”. The 12 genera listed by Geitler The others are distinguished by colony morphology, which is
and Desikachary included several without heterocysts such determined by the pattern formed by hormogonia when they
as Homoeothrix, but, even before molecular data started to first aggregate and also by the division pattern during colony
make it possible to assess relationships more critically, most growth. Rivularia colonies have more or less parallel sheathed
researchers assumed that non-heterocystous species were trichomes inside hemispherical, subspherical or spherical
different. colonies; the trichomes often have false branches. Isactis
The heterocystous Rivulariaceae include organisms found forms spreading colonies in the marine intertidal, with sparsely
widely in nature and are in some cases visually conspicuous. branched trichomes perpendicular to underlying rock
Perhaps the best known is the planktonic Gloeotrichia surface. Dichothrix forms small colonies of various shapes,
echinulata (Sect. 22.5.4; Fig. 22.1), which can form blooms, mostly cushions or dense tufts; trichome branching is con-
but other species of Gloeotrichia, Dichothrix and Rivularia spicuous and there are often many trichomes inside one
form conspicuous attached or floating colonies in shallow sheath. Many, but not all, freshwater Dichothrix and
waters (Sect. 22.5.3). This chapter tries to establish to Rivularia become partially calcified (Fig. 22.2).
what extent the heterocystous Rivulariaceae are a uniform The distinctions between genera are not always clear-cut,
group phylogenetically and ecologically. At the same time it such as between Dichothrix and Rivularia, but the names
sets out to explain how phenotypic differences influence the still prove useful in floristic accounts of natural communities.
success of a particular genus or species, and conversely, However, Rippka et al. (1979) included all heterocystous
the extent to which one can interpret the environmental cyanobacteria with a low or high degree of tapering in
features of a site from the morphology of its Rivulariaceae. Calothrix on the grounds that colony appearance in feral
The reader needs to know some of the older literature in samples seemed to be a doubtful taxonomic trait. Only a
order to understand the argument. brief justification for this statement was given and in any
22 Rivulariaceae 563

Fig. 22.2 (a, b) Dichothrix baueriana in River Caher, draining fluctuations in water level; (c) Rivularia colonies among developing
The Burren, Co. Clare, Ireland, June 2006: (a) Upstream view of calcareous crust on boulder in Loch Nam Bakgan, South Uist, Outer
calcified boulders; (b) close-up of the colonies during a period of low Hebrides (Scotland), September 2009; colonies up to 8 mm diameter,
flow; showing growth on the boulder in the zone influenced by recent with obvious calcification inside them (Photos B.A.W.)

case it is doubtful how many of the cultures had been in species where the trichome becomes much wider close to
observed closely when the organism was first sampled from the heterocyst, giving the appearance of a spindle-shaped
nature. Concern about the reliability of names in culture swelling (Schwenender 1894; Friedmann 1956).
collections using P-rich medium (Chap. 1) is especially Many species can form multicellular hairs, structures which
relevant to the Rivulariaceae due to the need for the organ- were defined by Sinclair and Whitton (1977a) as “a region of
isms to be at least moderately P-limited to express their the trichome where the cells are much narrower, elongated,
characteristic morphological features (Whitton 1987, 1989, highly vacuolated and usually apparently colourless”. This
2008, 2009; Berrendero et al. 2008; Sect. 22.4). Such con- definition fits the way the term is used for descriptive
cern extends to the names associated with sequence data purposes in most floras, including all but one of the species
deposited in GenBank. in Geitler (1932). However, other species occur with long
tapered structures which resemble hairs in outline, but the
cells retain their chlorophyll and do not elongate; these
22.2.2 Range of Form are quite common, at least in the subtropics. An example,
Calothrix D764, is discussed in Sect. 25.2.2. The only
22.2.2.1 Tapering and Hairs exception in Geitler (1932), C. kossinskajae, is somewhat
The tapered trichome has a terminal heterocyst at the wider like this, but the figures show a scarcely tapered trichome
end and growth is often localized in a region near, but not which contracts over one or two cells to a very long exten-
immediately adjacent, to the heterocyst. Although the term sion of the main trichome, but only about one-third of its
‘meristematic’ is often used in descriptions of Rivulariaceae width. If (as seems likely) this gives rise to hormogonia, they
to indicate this region, its position and the extent to which it would be little more than 1 mm wide.
is localized varies during growth. It is suggested that the All the descriptions of species in the genera forming
region corresponds to where longitudinal gradients of N and distinct colonies show hairs. In the case of Calothrix, 56 out
P in the trichome (see below) interact at any one time to pro- of the 78 species (72%) reported in the taxonomic literature
vide optimum growth conditions. The region is most distinct surveyed by Kirkby and Whitton (1976) formed hairs, while
564 B.A. Whitton and P. Mateo

82 of 103 (81%, omitting a few uncertain species) did so in Multicellular hairs which appear morphologically similar
the names in CyanoDB.cz (July 2011). However, only 7 out also occur in at least some species of most genera of
of 29 Calothrix strains (24%) in culture did so, in spite of Stigonematales, the similarity being especially marked in
being tested under a range of environmental conditions Nostochopsis and Brachytrichia. The ends of the trichomes
known to lead to hair formation (Sinclair and Whitton 1977a). of Aphanizomenon flos-aquae often taper into short hair-
This raises the possibility that isolation procedures may like lengths, while several species of the non-heterocystous
be selecting against hair-forming strains. The hair cells of Homoeothrix and Ammatoidea also form hairs. This indicates
Gloeotrichia echinulata mostly retain their gas vacuoles that multicellular hairs have evolved many times in cyanobac-
(Smith and Peat 1967). teria, just as they have in eukaryotic algae (Whitton 1988).
In the study by Sinclair and Whitton (1977a), P limitation
enhanced tapering in all 34 Rivulariaceae strains tested, 22.2.2.2 Heterocyst
but only 12 strains developed hairs. Even in the presence of Although all Rivulariaceae can form terminal heterocysts,
combined N, P-limitation still led to the formation of hairs in some also form intercalary ones. These have been observed
these strains (Sinclair and Whitton 1977b). Three strains in many species, but occur much more frequently in some
formed some hairs under P-rich conditions, although hair than others. Polarity of the terminal cell is established before
frequency increased with increasing P limitation (Sinclair the hormogonium is released from the mother trichome.
and Whitton 1977a). Much shorter hairs were formed under The heterocyst always develops in the cell adjacent to the
Fe deficiency in seven strains and under Mg deficiency in main trichome i.e. basal, even though the cell furthest from it
one strain, but there was no response to Ca, Mo or SO4 might be expected to be the most N-limited (Whitton 1987).
deficiencies. Strains lacking the ability to form hairs had all In contrast to the terminal heterocyst, an intercalary hetero-
been described as Calothrix in the culture collections from cyst has polar nodules (cyanophycin) on both sides, so
which they came. In addition to the uncertainty as to whether presumably fixed N can pass in both directions and thus
or not they possessed hairs when originally collected, there is permit further growth in both parts of the trichome.
also the possibility that they might have lost this ability dur- Particularly in Rivularia, a new heterocyst is sometimes
ing repeat subculture in a P-rich medium. However, when developed above the current one and the old one starts to
Gloeotrichia aff. pisum colonies with trichomes showing collapse, eventually showing with the light microscope little
obvious hairs were removed from deepwater rice plants in more than the wall. Typically the new heterocyst has only a
Bangladesh, all attempts to isolate trichomes able to form single polar nodule and thus becomes the terminal heterocyst.
hairs in culture failed (Aziz 1985). In addition to nutrient Growth of Calothrix parietina D184 (= PCC 7713) in medium
limitation, methods tested without success included chang- without Fe led to repeat formation of new single-pored
ing the light and temperature regimes, spectral composition heterocysts, with rapid degeneration of the old one (Douglas
of the light and incubation in various organic phosphates et al. 1986). The new heterocyst was often separated from
as the sole P source. It remains uncertain whether an impor- the old one by necridial cells. Several illustrations in the
tant factor was overlooked or whether the trichomes isolated literature suggest that the new heterocyst may in some cases
were not representive of the main colony. Similarly, during be intercalary, though this has never been observed by the
isolation of three Calothrix species from an Iraqi marsh authors; if it does occur, this might permit higher rates of N2
rice field, C. fusca and C. parietina both formed hairs fixation. Large Rivularia colonies, which have already grown
in enrichment culture, but, once they were brought into for several years, sometimes have as many as eight remnant
axenic culture, C. parietina failed to do so (Al-Mousawi and heterocysts beneath the normal terminal one. Presumably
Whitton 1983). each new heterocyst forms as a response to a change in envi-
Cultures grown under increasingly P-limited conditions ronmental conditions. One such possible response is a loss of
cease to produce hormogonia. The apical cells then start to the ability of the heterocyst to fix N2 under prolonged periods
develop intrathylakoidal vacuoles, which remain small in of high ambient combined N, resulting in the need for a
species which do not form hairs, but continue to increase in size new one to be formed the next time N2 fixation becomes
and lose their photosynthetic pigments in species forming important. All but one of 34 Rivulariaceae (representing all
hairs. Formation (where present) can continue for a long four genera) lost all heterocysts when cultured with 10 mM
period. The hair cells consist largely of vacuoles originating NaNO3 (Sinclair and Whitton 1977b). However, this concen-
from intrathylakoidal vacuoles and in very long hairs each tration of combined N is much higher than likely to occur in
cell is largely filled by a single vacuole. Rivularia and other most environments. No studies have yet been made on the
colonial forms with hairs which persist for many months effects of fluctuating concentrations of combined N supplied
usually have a long transition zone from typical vegetative at more realistic concentrations.
cell to cells with increasingly larger vacuoles and then to the Another possible response is the formation of a new
colourless hair cells (Wood 1984; Wood et al. 1986). heterocyst due to the deficiency of an element important in
22 Rivulariaceae 565

grown in the absence of combined N led to about 20%

heterocysts turning an obvious blue. In shaded forest habitats
Calothrix and Dichothrix with pink trichomes have bright
blue heterocysts, indicating the absence of phycoerythrin
in these heterocysts (B.A.W., unpublished). However, the
heterocysts of a lichenized Calothrix form phycoerythrin
(see Sect. 22.6.2)
The heterocysts of several Rivulariaceae have been
reported to germinate and produce short germlings. This
was described in most detail for Gloeotrichia raciborskii
and Rivularia manginii by Desikachary (1946) and a non-
sporulating mutant of Gloeotrichia ghosei by Singh and
Tiwari (1970). In all cases the cyanophycin granule by the
cross-wall disappeared at an early stage. Even where there is
not such a marked reversal of the initial differentiation to
form a heterocyst, heterocysts of Rivulariaceae sometimes
reform internal structures which have been lost in their initial
differentiation (Whitton 1987), such as carboxysomes in
Fig. 22.3 Trichomes near the centre of a Gloeotrichia pisum colony. The Calothrix D603 (Whitton et al. 1986). It was suggested
bright coloured heterocysts often occur in members of the Rivulariaceae that the heterocyst may have switched back from N2 fixation
attached to submerged plants, sometimes green or blue-green (as shown to CO2 fixation. Another possible explanation for blue
here), but other times bright blue (Photo C. F. Carter, with permission)
heterocysts is that the phycocyanin is behaving as a N store;
perhaps it can be mobilized more rapidly than cyanophycin.
heterocyst functioning. The new terminal heterocyst is Either or both features would be useful for an organism living
often smaller than the original one. Tests on the influence of in a highly variable environment.
Mg, Ca, Fe, Mo or S deficiencies in 13 Calothrix strains
showed a particularly marked effect of Mo deficiency on 22.2.2.3 Hormogonia
heterocyst frequency, the increase being at least four-fold in Hormogonia typically develop at the end of the trichome or,
each case (Sinclair and Whitton 1977a). Ca and Fe in species with a hair, immediately below this; in the latter
deficiencies also led to obvious increases in heterocyst fre- case the hair becomes detached and disintegrates. The main
quency in most strains. The extra heterocysts developed in zone of cell division typically shifts from nearer the base of
both basal and intercalary positions, but most of the latter the trichome to nearer the apex. A necridial cell is formed at
formed only a single polar nodule, thus leading to a ‘termi- the base of each hormogonium in Calothrix D184 and D550
nal’ heterocyst in the middle of the trichome. The hypothesis (Wood 1984; Wood et al. 1986) and this is apparently the
is suggested that in these cases the replacement of one type general situation in Rivulariaceae. Perhaps formation of the
of heterocyst by another may be due to a shift in the type of necridial cell helps to determine that the adjacent cell will
electron transport system. Presumably some of the element differentiate into a heterocyst.
in short supply is transported to the rest of the trichome, thus The rice-field isolate Gloeotrichia D613 (see Sect. 22.4.2)
aiding the formation of heterocysts elsewhere. showed a distinctive pattern when grown under a relatively
It is over a century since Fritsch (1907a, b) first commented high P concentration (Aziz and Whitton 1989). The trichome
on the tendency for heterocysts in tropical Rivulariaceae to developed as cell groups, each of which had originated
be blue and subsequent studies have shown blue heterocysts from one mother cell, something previously reported by
to be widespread, especially in ponds and rice fields (Whitton Schwendener (1894). Typically the cell group of Gloeotrichia
1987). This also occurs in temperate regions, although less D613 consisted of 8 cells; if so, cell 8 distant from the apex
widely. In other cases they may be bright green (Fig. 22.3) differentiated into a necridium, releasing the other 7 cells as
rather than blue. Studies on Calothrix D603 isolated from a cyanophycin-rich hormogonium. Subsequent to its release,
the surface of a deepwater rice plant in Bangladesh showed the lowermost cell of the hormogonium differentiated into a
that the blue colour increased as cultures became older and heterocyst about 1 day later. Seven is the typical cell number
trichomes increased in length (Whitton et al. 1986). This is in the hormogonia of many Rivulariaceae, although in some
the exact opposite of the situation with some Anabaena, strains there is considerable variation (Fig. 22.4).
especially tropical strains, where the blue colour persists for Hormogonia of Rivulariaceae usually contain all three
some time after differentiation, but eventually disappears. types of storage body, polyglucoside, cyanophycin and
Addition of NH4-N to young Calothrix D603 cultures polyphosphate. In C. parietina D184 cultured in N-free
566 B.A. Whitton and P. Mateo

of the missing element to cultures limited by other elements

also led to hormogonia formation, though the response
usually took longer than with P limitation. However, growth
of Calothrix parietina D184 to Fe-limitation, followed by
the addition of Fe, led to the release of gas-vacuolate
hormogonia, though often with hair fragments still attached
(Douglas et al. 1986). The study by Campbell et al. (1993)
on Calothrix PCC 7601 and 7504 showed that transfer to fresh
medium and incubation under red light led to hormogonia
formation, but not green light. Use of inhibitors demonstrated
Fig. 22.4 Hormogonia from Rivularia biasolettiana (B.A.W.) that the opposing effects arose through differential excitation
of photosystems I and II. Although the authors showed the
importance of electron transport in regulating cell differen-
medium cyanophycin was the most rapid to decrease (Wood tiation, assessing the ecological relevance of their results
et al. 1986). Few, if any, divisions occur in a hormogonium is more difficult. There is no mention of phosphate, but it
between the time it is differentiated and the time it separates seems likely that the cultures had been subcultured routinely
and often not until the first heterocyst is formed. However, under P-rich conditions and never encountered the alternation
subsequent to their release, Gloeotrichia echinulata hormo- of P-limited and P-rich conditions characteristic of their
gonia can elongate and then form necridia and fragment natural environment. (Based on its name in the UTEX Culture
into short lengths (Maxwell 1974). Something similar was Collection and published accounts, PCC 7601 is probably
reported by Adamec et al. (2005) for Calothrix elenkinii, not Calothrix, but Microchaete, though it has also been called
though their growth conditions make it hard to interpret Fremyella and Tolypothrix elsewhere! PCC 7504 was reported
the significance. When a culture grown in BG11 medium to be quite similar.)
(high combined N and high P) was transferred to N-free Calothrix strains in culture subjected to P limitation and
medium and then exposed to green light, there was a tran- then left for long periods eventually start to lyse, though
sient development of a trichome cell with high fluorescence often not for many months. However, in at least two strains
initiated by phycoerythrin absorption; this was followed by studied in Durham, short lengths in otherwise partially lysed
bleaching within about 20 min. These necridia permitted cultures differentiated into healthy hormogonia (B.A.W.,
trichome fragmentation. The authors suggested that this unpublished). Assuming the same behaviour occurs in some
allowed filaments to escape unfavourable environmental strains in nature, this would provide a means for a dying
conditions; in this particular case, however, there was no population to colonize new sites.
nutrient shortage.
Hormogonia can glide on surfaces, including other hormo- 22.2.2.4 Akinete
gonia and cyanobacterial trichomes, an important feature in The akinete develops next to the terminal heterocyst in most
colony formation (see below). Hormogonia of Calothrix in cases, but intercalary akinetes are frequent in some species.
streams, ponds and rice fields often have gas-vacuoles, even The akinete may develop from a single cell (Desikachary
though these are absent in the mature population; it is unclear 1959) or a number of cells with breakdown of the cross-walls
whether the presence of gas vacuoles influences gliding. (e.g. Gloeotrichia ghosei: Claassen 1973). Akinete forma-
Even without gas vacuoles, hormogonia of pond populations tion is a characteristic feature of Gloeotrichia, but also occurs
can persist in the plankton for some time and it needs careful in several species of Calothrix and in Dichothrix gelatinosa
observation to separate them from Oscillatoria. The transient (Böcher 1946). Two species of Calothrix have been reported
nature of the gas vacuoles was confirmed in the study of to form akinetes. The original illustration of C. stagnalis
two strains by Campbell et al. (1993): 8 h after release of by Gomont (1895) shows individual filaments epiphytic on
hormogonia, gas vesicle genes were expressed and phyco- Cladophora, so it is clearly not just a loosely organized
biliprotein genes repressed; by 24 h the converse was true. Gloeotrichia colony. The description of C. santapaui
In addition, hormogonia can lose their ability to form gas (Gonsalves and Kamat 1960) is less convincing, because
vacuoles during prolonged subculture in the laboratory, as the filaments were in a mucilaginous mass with other algae.
was shown for two Calothrix strains isolated from rice fields In addition, the spreading layers of the sheath are more like
in Nepal (Vaidya 1989). those of some Dichothrix. In G. ghosei, the only akinete-
The addition of phosphate to P-limited cultures led to forming strain of the 34 Rivulariaceae studied by Sinclair
hormogonia formation in all the Calothrix and Rivularia strains and Whitton (1977a), increased akinete formation occurred
tested (Sinclair and Whitton 1977a; Whitton 1987); addition under P limitation.
22 Rivulariaceae 567

Fig. 22.5 Growth of Calothrix parietina D550 in culture, showing

arrangement of trichomes following an initial period of hormogonial
aggregation and subsequent commencement to form multicellular hairs
Fig. 22.6 Very early stage in the formation of an epiphytic Gloeotrichia
when P-limited (Photo B.A.W.)
colony (perhaps G. pisum). The orange-brown colour of the heterocysts
probably indicates a high carotenoid content (Photo C. F. Carter, with
permission)
22.2.2.5 Colony, Trichomes and Sheath
Rivularia, Isactis, Gloeotrichia and most species of Dichothrix
all form colonies, while many species of Calothrix also Colony formation by a strain of Rivularia biasolettiana
form a macroscopic thallus with a characteristic appearance. on agar involves an initial period of aggregation, followed by
For instance, the hormogonia of C. pulvinata attach them- a period when no more trichomes are incorporated into the
selves to parent filaments, leading to a tufted, bushy struc- clump (B.A.W., unpublished). The trichomes then reorientate
ture. In many other strains of Calothrix grown in liquid into a hemispherical or subspherical arrangement and hetero-
culture the released hormogonia aggregate to form tight cyst development in the basal cell of each trichome becomes
clumps or, more usually, ropes (Fig. 22.5); observations on visually obvious. If determination of the cell to become a
C. parietina D550 isolated from a stream showed that the heterocyst has already occurred before the hormogonium is
most recently released hormogonia moved to the end of the released and occurs in the cell nearest the mother trichome,
rope (Livingstone and Whitton 1983). As growth proceeds, as observed for Calothrix D.256 (Sect. 22.2.2.2), rearrange-
the aggregated hormogonia eventually separate slightly ment to form a colony would require this end of a moving
(B.A.W., unpublished). Rivularia sp. IAM-M-261 showed a trichome to be in front, the opposite of what happens when
positive phototropic response to white light (Katayama et al. hormogonia are first released.
2007), but it is not known whether this is widespread in the Initially each trichome develops a sheath, which is attached
Rivulariaceae. to the lowermost vegetative cell; it never surrounds the
De Bary (1863) was the first to report that aggregation of heterocyst. Differences in colony structure, which vary
motile hormogonia into small non-motile groups was the initial markedly between species of Dichothrix, result from differ-
sign of colony formation in Rivularia. Similar behaviour ences in the way hormogonia become aggregated with the
occurs in Gloeotrichia echinulata (Maxwell 1974) and original after release from the mother trichome . There are
Gloeotrichia aff. pisum (Aziz and Whitton, unpublished). also marked differences in sheath structure, which are espe-
After re-arrangement into a spherical shape, the trichomes cially obvious in Dichothrix (Fig. 22.7). The sheath stays
start to differentiate (Fig. 22.6). Clonal cultures of colony- close to the trichome in D. orsiniana, with only the colourless
forming Rivulariaceae can sometimes form colonies, while parts of the hair projecting from the end; its sheath varies con-
others apparently do not (e.g. Chang 1979b), though in at siderably in the extent to which it is laminated. The sheaths
least some cases this is merely due to excessively high phos- of another widespread species, D. gypsophila, are not only
phate concentration in the medium, as shown by Berrendero strongly laminated, but the laminations splay open at the ends.
et al. (2008). However, other factors are probably involved in Sheath thickness increased in all 34 Rivulariaceae strains
at least some cases. For instance, in a study of the behaviour when grown to P limitation and in 13 strains became dark
of two marine Rivulariaceae strains transferred to laboratory brown due to scytonemin (Sinclair and Whitton 1977a). Other
culture, Darley (1967) found that aggregation of hormo- element deficiencies also led to thicker sheaths and in some
gonia only occurred if a large quantity was inoculated cases scytonemin formation. Comparison of two Calothrix
simultaneously. populations differing markedly in their scytonemin content
568 B.A. Whitton and P. Mateo

material when first removed from nature. It also relies on

the trichome or clonal culture originating from that trichome
being representative of the material isolated from nature.
In the Rivulariaceae in particular there is a risk that either of
these is wrong. Reliable identification of a P-rich culture
based solely on morphological features is almost impossible
and there is no way of knowing how representive a single
trichome taken from a colony is of the whole colony.
Two genome sequences have been completed: Calothrix
desertica PCC 7102 and Calothrix PCC 7103 (DOE Joint
Genome Project website, May 2011). Both strains have been
in culture collections for very long periods – over 60 years
for C. desertica. Both belong to the groups able to form hairs
(Sinclair and Whitton 1977a). Calothrix PCC 7103 was
originally maintained as Gloeotrichia sp. and has also been
Fig. 22.7 Dichothrix (probably D. gypsophila) filaments in a mixed called Nodularia sphaerocarpa, presumably when cultured
community developing into a stromatolitic crust on a boulder in Lough in high nutrient medium. Neither appears to have been used
Corrib, Ireland; sample treated with dilute HCl. Other phototrophs for ecologically orientated studies.
include Schizothrix fasciculata and several pennate diatoms (Photo
Rippka et al. (2001a, b) considered the taxonomic diver-
Bryan Kennedy, with permission). More views of this lake are shown in
the attached online article by Kennedy, O’Grady and Whitton sity of Calothrix and Rivularia. Clusters within these genera
were recognized by DNA-DNA hybridization studies using
the methodology of Lachance (1981), supplemented in some
from two Yellowstone thermal spring outflows indicated that cases by differences in pigment composition. Three clusters
the difference was partly genetic and partly environmental were distinguished within the 16 strains originally maintained
(Dillon and Castenholz 2003, Dillon et al. 2003). However, the as Calothrix (Rippka et al. 2001a). Cluster 1 (eight strains)
sheath composition (with about 50% neutral sugars and also showed a relatively high degree of genetic relatedness,
including 5% amino acids, small amounts of glucosamine and although it could be divided into five subclusters. All but one
galacturonic acid) of Calothrix parietina D550 and C. scopu- strain (C. marchica PCC 7714 = D184) can form hairs.
lorum D256 in culture was not influenced by changes in the P Cluster 2 (renamed from the cluster 3 of Rippka et al. 1979),
or Fe content of the medium (Weckesser et al. 1988). which had only one strain, had been isolated from a sphagnum
Three different morphological types of Rivulariaceae bog and was the only strain to form akinetes, when cultured
trichome were isolated from a single colony of Rivularia in the absence of combined N. It conformed best, though not
biasolettiana from a highly calcareous pond (Sinclair perfectly, to C. stagnalis Gomont. Subsequent phylogenetic
and Whitton 1977a). Molecular studies by Berrendero et al. analysis (Wilmotte and Herdman 2001) has shown that this
(2008) also indicate that Rivularia colonies may include strain (PCC 7507) fits in a different clade, where it shares
more than one genotype (see below). a branch with Cylindrospermum stagnale 7417. The other
cluster (seven strains), which were all marine isolates, was
transferred to the form-genus Rivularia based on the fact that
22.3 Molecular Perspective on Taxonomy one of the strains had previously been identified by R. A.
Lewin as Rivularia sp. Essentially this means that Rippka
22.3.1 Status of Classical Genera et al. (2001b) were treating freshwater tapered organisms
with and without hairs as Calothrix and marine ones as
A considerable number of molecular studies have been Rivularia, irrespective of any colony structure. Because of
reported to help understanding of the phylogenetic relation- uncertainty about strain names in the Pasteur Culture
ships within the cyanobacteria in general or in particular Collection, it is unclear whether any freshwater Rivularia
groups. Most have been based on 16S rRNA gene sequences, (or Dichothrix) had been included in the study.
with the interpretation on results relying on the fact that no The study of Sihvonen et al. (2007), which was based
horizontal transfer has so far been detected for this gene on 16S rRNA sequencing, compared 42 strains of Calothrix,
(Thomazeau et al. 2010). A variety of terms have been Gloeotrichia and Tolypothrix. This study had the advantage
introduced to help interpretation of molecular results, such over Rippka et al. (2001a, b) in that 34 of the strains had been
as form-genus in the 2001 edition of Bergey’s Manual. As collected from brackish (mostly c. 50/00) and freshwater
mentioned above, interpretation of such studies relies on sites around the Baltic Sea and only eight were taken from
the name given to a strain being that most suitable for the the Pasteur Culture Collection. The three genera showed a
22 Rivulariaceae 569

high level of genetic diversity and, in the case of organisms by light microscopy and both this and the DGGE comparison
identified morphologically as Calothrix, the sequence differ- indicated one Rivularia and one Gloeotrichia.
ences were sufficiently large to suggest at least five different Phylogenetic analysis by Berrendero et al. (2008) used
genera. There was no correlation between the phylogenetic sequences from both 16S rRNA genes and an intergenic
clusters and site or habitat from which the strain had been spacer (cpcBA-IGS) (see Sect. 22.3.2). A neighbour-joining
isolated, nor did the nine strains able to produce hairs group tree based on 16S rRNA genes showed 35 Rivulariaceae
together. Several strains clustered with 16S rRNA genes grouped together, including all those isolated in their study.
from other genera e.g. Calothrix brevissima IAM-M249 with Data for two other strains listed as Calothrix in GenBank
Tolypothrix strains. The strongly tapering Calothrix strain grouped with other genera. A further analysis based on 16S
BECID 18 did not cluster with any other strain and had the rRNA gene sequences (Berrendero et al. 2011) confirmed the
closest similarity (94%) with Cyanospira rippkae PCC 9501. diversity of Calothrix, but also their clear separation from
A cluster comprising Gloeotrichia echinulata strains shared eight Tolypothrix isolates and material of T. penicillata, all
98% sequence similarity, but were distant from the strains of from rivers in Spain. The two groups could also be separated
the other genera. The authors also reported that a number of based on their morphology when cultured in a medium with
Calothrix strains from the Baltic Sea differentiated solitary 0.2 mg L−1 P, but not in standard BG-110 medium with
akinetes or chains of akinetes. Although it seems clear that 5 mg L−1 P.
several organisms considered as Calothrix can form akinetes Domínguez-Escobar et al. (2011) made a comparison
(Sect. 22.2), the comment by Sihvonen et al. suggests that based on not only almost the complete 16S rRNA gene, but
their study may have included strains corresponding to also intergenic transcribed spacers and part of the 23S rRNA
Gloeotrichia based on classical taxonomic criteria. gene. Strains of Calothrix, Rivularia and Tolypothrix were
Calothrix is also mentioned among various cyanobacteria isolated from diverse geographical regions and habitats.
in several 16S rRNA sequence studies dealing with a par- Based on results for their newly isolated strains and data
ticular type of environment. Taton et al. (2006) isolated 59 for Gloeotrichia from Sihvonen et al. (2007), the authors
cyanobacteria from 23 Antarctic lakes in order to characterize made molecular clock estimates on the origin of the various
morphological and genotypic diversity (though sequence genera. The methodology for doing this was based on
studies were only made on 56 strains). Based on morphology, a number of previous studies (e.g. Sanderson 2002) and
12 species were recognized, 4 of which are Antarctic endemics. involves approximations and estimates, such as the node
Based on gene sequence, 21 OTUs (operational taxonomic defining cyanobacteria being fixed at ~2,700 Ma (million
units) were recognized, using the criterion of sequences years ago) and a minimum age for the heterocystous
having more than 97.5% similarity. These included 9 novel cyanobacteria at ~1,618 Ma (Falcón et al. 2010). The latter
and 3 exclusively Antarctic OTUs. Calothrix was represented value in particular differs considerably from the ~2,400 Ma
by one morphospecies and two molecular data analyses. for Nostocales suggested in Chap. 2 (Sect. 2.4.1.2), so
A project (Cuzman et al. 2010) on the biodiversity of pho- the values of ~1,500 Ma for Calothrix and Rivularia, and
totrophic biofilms on fountains associated with monuments in 400–300 Ma for Gloeotrichia and Tolypothrix should be
Italy and Spain led to a comparison of 16S rRNA for 31 isolates treated with caution. Nevertheless they provide a stimulus
with sequences of strains from other sources in the GenBank for further critical study.
database. A neighbour-joining phylogenetic tree showed all
seven Calothrix and Rivularia strains grouping more closely
together than with any other genera. These included two 22.3.2 Molecular Diversity Within Form-Genera
Calothrix and one Rivularia from their own isolates.
Hongmei et al. (2005) reported a phylogenetic analysis of While studies described above include information on the
communities of mats of mostly filamentous cyanobacteria form-genera Calothrix and Rivularia, several deal specifically
in the 42–53°C range from China, The Philippines and with them. Shalini et al. (2008) using RAPD – PCR to assess
Thailand. Separation of 16S rRNA gene-defined genotypes the phylogenetic relatedness of 31 Calothrix strains from
from community DNA was achieved by DGGE, leading to India and a reference strain (UTEX 379). A combination of 12
the recovery of 36 sequences. Phylogenetic analyses indi- sets of primers generated 903 distinct polymorphic DNA
cated these formed novel thermophilic lineages distinct from fragments, indicating a wide range of variation among the
their mesophilic counterparts in the case of seven genera, strains. The highest correlation coefficient (0.821) was found
including the only Calothrix sampled. Srivastava et al. (2009) for two strains which came from the same geographical loca-
also used comparisons of DGGE bands from samples tion. The authors discussed the possible importance of
originating in (Uttar Pradesh) rice fields with GenBank geographical proximity in relatedness between strains,
database to characterize the cyanobacterial flora of low and though it seems just as likely that environmental similarity is
high salinity sites. They included a list of the taxa observed a key factor in this genus.
570 B.A. Whitton and P. Mateo

Berrendero et al. (2008) focussed on Rivularia, using The Blanco and Muga also had colonies with Genotype II,
colonies from five different rivers in Spain and one stream in suggesting the presence of Calothrix-like filaments in the
the UK, all calcareous. They also used 13 strains isolated from Rivularia colonies. Some colonies from the Blanco showed
calcareous rivers and one from a stream flowing over siliceous bands corresponding to both Genotypes I and III, suggesting
substrates. All were listed as ‘strongly tapering (Rivularia or that a single colony may include filaments of two different
Calothrix)’, but only Calothrix – no Rivularia – occurred in types (“species”) of Rivularia.
the siliceous stream. The methods included analysis of the The phylogenetic sequencing analysis, which formed part
phycocyanin operon (PC) and intervening intergenic spacer of the study by Berrendero et al., showed that the 31 strains
(cpcBA-IGS) and 16S rRNA gene sequences, together with in the Rivulariaceae group (see Sect. 22.3.1) fell into three
molecular fingerprinting. The cpcBA-IGS analysis showed distinct genotype clusters. The Genotypes I, II and III from
that all the sequences of environmental Rivularia colonies studies on their own colonies and isolates each fitted into one
and rivulariacean-type isolates from calcareous rivers fell of the three broader genotype clusters.
into one of three distinct genotype groups. Alignment of the Apparently no similar studies have included Dichothrix,
sequences revealed 100% similarity of some isolated strains but the results would be of considerable interest, because
with the sequences in some field Rivularia colonies. some species are morphologically little more than complex
Genotype I was found in Rivularia colonies from the forms of Calothrix, while others are hard to distinguish from
Endrinales and Matarraña rivers and strains isolated from Rivularia. A detailed analysis of Gloeotrichia would be even
these rivers, together with two other strains. Genotype II was more interesting, because the planktonic G. echinulata differs
found in isolates from the Endrinales, Muga and the siliceous considerably from other species in the genus, at least some of
stream. Genotype III was found in Rivularia colonies from which seem little different from a Rivularia able to form
the Alharabe, Muga and Red Sike (UK) and one isolate from akinetes (Sect. 22.5).
another river. All three genotypes were reported for the
Muga, though this may simply reflect the fact that, in addition
to the colonies, six isolates came from this river. Culture of 22.4 Physiology
Genotype I isolates in a medium with relatively low phos-
phate concentration (0.2 mg L−1 P) led to Rivularia-like 22.4.1 Carbon and Nitrogen
morphological characteristics, including secondary trichomes
remaining in the mother sheath, lamellated sheath, confluent In laboratory culture most Rivulariaceae appear to grow
trichomes and a tendency to form spherical colonies. However, more slowly than filamentous species with untapered
when Genotype II isolates were cultured in the same medium, trichomes, though a Gloeotrichia aff. pisum culture from a
they maintained Calothrix-like morphological characteristics Bangladesh deepwater rice field had a doubling time of
and only formed irregular clumps or bundles of trichomes. 12.6 h under optimum growth conditions (Aziz 1985). There
These results suggest that Genotype I isolated strains belong are a number of reports of photoheterotrophic growth and
to traditional Rivularia and Genotype II strains to traditional other physiological responses to sugars. When Calothrix
Calothrix. elenkinii was grown on a light-dark cycle, glucose enhanced
Berrendero et al. cautioned that, because some cyano- pigment production, especially b-carotene and chlorophyll
bacteria possess two or three PC operons (Golden 1995), (Prasanna et al. 2004a, b). Lebedeva et al. (2005) found that
their cpcBA-IGS analysis does not rule out the possibility of glucose enhanced phycocyanin production of Calothrix PCC
more than one PC being present, but only one sequenced. 7601 under red light, but not phycoerythrin under green light.
They therefore investigated this further using TGGE Dark heterotrophic growth with sucrose was reported for
(temperature-gradient gel electrophoresis), which allows the two Calothrix strains included in the study by Khoja
sequence-dependent separation of PCR products. The high and Whitton (1971); glucose did not support heterotrophic
sequence variability among the three genotypes, which gave growth of Gloeotrichia echinulata (Chang 1979a).
rise to three clearly separated bands, allowed each genotype All (heterocystous) Rivulariaceae tested have proved
to be characterized by its corresponding fingerprint. There was capable of N2 fixation and, in batch culture under continuous
only one band for each culture and this was consistent with light, the highest rates have been reported several days
the corresponding fingerprint. Colonies from the Alharabe after subculture to fresh medium. The rates are usually
and Red Sike, which best fitted Rivularia biasolettiana, much higher in the light than the dark, whether measured
corresponded to Genotype III. Colonies from the Blanco, in the laboratory (Stewart 1967; Chang and Blauw 1980;
Endrinales and Matarraña rivers all had bands corresponding Al-Mousawi 1984) or the field. The rate dropped rapidly
to more than one genotype. Those from the Endrinales, when intertidal Rivularia atra was transferred from light to
which were typical R. haematites, had not only a band dark (Khoja et al. 1984), a useful feature for this population
corresponding to Genotype I, but also one to Genotype II. which is sometimes smothered in sand for part of the tidal
22 Rivulariaceae 571

cycle. This contrasts with the only slight initial change in Rivulariaceae in the field, mainly marine sites, was summa-
rate shown by Calothrix crustacea mat on sand and Rivularia rized by Whitton (1987).
mat on silt at the edge of the lagoon of Aldabra Atoll (Potts Marked changes in N composition were found during
and Whitton 1977). Diel studies by Hübel and Hübel (1974) batch culture of Calothrix D764 (Islam and Whitton 1992b).
of C. scopulorum and Rivularia on the Baltic Sea coast found The concentrations of chlorophyll, phycocyanin and phyco-
that rates were usually 6–10 times higher at midday than in erythrin had all reached their highest values by the stage when
the night, though the difference was less marked during the culture had reached 35% of its final yield. Soon afterwards
July and August, presumably due to the greater daytime there was a sharp decrease in nitrogenase activity, which
accumulation of carbohydrate. The ratios between midday subsequently persisted at the same rate for several weeks.
and midnight N2 fixation in R. biasolettiana in Red Sike, 51% of the N present in pigments at the time they reached
Upper Teesdale, northern England, on two dates in August their peak values was transferred to other substances in old
were similar (8–16% at night) (Livingstone et al. 1984). cultures, presumably cyanophycin and molecules associated
Overall about 400 mol CO2 to 1 mol N2 was fixed during with maximizing uptake of nutrients in limited supply.
daylight and the authors suggested that N2 fixation may There are a number of reports of biochemical features
supply only a small percentage of its N requirement. However, which appear to characterize the Rivulariaceae. For instance,
another possibility is that N2 fixation rates are higher in in a study of heterocyst glycolipids, those of four Calothrix
spring when ambient, mostly organic, P can be almost three strains were dominated by a C28 rather than by the C26 carbon
orders of magnitude higher in this stream than in August chain of the 17 Nostocaceae studied (Bauersachs et al. 2009).
(Livingstone and Whitton 1984). (Use of the term ‘organic’ The functional and possible ecological significance of such
for P fractions is explained by Whitton and Neal 2010). molecular differences awaits study.
If so, then much of the C fixed in summer may be used in
sheath formation. The upper intertidal organisms Calothrix
scopulorum (Jones and Stewart 1969) and Rivularia atra 22.4.2 Phosphorus
(Reed and Stewart 1983) show greater inhibition under high
salinity of nitrogenase than photosynthesis, and it was sug- The inhibitory effect of even moderate concentrations of
gested that this may reflect channelling of fixed C into an inorganic phosphate noted by Fogg (1969) for Gloeotrichia
osmoticum. echinulata seems to be widespread in Rivulariaceae; however,
A comparison of nitrogenase activity of Gloeotrichia all the reported studies are for hair-forming species, so it
pisum colonies from the aquatic roots of deepwater rice is unclear whether this also applies to Calothrix strains
plants in Bangladesh with a laboratory isolate (Gloeotrichia incapable of forming hairs. The formation of hairs under P
D613) showed a rapid fall in activity in both cases with limitation (Sect. 22.2.2.3) was investigated further in Calothrix
the onset of dark conditions (Aziz and Whitton 1988). parietina D550 (Livingstone and Whitton 1983). Hairs are
Nitrogenase activity was much higher when material grown formed as the average value for cellular P falls to about 1%
in the dark for 12 h was transferred to the light than the highest dry weight, when the filaments still appear healthy, indicating
rate found under continuous illumination. Longer periods that the change occurs when the organism is only moderately
of dark pretreatment led to only moderate increases in the P-limited. If phosphate is added to a culture with hairs, poly-
period before peak nitrogenase activity was reached again. phosphate granules are formed rapidly in cells towards the
On transfer from light to dark, nitrogenase activity fell rapidly base of the trichome and a few hours later several hormogonia
to very low values. Comparison in a Bangladesh deepwater start to differentiate at the apical end of the chlorophyll-
rice field of the% total nitrogenase activity at night for containing part of the trichome. Light is not essential for
Gloeotrichia cf pisum and G. natans (each on two different polyphosphate granule formation in Calothrix D550, though
days) compared with that of four other cyanobacteria showed it is for hormogonia formation.
that Gloeotrichia always had much lower % values (Rother Surface phosphomonoesterase (PMEase) and phospho-
et al. 1988). Nitrogenase activity of Calothrix D764, another diesterase (PDEase) activities of C. parietina D550 during
deepwater rice-field isolate, showed similar responses (Islam batch culture commence at about the same stage of P limi-
and Whitton 1992b). Rapid and marked responses to changes tation as hair formation (Livingstone and Whitton 1983);
in light are important during the monsoon season and may be release of extracellular PMEase commences at the same
a feature of deepwater rice-field cyanobacteria, as many were time (Grainger et al. 1989), though in some other strains it
found to show peak activity 6 h after dawn (Rother et al. commences later. No soluble extracellular PDEase is formed
1988). This response of nitrogenase activity on transfer to in C. parietina D550, nor in most other cyanobacteria and
light parallels the high rates of phosphate accumulation when eukaryotic algae (Whitton et al. 2005).
P-deficient cyanobacteria are presented with phosphate Several staining techniques have been used to compare
(Healey 1982). The early literature on N2 fixation rates by differences in distribution of PMEase activity between
572 B.A. Whitton and P. Mateo

Fig. 22.8 (a–c) Examples of

location of phosphomonoesterase
(PMEase) activity following
incubation in para-nitrophenyl
phosphate (2 mg L−1 P) for
30 min with subsequent staining
in 1% lead nitrate to deposit lead
phosphate: (a) PMEase activity
localized mainly on outer wall
layer of the hair cells of
Calothrix parietina D184
(= PCC 7713); (b) PMEase
activity in sheath of C. parietina
D184; (c) PMEase activity
mostly inside the cytoplasmic
membrane of hair cells of
Rivularia biasolettiana from a
stream in Middleton-in-Teesdale,
UK; (d) Microtubule crossing
middle of the cross-wall of a
vegetative cell of Calothrix
parietina D184: mi, microtubule
(Photos A. Peat, P. Wood and
B.A.W.)

species, growth stage and to show the influence of the whether PDEase activity is also present, but in view of the
environment. Light microscopy using BCIP (bromo-4- absence of soluble extracellular PDEase, this seems unlikely.
chloro-3-indolyl phosphate) and a simple phosphomonoester Electron micrographs of old cultures of Calothrix and field
as substrate to generate a blue stain can provide much useful Rivularia indicate that some activity also occurs inside the
ecological information, but electron microscopy with pre- cytoplasmic membrane of old hair cells (Fig. 22.8c), sug-
cipitation of lead phosphate is needed to show the exact gesting that organic P molecules sometimes pass through the
location of PMEase (Wood et al. 1986). cytoplasmic membrane of the hair cell. Hairs of Calothrix
PMEase activity usually occurs on the outer layer of the D550 formed in response to Fe limitation show no phos-
cell wall (Fig. 22.8a); it is often especially strong on the phatase activity (Douglas et al. 1986).
cross-walls. In C. parietina strains it develops on all cell walls In C. viguieri D253 (= PCC 7709) phosphatase activity
(apart from the heterocyst) and also in the sheath (Fig. 22.8b). is largely restricted to the hairs (Mahasneh et al. 1990).
It is more restricted in some other Rivulariaceae, developing This strain, which had been isolated from a mangrove root,
mainly on the hair cells and chlorophyll-containing cells was able to grow in media of varying salinities ranging from
near the hair and also the part of the sheath furthest from the freshwater to 20% seawater. However, when the culture was
heterocyst. However, the extracellular matrix of Rivularia P-limited, hair formation only occurred in freshwater medium.
colonies often shows marked PMEase activity. It is uncertain During growth in saline medium the PMEase activity was
22 Rivulariaceae 573

much lower and PDEase activity absent, while yields were the strains in the study formed extracellular PDEase. Within
less for most of the organic P substrates tested as the P source the Rivulariaceae, strains from calcareous environments show
for growth. It would be interesting to establish whether such higher PMEase activity than strains from non-calcareous
differences reflect adaptations to variations in the P status environments at pH 10.3 (p < 0.01), though not at pH 7.6. All
of water at its original location, such as might occur over a strains in this study were assayed using 250 mM substrate,
14-day tidal cycle. but a further study with 16 phototrophs showed that sub-
Once phosphate ions are released in the hair, rapid transfer strate concentration sometimes, but not always, influences
must occur to the base near of the trichome where poly- the response to pH (Whitton et al. 2005; Whitton and
phosphate granule formation starts. Electron-microscopy of Donaldson, unpublished data). The pH optimum for three
several strains showed conspicuous granule formation here Calothrix strains was 1.5–2 pH units lower using 1 mM
within 1 min, but much later further along the trichome substrate (methylumbelliferyl phosphate) compared with
(Wood 1984). Studies are needed to establish the exact 250 mM; the lower pH value was close to the typical field pH
mechanism by which phosphate moves from the hair to the All three strains were ones with hairs, as was the only eukary-
base of the trichome, but presumably a diffusion gradient is ote to show a similar response (Stigeoclonium D565). The
important. Calothrix D184 has a conspicuous microtubule strains not showing a response included all the Rivulariaceae
passing through the middle of the cross-walls of vegetative not forming hairs. Perhaps the species showing two pH
cells (Wood 1984). This extended for about 1 mm each side of optima have more than one mechanism for mobilizing
each cross-wall, but apparently not the whole length of organic phosphate. Phytase activity has been reported for
the cell (Fig. 22.8d). many Rivulariaceae, such as a Calothrix parietina strain
Several studies have permitted comparisons to be made from Upper Teesdale, UK, (Livingstone et al. 1983) and 35
between Rivulariaceae versus other cyanobacteria. In one of of the 42 strains tested by Whitton et al. (1991: see above),
these (Whitton et al. 1991) this was based on the ability of but the influence of pH has yet to be studied.
50 cyanobacterial strains (mostly tropical and subtropical) to Further insight into differences between Rivulariaceae
grow in batch culture with various P sources (1 mg L−1 P) and non-Rivulariaceae was provided by comparisons between
for 16 days; the study involved 30 Rivulariaceae and 20 two strains isolated from Rio Alberche, Spain: Calothrix
non-Rivulariaceae (13 filamentous and 7 Synechococcus) and elenkinii (not hair-former) and Nostoc punctiforme (Mateo
between hair-forming and non-hair-forming Rivulariaceae. et al. 2006). When inorganic phosphate was supplied to a
Several differences were significant (p < 0.05). In general P-limited culture, P uptake kinetics was closely similar for
Nostoc (six strains) produced the highest yields with inor- both strains. For instance, the half-saturation constant (Km)
ganic P, whereas Rivulariaceae produced higher yields was 2.98 mM for C. elenkinii and 2.99 mM for Nostoc
than filamentous non-Rivulariaceae with b-glycerophosphate, punctiforme. This indicates that a higher affinity for a low
pNPP and DNA. All Rivulariaceae grew well with a phos- inorganic phosphate concentration was not a factor likely to
phomonoester (pNPP, para-nitrophenyl phosphate) and a influence the relative success of C. elenkinii. The authors
diester (bis-pNPP, bis-para-nitrophenyl phosphate) and suggested that this was due to its greater ability to store P
all but one (Calothrix D764 from a deepwater rice field) as polyphosphate granules and its higher surface PMEase
grew with DNA. Many also used phytic acid (myo-inositol activity. However, an in situ survey (Mateo et al. 2010) of
hexakisphosphate), but seven did not (including Calothrix phosphatase activities of Rivularia biasolettiana and three
D764). Rivulariaceae forming hairs were more effective other cyanobacteria (Schizothrix coriacea, Tolypothrix
than those not forming hairs at utilizing phytic acid. It distorta var. penicillata and Nostoc verrucosum) in the River
seems likely that P is sometimes released by nuclease as Muga, found that Tolypothrix had the highest PMEase and
well as phosphatase activity, since 10 strains, all Rivulari- PDEase activities (related to chlorophyll), Schizothrix the
aceae, produced a yield with DNA at least 1.5 times that next highest and Rivularia the least on the four occasions
with pNPP. measured. Surface phosphatase activities of all the popula-
This study also indicated that Rivulariaceae are especially tions obeyed apparent Michaelis-Mention kinetics, showing
sensitive to ATP. Eight Rivulariaceae (including six hair- similar values for Km, but markedly different ones for Vmax,
formers) failed to show any growth with ATP (1 mg L−1 P) with Rivularia having the lowest values for both PMEase
and in some cases this was toxic. All the other filamentous and PDEase activities. In March, when Rivularia not only
forms grew well with ATP. A possible explanation is that showed the least phosphatase activities of any season, but
ATP enters the hair cells rather than being hydrolyzed at the also the greatest contrast with Schizothrix and Tolypothrix
surface and this leads to internal concentrations which are (Nostoc was absent), its trichomes had prominent polyphos-
inhibitory or toxic. phate granules. It was suggested that the contrasting results
The Rivulariaceae tended to show higher rates of surface may be due to Schizothrix and Tolypothrix growing faster
and extracellular PMEase and surface PDEase activity and the than Rivularia and already responding to the low ambient P
highest rates all occurred in strains of Gloeotrichia; none of found at the time.
574 B.A. Whitton and P. Mateo

Stream surveys provide records of Calothrix populations implicated in their action. The antiproliferative effect of
at zinc concentrations just below 10 mg L−1 (Shehata and calothrixins on several human cancer cell lines may be related
Whitton 1981; Whitton et al. 1981), a value well above that to their ring structure (Chen et al. 2003) and their ability to
for other heterocystous cyanobacteria. It is suggested that undergo redox cycling (Bernardo et al. 2004); further insight
this is another example of an environment where an ability to to the mechanism was obtained by synthesizing related
use organic P effectively is important, because inorganic P quinones (Bernardo et al. 2007). Among various effects on
is relatively insoluble under these conditions, especially as human cell metabolism, Khan et al. (2009) found that calot-
these streams also had elevated lead. Pb++ removal from hrixins act as poisons of DNA topoisomerase I and do so
wastewater by Calothrix marchica was higher in old than reversibly. The two molecules have now been synthesized
young material (Ruangsomboon et al. 2006), presumably (McErlean et al. 2007; Abe et al. 2011).
because of increased sheath production. Among other molecules reported from Rivulariaceae, but
few, if any, other cyanobacteria, are octadecatetraenoic
acid (Kenyon et al. 1972), brominated phenolic substances
22.4.3 Molecules with Possible from an axenic freshwater Calothrix and field material of
Ecological Effects marine Rivularia (Pedersen and DaSilva 1973) and six
polybrominated biindole derivatives from R. firma (Norton
A range of organic molecules with biological effects on cells and Wells 1982), the last being named rivularins by Maehr
of other organisms have been isolated from cyanobacteria and Smallheer (1984). Several of these authors discussed
(Smith and Doan 1999; Skulberg 2000; Van Wagoner et al. possible biological effects, but apparently none has been
2007), including some Rivulariaceae, such as the carbolines tested thoroughly. In an account of gene products of cyano-
from Dichothrix baueriana (Larsen et al. 1994). In some bacteria, Ehrenreich et al. (2005) listed a desert sand strain of
cases the circumstantial evidence suggests that these may Calothrix, which released a siderophore into the medium, as
be involved in protection from grazing (see Sect. 22.6.3.3). having some inhibitory effect on Synechococcus PCC 7002.
In other cases, even when there have been no ecological Molassamide, a depsipeptide serine protease inhibitor was
studies, features of the molecule, including its effects in bio- isolated from the marine Dichothrix utahensis (Gunasekera
assays, suggest that it be well worth doing so. Schlegel et al. et al. 2010).
(1998) found that, of 198 cyanobacterial strains, 7 (out of 13) The possible role of microcystins and other toxins in
Fischerella, 5 (out of 28) Nostoc and 3 (out of 9) Calothrix reducing grazing is considered in Sect. 22.6.3.3.
had bioactivity against green algae; the Calothrix affected
all three species tested. As the cyanobacteria were cultured
in a very P-rich medium, it would be worth repeating the 22.5 Overview of the Genera
survey with old, P-limited cultures, especially for Calothrix.
An extract of a marine Rivularia sp. showed marked antibac- 22.5.1 Introduction
terial activity against gram negative bacteria in comparison
with ampicillin and streptomycin (Zarmouh 2010). Studies The features of the five genera of Rivulariaceae were intro-
initiated by the research group of G. D. Smith at Canberra duced in Sect. 22.2.1. The morphological features of these
were especially promising, so it is worth summarizing how and other morphologically complex cyanobacteria frequently
this research proceeded. show an obvious relationship to features of their environment
This project started when Rickards et al. (1999) showed (Whitton 2008). It should therefore be possible to comment
that cell extracts of two Calothrix isolates inhibited the on the range of environments where Rivulariaceae occur from
growth in vitro of a chloroquine-resistant strain of the malaria an understanding of their morphological diversity. In addi-
parasite, Plasmodium falciparum, and of human HeLa cancer tion, the increasing realization of the molecular diversity
cells, both in a dose-dependent manner. Two pentacyclic of the genera (Sect. 22.3.2) raises the question as to how
metabolites (calothrixins A and B), with an indolo[3,2-j] much it will be possible to recognize by morphological crite-
phenanthridine ring system unique amongst natural products, ria the groups within the form-family Rivulariaceae which
were isolated and shown to have growth-inhibitory effects have close molecular similarity. If this proves possible,
at nanomolar concentrations (Doan et al. 2000, 2001). classical taxonomy could be revized to fit better with the
Calothrixin A was one of two cyanobacterial molecules molecular data.
found to inhibit Escherichia coli RNA polymerase competi- The presence of heterocysts indicates that N2 fixation is
tively with respect to ATP, and non-competitively with important at least some growth stage and thus there is prob-
respect to UTP. Based on comparisons with the sensitivity of ably a relative deficiency in combined N at that time. As the
whole cells to these inhibitors, the authors concluded that extent of tapering increases with increasing P limitation
other targets in addition to RNA polymerase may also be (Sect. 22.4.2), while hormogonia formation occurs when
22 Rivulariaceae 575

phosphate is added to P-limited material, the hypothesis loss. Chlorophyll a ranged from 0.25% to 2.8% (dry weight),
is suggested that the Rivulariaceae as a whole are adapted with values >1% only occurring for a short period when
to environments showing alternating N and P limitation. cellular P was at its maximum; 0.5% dry weight is probably
The extent to which the available data supports this is dis- typical for healthy field material. Chlorophyll a and phyco-
cussed below. cyanin contents both increased in% values as light intensity
was reduced from 85 to 10 mmol photon m−1 s−1. There was a
shift of N from cyanophycin to phycocyanin formation with
22.5.2 Calothrix decreasing light intensity.
When P was added to a P-limited culture of Calothrix
In addition to trichome width, whether or not mature D764 at the highest light value, the maximum cellular P
trichomes end in multicellular hairs and whether intercalary content was reached by 1 h, while the maximum nitrogenase
heterocysts form under some conditions, there are a number activity by 1 day. After a relatively short period of very high
of features which vary within the genus. Some, but not all, nitrogenase activity, the rate per unit mass fell rapidly, being
have been used as criteria for distinguishing species. Two 150 times higher on day 2 than at 5 weeks. However, each
species have been reported to form akinetes. The original heterocyst had to support about five times as many cells, so
illustration of C. stagnalis by Gomont (1895) shows indi- the equivalent comparison based on heterocysts between day
vidual filaments epiphytic on Cladophora, so it is clearly not 2 and 5 weeks was 32 times. Formation of new trichomes
just a loosely organized Gloeotrichia colony; the trichomes had slowed down by the end of the first week, but some still
have hairs. formed for a few more days; the subsequent increase in
The basal part of the trichome is swollen in some species biomass resulted entirely from the filaments growing longer.
(Sect. 22.2.2.1) and most, if not all, shown in Geitler (1932) Addition of P during this stage led to rapid formation of
are species forming hairs. The data by Sinclair and Whitton further hormogonia, each one being initiated at the end of the
(1977a, b) together indicate that species with swollen bases filament. The P content of 2.9% at day 1 fell rapidly and
tend to form hairs when P-limited. In the study of how surface PMEase first became detectable when it had fallen to
Rivulariaceae strains respond to combined N (nitrate), all 0.95%. PDEase was initiated at the same time as PMEase
strains with swollen bases in N-free medium belonged to the and the two activities ran closely parallel for the first 2 weeks,
group of strains where many trichomes retained obvious with values for PDEase being about one-third those of
tapering (but no heterocyst) in the presence of N; none PMEase. The presence of combined N in the medium led to
belonged to the other group where all the trichomes had higher surface PMEase and PDEase activities. Light had no
parallel sides, much like Lyngbya. However, Rai et al. (1978) effect on PMEase or PDEase activities on this or other
showed that the response of a C. brevissima strain differed Calothrix strains tested over periods up to at least 1 h, nor on
according to N supply: slight tapering remained with NO3-N, two rice-field Rivularia strains (Banerjee and John 2005) or
but not with NH4-N. When a culture supplied with NH4-N Rivularia colonies from River Muga (Mateo et al. 2010).
had depleted this, the trichomes formed intercalary hetero- This species grew almost as rapidly with glucose-6-P as with
cysts, followed by the initiation of polarity once more with inorganic P and quite rapidly with phosphomonesters, but
trichome breakage adjacent to the heterocyst.. not with DNA, in spite of the high PDEase activity and the
The other characters which have been incorporated into fact that most other Calothrix strains grow well with DNA as
taxonomic descriptions are whether the sheaths are brown the P source (Whitton et al. 1991).
(scytonemin), whether the sheaths are layered (e.g. C. pari- No doubt studies on other strains would all show slight
etina) and whether there is a distinctive colony structure differences in the sequence of events, but the morphological
(e.g. C. pulvinata). There are thus at least six features in changes in C. parietina D550, isolated from a UK upland
addition to dimensions that could be considered in relation to stream, were largely the same (Livingstone and Whitton
molecular groupings. 1983; Sect. 22.4.2), the main differences being that it formed
Batch culture studies on Calothrix D764, a strain isolated colourless hairs, which involved cell wastage when hormo-
from a hormogonium in the plankton of a Bangladesh deep- gonium formation was initiated beneath it; in addition,
water rice field provide insight on how trichome morphology, hormogonium formation ceased at an earlier growth stage
cell composition, nitrogenase and surface phosphatase than in Calothrix D764. The key changes in batch culture of
activities interact (Islam and Whitton 1992a, b). Although Calothrix seem clear. Nitrogenase activity is at its highest
this strain produced long, tapered filaments, which were when the P content is highest; surface phosphatase activities
ultimately very narrow and thus had the shape of a hair, the are absent at this stage, but then start to increase quite
terminal cells remained photosynthetic and increased only rapidly. Shortly after this, hormogonia formation ceases,
slightly in length. Under P-rich conditions a hormogonium and only recommences if further P is added to the culture.
formed in the apical region of the trichome without any cell Strains probably differ in that differentiation of hormogonia
576 B.A. Whitton and P. Mateo

Fig. 22.9 Rivularia bullata colonies on boulder taken from shallow Fig. 22.10 Colonies of Rivularia cf R. biasolettiana and the red alga
water in the very slightly brackish Loch Àirdh a’ Mhuile, South Uist, Chroothece growing in shallow water on the same boulder in a fast-
Outer Hebrides (Scotland), in September 2009 (Photo B.A.W.) flowing stretch of the Rio Chícamo, S-E. Spain. The dark colour of the
Rivularia colonies is due to highly pigmented brown sheaths, while the
orange-brown of the Chroothece is due to intracellular carotenoids
tends to cease earlier in strains forming hairs than in those (M. Aboal, personal communication) (Photo B.A.W.)
which do not.
As about 100 Calothrix species have been described, it is
not surprizing they are recorded from a range of environments. spread out in many layers; freshwater forms are also separated
However, quite a number occur in highly variable ones, such according to whether they show calcification. The taxo-
as the upper part of the marine intertidal zone. C. parietina nomic characters used for Dichothrix are similar to those for
often forms part of the microbial community in the zone Rivularia, except that the extent to which hormogonia are
where the water level fluctuates in about half the mature arranged in bundles is important; there is a tendency for
garden ponds in the UK with water above pH 7.0 (B.A.W., the trichomes of marine species to be wider than freshwater
unpublished). This also applies to C. parietina D550, which species. Isactis is unispecific; it is little more than a large
was isolated from the side of one of the streams described by group of vertical Calothrix filaments embedded in mucilage.
Livingstone and Whitton (1984), where the ambient P con- Freshwater Calothrix and Dichothrix occur in both very
centration is highly variable and mostly organic. Organic P soft (Heuff and Horkan 1984) and hard waters. The records
formed well over half the mean value for filterable P (n = 53) for Czech and Slovak Republics listed by Skácelová (2006)
in Bangladesh deepwater rice fields (Whitton et al. 1988a), confirm this for Dichothrix. Most records for Rivularia
where Calothrix and Gloeotrichia were frequent, and where are for calcareous waters (Fig. 22.10) and it is often the
Calothrix D764 (described above) was isolated. In the case dominant near the source of highly calcareous streams
of the Calothrix population in Hunter’s Hot Spring described (see Whitton 1987; Sabater 1989; Sabater et al. 2000).
by Castenholz (1973; Sect. 3.2.3.2; see also Fig. 3.2d, g), it However, in Jämtland, Sweden, and probably elsewhere in
seems probable that the intense grazing of the Oscillatoria northern Scandinavia (Johansson 1979; Johansson, personal
mat immediately upstream releases organic P. communication 1981) the genus is widespread in non-
calcareous waters. In the marine environment Dichothrix
is frequent on submerged angiosperms (Uku et al. 2007)
22.5.3 Rivularia, Dichothrix and Isactis and floating masses of larger algae. Floating masses of
Sargassum and epiphytic Dichothrix fucicola contributed
Rivularia species in classical floras are separated into marine over 0.5% total primary production in the western Sargasso
and freshwater, though records are often confused because Sea (Carpenter and Cox 1974), while production in October
of freshwater streams flowing into the intertidal zone. by Dichothrix was about 15% macroalgal production in
Conversely, waterbodies near the sea, but which are only continental shelf waters, though only 1.2% in the northern
very slightly brackish, may have marine species, as shown Sargasso Sea. The greater abundance of Dichothrix in shelf
for R. bullata (Fig. 22.9). The characters used for separating waters than the Sargasso Sea probably reflects the availability
species are mostly similar in marine and freshwater forms: of Fe. Calothrix is also frequent on marine angiosperms, but
trichome width, maximum colony size, soft or firm, whether more especially on ones that are intermittently exposed, such
the sheath is layered, whether the ends of the sheaths are as described by Webber (1967).
22 Rivulariaceae 577

The cycle of morphological changes for Rivularia in

relation to ambient P is similar to that for Calothrix, but the
periodicity of hormogonia formation and release is much
longer. Streams in Upper Teesdale, UK, show an annual cycle
of elevated P in spring, followed by far lower concentrations
for much of the rest of the year (Turner et al. 2003a, b).
The annual cycle of changes was especially clear in 1981–1982
(Livingstone and Whitton 1984); most release of hormogo-
nia by R. biasolettiana occurred in early spring following a
period of high organic P concentrations in the water. However,
in some years there are further short periods of sufficiently
elevated P concentrations to lead to marked hormogonia
release and further colony formation (Whitton et al. 1998).
In addition to the release of hormogonia, trichomes arising
from “false” branches occur in almost all Rivulariaceae; the
lower part of the original trichome develops a tapered shape Fig. 22.11 Rivularia cf R. biasolettiana in River Muga, N-E. Spain,
as it grows. However, in some cases true hormogonia are showing range of colony size reflecting older colonies and recently
formed which are not released from the colony, but differen- formed ones (Photo P.M.)
tiate into typical filaments inside the colony.
Although growth of an upper intertidal R. atra population
at Tyne Sands, S-E. Scotland, occurred mostly in summer Many “oligotrophic” waters do not contain Rivulariaceae.
(Yelloly and Whitton 1996), periodicity of colony formation However, the sites with Rivularia studied by Livingstone and
depended on a combination of extreme storm events and tides. Whitton (1984) and Yelloly and Whitton (1996) do at times
Storms deposited large masses of detached, mostly sublittoral, have high concentrations of ambient P (in some cases
seaweeds high on the supralittoral. These rotted and released >1 mg L−1 P for short periods), even though the annual mean
high concentrations of nutrients next time there was a high is far lower.
spring tide; much of the filterable P was organic. All the It is unclear how wide a range of P concentrations or
trichomes in large colonies released hormogonia within a N:P ratios is required to provide competitive success for
couple of days, leading to the formation of new colonies. Rivulariaceae and whether an alternation between low and
Dichothrix shows a similar response to periods of elevated extremely low values would be suitable. The River Muga,
ambient P, with hormogonia release followed by colony Spanish Pyrenees, never showed values for ambient total
formation, but the periodicity seems less clear-cut. Dichothrix filterable P > 6.8 mg L−1 P (mostly organic) during measure-
shows a marked tendency to be more frequent than Rivularia ments at five different times of year (Mateo et al. 2010), yet
in the west of the British Isles, while the reverse applies in new colonies can form in spring (Fig. 22.9).
the east (Whitton 2011). It was suggested that this may be The Rivularia population in the highly calcareous and
favoured by the greater and more irregular precipitation and slightly saline Rio Chicamo, S-E. Spain, presents a still
less marked seasonal difference between summer and winter unexplained anomaly (M. Aboal, personal communication).
that occur in the west. These may also explain why the Although healthy colonies with typical heterocysts are abun-
dominant Rivularia species in streams on Clare Island off the dant in some stretches of the river, often together with the red
west coast of Ireland is R. beccariana (Whitton 2007), which alga Chroothece (Fig. 22.11), the mean concentration of
forms only very small colonies, and probably does so for ambient combined N is high, hence no obvious advantage for
much of the year rather than mainly in spring. a N2-fixer. However, the mean P concentration is low and
Many studies have reported that Calothrix species and mostly organic, features which are likely to favour Rivularia.
sometimes Rivulariaceae in general are associated with low The most probable explanation is that there is some season of
levels of nutrients. For instance, Schneider and Lindstrøm the year or river condition when combined N is sufficiently
(2011) presented an index based on non-diatomaceous low to give Rivularia a selective advantage in competition
benthic cyanobacteria and algae to characterize river with Chroothece, but this has yet to be established. Other
trophic status in Norway based on total ambient P; all the possible (though unlikely) explanations for formation of the
Rivulariaceae showed a low indicator value. Although such hormogonia is that at some time of year Rivularia switches
indices are often required by water administration organi- almost entirely to P accumulation, leading to a high internal
zations, they neglect the importance of temporal variability concentration in spite of low ambient concentration, or that
in flowing waters draining semi-natural ecosystems and some other element shifts from scarcity to abundance for a
may hinder understanding of the processes occurring there. short period and this triggers hormogonia formation.
578 B.A. Whitton and P. Mateo

lamellae during dry spells; subsequent bacterial micritization

of the lamellae during an extended warm dry season. In the
particular climate experienced during the study period there
was either a single dark lamina for 2 years growth or a dark
lamina thicker than the annual growth rate. This suggests that
the extent to which laminations reflect marked annual changes
in climate and nutrient concentrations is likely to differ
between regions and sometimes between years. Although
carbonate deposition is rare among marine Rivularia, it has
been reported for R. mesenterica and R. polyotis (Golubic
and Campbell 1981), but apparently without laminations.
In a comparison (Myshrall et al. 2010) of stromatolitic
and thrombolitic (non-laminated) mats at Highbourne Cay,
Bahamas, the most obvious difference was the button mats of
calcifying Dichothrix in the latter. Dichothrix can also be
an important component of freshwater calcifying cyano-
Fig. 22.12 Rivularia haematites, from R. Guadiela, Spain. The layers bacterial communities (Whitton et al. 1986), individual
of calcite obvious in field material have been dissolved with very dilute colonies are not large enough to form distinct layers. Its role
acid, but a banded structure is still obvious due to differences in sheath in the marine environment is discussed in Sect. 22.7.
density and scytonemin formation (Photo P.M.)
Two other genera have been described. Sacconema Borzi
(1882) ex Bornet et Flahault (1886) seems little more than a
The seasonality of growth of Rivularia in many temperate form of Gloeotrichia with very thick and partly confluent
region streams and lake margins suggests this may be an sheaths, while Gardnerula (de Toni 1936) resembles a large
important factor leading to the laminated structure of Dichothrix colony with subdichotomous branching. Both
many colonies, especially those treated as R. haematites genera were mentioned briefly by Castenholz (1989), but
(Fig. 22.12); evidence for this in a UK stream population was only Gardnerula by Rippka et al. (2001c). However there
given by Pentecost (1987). Intermittent exposure to the air seems little reason why these should be treated as separate
and evaporation during the warmer season led to some genera rather than species of Gloeotrichia and Dichothrix,
calcium carbonate deposition in this population. Rivularia respectively.
EPS may also trap and bind calcite crystals (Pentecost and
Riding 1986). The factors influencing calcite formation
inside R. haematites colonies were studied at five sites in the 22.5.4 Gloeotrichia
Salzkammergut, Austria, by Obenlüneschloss and Schneider
(1991). The sites provided a wide range of conditions for Gloeotrichia includes all the colonial forms producing
light, flow variability and current speed and calcite crystal akinetes. Most are benthic in shallow lakes, ponds and
size showed an obvious correlation with these. For instance, ditches, but G. raciborskii and G. natans typically float at the
the largest and most regular crystals occurred at sunny sites surface for a considerable period, G. pisum and similar forms
with continuous flow and low current speed. The use of are epiphytic on older parts of submerged aquatic plants and
planar optodes and microelectrodes helped Pentecost and G. echinulata is planktonic during part of its growth cycle.
Franke (2010) to study the process of calcification in still G. ghosei was reported as floating or benthic (Claassen 1973)
more detail. A quantitative assessment of the factors involved and it seems likely that some other species are the same.
at each of various depths within the colonies of two popu- Other characters used in species descriptions include size of
lations (R. haematites and R. biasolettiana) led them to colonies, whether the sheath is layered, whether the hair
conclude that about 14% total calcium carbonate was the extends beyond the surface of the colony and the size and
result of photosynthesis. The calcite crystals grow parallel to shape of akinetes. Akinete details are in some cases essential
the trichomes and nucleate on the fibrous outer layer of the for species recognition, while long inspection of a pond
sheath (Caudwell et al. 2001). population may be needed to decide whether or not it can
The formation of laminae in R. haematites was monitored form akinetes. If not, it would be recorded as Rivularia, as
over a 7-year period by Caudwell et al. (1997, 2001) in molecular data would be needed to exclude the possibility
central France. A micritic dark lamina formed in three stages: that it was a Gloeotrichia which had adapted for survival at
(i) initial development of a dark lamina in the zone where that site by no longer forming akinetes..
the filaments develop false branching during the wet season; Akinete formation often leads to disintegration of the
(ii) calcification in this zone as microsparitic and sparitic trichome. However, sometimes several akinetes are formed,
22 Rivulariaceae 579

whilst at other times the trichome breaks away and can then without added chelator, as opposed to six which did. However,
form another akinete. Many queries could be answered by even when an artificial chelator was included in the medium,
careful observation. To what extent is the behaviour of Chang (1979a) found that soil extract and 5–40 mM glucose
the trichome subsequent to formation of its first akinete a both aided growth of an axenic strain. It has still not been
species- or strain- specific character? To what extent can established clearly whether or not planktonic G. echinulata
increase in colony number occur without akinete formation? forms its own chelator. This also raises the question as to how
Does the large size of the akinete permit a colony to develop important accumulation of elements besides P (see below) is
from a single trichome and, even if so, does colony formation for colonies developing on bottom sediments.
normally involves trichome aggregation. If trichome aggre- Although many of the reports of conspicuous G. echinulata
gation is the norm for colony initiation, what happens if the populations are for lakes which might otherwise be consi-
trichomes are too sparse for this to happen? The highly dered oligo- to mesotrophic, research was focussed initially
tapered and highly gas-vacuolate trichomes lacking a hetero- on eutrophic lakes. Caution is needed in comparing results for
cyst which were occasional in the plankton of a shallow a bloom-forming species at different sites, as has become
lakes on Clare Island in 2004 may have been such a case clear in the study of Microcystis (Chap. 7). Formation of dense
(Whitton 2007). These might have been a residual population plankton populations of Gloeotrichia echinulata was first
of G. echinulata too sparse to permit trichome aggregation, described for Ellesmere, a shallow English lake, by Phillips
as this species had been reported on the island by West (1912), (1884), though he quotes an 1880 report which mentioned its
but typical material could no longer be found there. period of hibernation at the bottom and then rising in summer.
Apart from G. echinulata, G. natans is the most widely However, the first detailed account was by Roelofs and
reported species, though apparently more frequent in sub- Oglesby (1970) for Green Lake, Washington, a shallow lake
tropical and tropical waters. It is common in rice fields. For without a permanent thermocline in summer. Subsequent to
instance, it is the most widespread cyanobacterium in rice G. echinulata disappearing from the plankton in September,
fields in Chile (Pereira et al. 2005), frequent in rice fields a bottom sample taken in November showed akinetes, but no
around Los Baños, Philippines (Martinez-Goss and Whitton, colonies. However, developing colonies were found on the
unpublished data) and frequent in deepwater rice fields near bottom in the following January. The authors mentioned short
Manikganj, Bangladesh (Rother et al. 1988). Populations filaments of 4–6 cells, though they did not explain whether
usually start to develop as attached colonies, but then become these were organized into spherical colonies. Colonies were
detached; these floating colonies sometimes become inter- still absent from the plankton on 23 June, but were entering it
mingled with submerged macrophytes, but often they float on 3 July. Apparently colonies were developing on the bottom
to the surface. Young colonies may include trichomes with for 6 months, while the planktonic phase only lasted for
gas vacuoles (Geitler 1932), but old colonies without gas about one-quarter of the year. In a 2-year study on the same
vacuoles may still float. eutrophic lake, Barbiero and Welch (1992) concluded that
A Philippines rice-field isolate was studied in the labora- the plankton derived 40% G. echinulata colonies from the
tory and outdoor raceway ponds by Querijero-Palacpac et al. benthos and that these accounted for a significant part of the
(1990), but BG-110 medium was used, so the results are internal P loading of the lake. However, Istvánovics (2008)
unlikely to reflect its behaviour in nature. In the laboratory concluded from their results and those of Karlsson-Elfgren
the specific growth rate was 0.076 h−1. Using a stirring rate of et al. (2003) that recruitment of colonies was insignificant in
30 rpm in the raceway ponds, daily production of cultures some years and so the internal P load is highly variable in
harvested to maintain cell densities of 0.7, 1.15 and 1.5 g Gloeotrichia lakes.
(d. wt) L−1 was 24.7, 17.1 and 18.1 g m−2 day−1, respectively. The most detailed studies have been on the moderately
The phycobiliprotein content in the culture maintained at eutrophic, stratified (in summer) Lake Erken in S-E. Sweden.
1.5 g L−1 reached 14% of the biomass. Heavy blooms of G. echinulata often occur during July
The planktonic G. echinulata has received considerable and August at the same time as the epilimnion deepens
study. Some of the first field experiments were by Spodniewska gradually to 10 m (Pettersson et al. 1990, 1993). Like other
(1971) using suspended bottles during summer in the eutro- wind-exposed lakes, akinetes and colonies are found in large
phic, holomictic Lake Mikołasjskie, Poland. She found that numbers on the bottom sediments (Istvánovics et al. 1993).
respiration averaged about 30% gross primary production for Benthic colonies averaged 5 × 105 m−2 in the top 4 cm of
G. echinulata. A suggestion by Rodhe (1949) that G. echinu- sediments in areas of the lake shallower than 10 m in March
lata needed an unknown organic component for growth led 1991 (Pettersson et al. 1993). Istvánovics et al. (1990) and
Zehnder (1963) to obtain evidence that the only organic factor Pettersson et al. (1990) suggested that epilimnetic growth
required for laboratory growth is a chelating agent. Lange might be largely or solely based on the internal P pool obtained
(1974) reported that G. echinulata was one of four bacter- while the organism was associated with the sediments and a
ized strains (species) of cyanobacteria which failed to grow number of P uptake experiments led Istvánovics et al. (1993)
580 B.A. Whitton and P. Mateo

to conclude the colonies were unable to acquire any P in the Lake (Barbiero 1993) and c. 1,520 colonies cm−2 day−1
epilimnion. The P uptake threshold exceeded the epilimnetic for Lake Erken (Forsell and Pettersson 1995). Nevertheless
concentration of soluble (filterable) reactive P by an order of Carey et al. (2009) concluded that increased sediment
magnitude. An overview of the results for Lake Erken indi- total dissolved phosphate may have influenced recruitment.
cated that recruiting colonies translocated some two-thirds A pulse of sediment was typically followed by an increase in
of the total net P load from the sediments to the epilimnion G. echinulata 18–19 days later. The authors commented that
(Istvánovics 2008). It is not clear how this fits with the this time-lag corresponds to the time akinetes need to germi-
observations of Karlsson-Elfgren et al. (2003) made during a nate (1–7 days) and take up P from the sediment (2–3 weeks)
2-year study that recruitment only contributed to <5% of before recruiting to the water column (Tymowski and Duthie
the maximum G. echinulata abundance during late summer. 2000; Karlsson 2003). Carey et al. (2009) also raised the
However, the authors emphasized that variations in the question as to whether the influence of P on germination is
measured abundance of G. echinulata could reflect measured accelerated by a discrete pulse or because the concentration
rates of migration from the sediment, and variations in either exceeds a particular threshold, as suggested by Pettersson
pelagic colony division rate and pelagic residence time. et al. (1993). Temperature and light are also factors which
The conclusion of Istvánovics et al. (1993) that epilim- can be involved (Karlsson-Elfgren et al. 2004).
netic G. echinulata did not use organic P in Lake Erken was In spite of the many studies on G. echinulata the growth
based on “alkaline phosphatase” activity measurements using and division of colonies have not been described in detail,
the method of Pettersson (1980). However, this methodology though partially separated, healthy colonies quite often occur
has limitations. Because of the high substrate concentra- in samples. Grazers can impact in various ways, including
tion used, the results may be unreliable at the pH tested removal of a whole colony or disruption into fragments
(Whitton et al. 2005). PMEase activity tends to be higher in (Sect. 22.6.3.1). It is unclear whether single filaments or the
Rivulariaceae than other cyanobacteria (Sect. 22.4.2) and small groups remaining after grazing can continue growth
when PDEase activity was compared, a Gloeotrichia strain and perhaps eventually form akinetes. G. echinulata can also
showed the highest ratio to phosphomonoesterase activity to have a considerable impact on other phytoplankton grazers.
any strain, suggesting the importance of phosphodiesters Colonies and culture filtrate of Lake Erken G. echinulata both
as substrates (Whitton et al. 1991). In addition Gloeotrichia stimulated the growth of some species known to co-occur
strains were the most successful genus at utilizing phytic with it in Lake Sunapee and Lake Erken (Carey and Rengefors
acid. Although these strains did not include G. echinulata, 2010). Of the seven species tested, none isolated from Lake
they indicate the importance of checking its ability to use a Erken, five were stimulated by the presence of colonies and
range or organic P compounds under realistic assay condi- two by filtrate. The potential effects of zooplankton popula-
tions. If the hairs of planktonic Gloeotrichia do not have this tions may depend on the duration and severity of a bloom
role, are they little more than a relic of structures important and the tolerance of the zooplankton to potential toxins;
at a late stage of benthic growth which helps to enlarge zooplankton populations may be able to maintain themselves
colony size? during prolonged blooms (Fey et al. 2010). However, inter-
The possibility that iron and boron might influence growth actions with G. echinulata and zooplankton might change
of G. echinulata colonies in Lake Erken was considered by with time due to the development of tolerance to toxins.
Hyenstrand et al. (2001) using an in situ experiment. Iron Cyanobacteria and heterotrophic bacteria associated with
had the most effect, enhancing the effect of adding phosphate G. echinulata colonies in Lake Erken, Sweden, may be a sup-
and nitrate. Addition of boron led to an even greater increase, plementary food source for the grazing zooplankton (Eiler
but boron had no effect if there was not additional iron at the et al. 2006), especially Daphnia pulex (Fey et al. 2010).
same time. Studies by Vuorio et al. (2009) on carbon isotope The use of experimental ponds by Carey et al. (2011)
signatures in colonies in Erken and Pyhäjärvi (Finland) showed that in nutrient-limited ponds the presence of
showed that there was a systematic increase in d13C with G. echinulata led to an increase in the biomass of small-sized
increasing colony size, in spite of substantial differences in phytoplankton and that this stimulation was related to the
the average d13C in the two lakes. The response to size was zooplankton biomass. An increased zooplankton biomass led
probably due to diffusion limitation of C availability. to increased grazing of colonies, which may have increased
Carey et al. (2008, 2009) reported on recent outbreaks of the rate of nutrient leakage to other phytoplankton, thereby
G. echinulata in oligo- to mesotrophic lakes in N-E. USA, intensifying the stimulatory effect. In contrast, G. echinulata
where at least 27 examples had occurred between 2002 had a negative effect on small-sized phytoplankton in eutro-
and 2006 in Maine and New Hampshire. In one of these, phic ponds. The authors concluded that in nutrient-limited
Lake Sunapee, recruitment of colonies was 1.13 and 0.32 systems, G. echinulata may subsidize plankton food webs in
colonies cm−2 day−1 in 2005 and 2006, respectively. These nutrient-limited systems through nutrient leakage and could
values contrast with the 36 colonies cm−2 day−1 for Green thus accelerate eutrophication.
22 Rivulariaceae 581

In several lakes studied in the UK, such as Talkin Tarn, Bangladesh at situations where the underwater parts of the
Cumbria, akinetes in planktonic colonies are most frequent plant are well illuminated, such as next to channels (Whitton
towards the end of the growth period, though occasionally et al. 1988b).
occur earlier in the season (B.A.W., unpublished). The storage There are many studies on the effects of cyanobacteria on
granules abundant in the akinetes are cyanophycin, suggesting rice plants, but most have used strains which had not been
the trichomes are P-limited by the time the akinetes form; growing in the vicinity of rice plants in the field. However,
presumably they are important as a N source when germinating Karthikeyan et al. (2009) studied the effects of 8 axenic
on the sediments. P limitation is therefore one factor likely to strains, including 3 Calothrix, which had been isolated from
be involved, but other factors should be investigated such as the rhizosphere of a wheat cultivar. C. ghosei showed the
possible responses to grazer activity. second highest nitrogenase activity in the light and the high-
In view of the many studies on G. echinulata we will est value in the dark. When wheat seedlings were co-cultured
summarize our own interpretation of the results. The species with C. ghosei, short filaments were found inside the root
can occur in lakes or other waterbodies ranging from near hairs and cortical region. Such strains were considered prom-
oligotrophic to eutrophic, but obtains much of its phosphate ising candidates for developing plant growth-promoting
from bottom sediments. It is therefore possible for moderate associations with wheat.
blooms to occur in lakes where water management organiza- In a comparison of the distribution of the epiphytes on the
tions had not expected a problem, providing the sediments marine angiosperm Posidonia by Trautman and Borowitzka
are rich enough in P. The presence of the organism may itself (1999), Calothrix, the only cyanobacterium included in the
enhance eutrophication over a number of years. Although list, grew on both sides of the leaves of Posidonia australis,
no evidence of P uptake could be found for epilimnetic though restricted to the basal sections. Other records include
G. echinulata in Lake Erken, further research is needed on Cymodocea nodosa (Reyes and Sansón 1997) and on
before it can be assumed that this applies to most lakes. Thalassia testudinum, where N2-fixing activity was correlated
The possibility that hairs have a role in mobilizing organic with the abundance of Calothrix (Capone and Taylor 1977).
P in less nutrient-rich lakes should be investigated. A similar correlation was suggested for N2-fixing activity on
Populations can persist in lakes ranging over at least three the mangrove Avicennia marina (Hicks and Silvester 1985).
orders of magnitude of colony recruitment from the sediments. Colonial Rivulariaceae almost always contain other cyano-
The species mostly occurs in stratified lakes, but populations bacteria and sometimes eukaryotic algae as well, especially
can persist in relatively shallow unstratified lakes, at least for pennate diatoms. Perhaps the initial period of trichome
a few years. In temperate regions it persists on the bottom for aggregation leading to colony formation permits entry of
the majority of the year, but little is known about how much some other motile species, though little is known about the
growth occurs during this period. Although the species extent to which invasion of mature healthy colonies occurs.
occurs in the tropics (e.g. Aldabra Atoll, 9° S: Donaldson Chang (1983) reported that Pseudanabaena catenata was
and Whitton 1977; central Brazil, 15° S: Campos and Senna frequent in Gloeotrichia echinulata colonies in Plöner See,
1988), there are no accounts of its seasonality in large tropi- Germany, in August and September, but not in G. echinulata
cal waterbodies. colonies earlier in the year. Based on various observations,
the author suggested that release of substances by G. echinu-
lata may favour growth of Pseudanabaena catenata.
22.6 Interactions with Other Organisms Quantitative studies on the frequency of various types of
diatoms in and on colonies of the marine Rivularia atra versus
22.6.1 Free-Living Phototrophs their frequency as epiphytes on macroalgae were made by
Snoeijs and Murasi (2004); the former relationship was des-
There are many records of Calothrix and Gloeotrichia, and cribed as symbiosis, but this extends the definition well beyond
occasionally other Rivulariaceae, growing as epiphytes, but that used by most authors. Among the 35 most frequent dia-
the extent to which this depends on features of the host tom species, the relative abundance of species with motile and
plant or merely the overall chemical environment is usually epipsammic life-form was 2.5 times higher within the Rivularia
unclear. However, the physical association with the host colonies than those with the attached epiphytic life-form.
plant is especially close in some cases, such as the occurrence The frequency of epipsammic forms in the colonies was due
of Calothrix and Gloeotrichia (and several other cyanobacte- to the frequency with which sand grains were incorporated
rial genera) on the lower epidermis and reproductive pockets into the colonies. Diatom community diversity was higher in
of Lemna leaves, and are presumably responsible for the the Rivularia samples, probably because cells epiphytic on
N2-fixing activity associated with some duckweed blooms the colonies were included. The motile diatoms inside the
(Duong and Tiedje 1985). A small colonial Gloeotrichia is colonies were ones that occurred in mucilage matrices when
frequent on the submerged stems of deepwater rice plants in present on stones. Other reasons were suggested why the
582 B.A. Whitton and P. Mateo

relationship should be favourable for diatoms, including the nitrogenase activity, no heterocysts could be distinguished, yet
fact that the colonies are tough and can resist wave action; the heterocysts were found during culture; akinetes were also
authors did not consider the possibility that Rivularia toxicity formed, again raising doubt whether this symbiont really is
might deter grazers (see below), nor did they have any sug- Calothrix. Thajuddin et al. (2010) reported one strain of
gestion as to how Rivularia might gain from the interaction, Calothrix (again based on culture with BG-11o medium) among
other than some possible nutritional advantage. 18 cyanobacteria from coralloid roots of Cycas revoluta; pre-
sumably they overlooked the previous study, as they claimed
their record to be the first for Calothrix as a cycad symbiont.
22.6.2 Symbiotic Associations The importance of marine diatoms with symbiotic N2-
fixing cyanobacteria in various subtropical oceans, especially
Extracellular growths of Calothrix have been reported from the North Pacific, has only become clear in recent years,
the thalli of several marine green algae, either entirely within although they were first described by Lemmermann (1905).
the tissue, as in the Enteromorpha reported by Lami and The two intracellular symbionts, Richelia intracellularis and
Meslin (1959) and Codium decorticum from USA (Rosenberg Calothrix rhizosoleniae, both have terminal heterocysts, but
and Paerl 1981), or partially epiphytic and partially inside only the latter has a trichome with obvious tapering. Although
the tissues, as a Codium from New Zealand (Dromgoole Richelia intracellularis has not been isolated and brought
et al. 1978). In the case of C. decorticum, Calothrix was one into long-term culture, this has been done for Calothrix
of three cyanobacteria responsible for nitrogenase activity rhizosoleniae from Chaetoceros in the N. Pacific (Foster
within a reducing microzone. et al. 2010). The trichomes retained the terminal heterocyst,
The best known symbiotic associations between Calothrix but 2 years after isolation a culture also showed intercalary
and other organisms are cyanobiont-containing lichens heterocysts. The nifH, 16S rRNA and hetR sequences were
(Adams 2000). Although Nostoc is much the most frequent amplified and cloned from this isolate and field populations
cyanobiont in lichens, Calothrix is probably the next most of Richelia associated with Hemiaulus hauckii (N. Atlantic)
frequent. According to Ahmadjian (1967), it is the phototroph and Rhizosolenia clevei (N. Pacific) (Foster and Zehr 2006).
in Lichina, Calotrichopsis and Porocyphus and Dichothrix in The results indicated that the symbionts in the three different
Placynthium, although other authors consider the phototroph hosts are distinct species or strains. Based on assays of nifH
of some Lichina corresponds better to Dichothrix. The gene abundance and gene expression of plankton popula-
morphological appearance inside the lichen usually has only tions, there was no record for Calothrix rhizosoleniae in the
slight resemblance to free-living Calothrix. Henssen (1969) western tropical Atlantic (Foster et al. 2007), but there was in
found that the phototroph of Lichina rosulans consisted of the eastern equatorial Atlantic (Foster et al. 2009). This was
short, contorted chains and basal heterocysts were rare. probably the intracellular symbiont, but the possibility of
Basal heterocysts, but no tapering were found in L. polycarpa, free-living trichomes could not be ruled out.
while the photobiont of L. tasmanica and L. willeyi had nor- A comparison of the growth rates of cells in symbiotic
mal tapering (Henssen 1973). An ultrastructural study of association with estimates for ones which were not showed
L. confinis by Janson et al. (1993) showed that heterocysts that the rates were higher for symbiotic cells (Foster et al.
were present in the thallus, but differed from the rest of 2011). In the case of N2 fixation, the rates were similar among
the Calothrix cells in that no haustoria were in contact with the symbioses and there was rapid transfer (within 30 min)
them. Glutamine synthetase levels in the cyanobiont were of fixed N. The N2 fixation rates estimated for Calothrix and
a great deal less in free-living (cultured) Calothrix sp. The Richelia symbionts were 171–420 times higher when the
decrease was greater in mature parts of the lichen thallus cells were symbiotic compared with estimates for cells living
than in the apical region. Rubisco was mostly located in freely. The cyanobacterial symbiont fixed more N than
carboxysomes of the vegetative cells of the cyanobiont. needed for its own growth and in the case of Richelia, up to
In free-living (cultured) Calothrix sp., phycoerythrin was 97.3% fixed N was transferred to the diatom.
located along the thylakoid membranes in both vegetative
cells and heterocysts. Although the cyanobiont cells showed
a similar pattern, the levels were lower. 22.6.3 Animals
The cyanobacterium in the coralloid roots of the cycad
Encephalartos hildebrandtii showed no resemblance to any 22.6.3.1 Introduction
well known genus, but developed what the authors considered The account of Gloeotrichia echinulata in Sect. 22.5.4 indi-
to be a typical Calothrix morphology in culture (Huang and cates that a lot needs to be known for successful application
Grobbelaar 1989). The micrographs of the association do not of a modelling approach to provide quantitative predictions.
show unequivocally that the organism is Calothrix, perhaps Nevertheless Benedetti-Cecchi et al. (2005) showed for a
because the study used BG-11o medium, so further studies are marine mid-littoral assemblage how a basic understanding of
needed. Although the endophyte exhibited substantial the mechanisms of interaction of the main species plus some
22 Rivulariaceae 583

knowledge of their natural history can lead to correct predic- which is endemic in Lake Catemaco, Mexico, was investigated
tions of the effects of one species on another. Filamentous by Ruiz-Ramírez et al. (2005). The survival of the snail,
algae monopolized the substratum when limpets were absent, which is an important fishing resource, is threatened and
but, when present Rivularia, the red alga Rissoella and hence there is a need to culture it. Calothrix sp. grown in
barnacles colonized. Barnacles and Rissoella jointly reduced 40-L containers proved to be better than pelleted carp food.
the coverage of Rivularia and the local density of limpets
and this eventually led to colonization by filamentous algae 22.6.3.3 Partial Destruction of Filaments
late in succession. There was thus an intermediate stage in A number of studies are known where Rivulariaceae popula-
the succession when Rivularia was successful. The interac- tions appear especially successful in resisting grazing pres-
tions are probably similarly complex in most ecosystems, but sure. Several reasons have been put forward to explain this.
the following are simplified accounts of the main types of Mats of Calothrix embedded among Pleurocapsa persist
interaction between Rivulariaceae and animals.. in the lower parts of the temperature gradient of hot springs
of the western USA, where grazing by ostracods eliminates
22.6.3.2 Destruction of Whole Filaments other cyanobacteria capable of overgrowing these species
Rivulariaceae are of course frequently influenced by graz- (Wickstrom and Castenholz 1985). In the case of Hunter’s
ing and this is described for Gloeotrichia echinulata in Hot Springs, Oregon, Calothrix and Pleurocapsa withstood
Sect. 22.5.4. Sometimes there may be little selection for or a dense population of Potamocypris sp., which exerted heavy
against a particular cyanobacterium, as in the study by grazing pressure on Oscillatoria terebriformis, the cyanobac-
Theivandirrajah and Jeyaseelan (1977) on grazing of Calo- terium dominating immediately upstream in the temperature
thrix and Anabaena by mosquito larvae in a Sri Lankan pond. zone where the ostracod was unable to persist (Castenholz
However, Edmondson (1938) reported that the rotifer Lindia 1973). The hairs of the Calothrix, which protrude from the
euchromatica in the littoral zone of Linley Pond, Connecticut, colonies, are, however, heavily grazed (Castenholz, personal
targeted Gloeotrichia. As it lived in the “slime” of the cyano- communication 1978). An experimental study (Power et al.
bacterium, where it fed on the filaments and deposited its 1988) showed that the dominance of Calothrix in a stream
eggs, it is unclear whether this was G. echinulata or a spe- in Ozark Mountains, Oklahoma, depended on the presence
cies forming larger colonies. In the case of floating G. natans of grazing by fish such as minnows. When the grazers were
colonies in the Botanic Garden near Chiangmai, Thailand, in removed, the Calothrix mats became overgrown by diatoms
October 2011, the colonies contained three large species of within 4–10 days, while re-exposure to grazers led to the
testate amoebae, at least one of which was frequent and grazing mats developing again. The authors suggested that the
Gloeotrichia trichomes by gradually engulfing and digesting ability to regenerate from basal parts of the trichome may
them from the ends (B.A.W., unpublished data). Lindia contribute to their persistence under intense grazing. They
euchromatica was the only grazer feeding on G. echinulata also discussed possible ecosystem-level effects, such as
in Green Lake, Washington (Roelofs and Oglesby 1970). whether the removal of loosely attached diatoms contributed
Although sometimes very abundant, it was noted on relatively to the water clarity of Ozark streams dominated by cyanobac-
few occasions and only in late summer. Colony size (up to teria felts. This was in spite of the fact that dominance by
2 mm) was thought to restrict grazing by copepods and cla- the N2-fixer brought about by the grazing might enhance N
docerans. However, mesocosm experiments with Daphnia loading in the stream, as shown by Wilkinson et al. (1985) for
pulex, Holopedium gibberum, Ceriodaphnia quadrangula and the grazing of abundant N2-fixing cyanobacteria (including
Bosmina longirostris showed that they all increased the pro- Calothrix) on coral reefs.
portion of damaged colonies (Fey et al. 2010). Ceriodaphnia
damaged the greatest proportion, but only Daphnia pulex fed 22.6.3.4 Avoiding the Grazers
on Gloeotrichia echinulata reproduced. Nothing is known Cattaneo (1983) interpreted the success of Gloeotrichia pisum
about the impact of grazers on bottom sediments. as an epiphyte in Lake Memphremagog, Québec-Vermont,
G. echinulata was one of a number of filamentous cyano- as resulting from its ability to resist grazing by snails, which
bacteria cultures grazed by the amoeba Naegleria isolated had a large impact on other algae. When snails were excluded,
from Dianchi Lake, Kunming, Yunnan, China (Liu et al. but not oligochaetes and chironomids, the control epiphyte
2006). Forms with aggregated filaments such as Aphanizo- community was replaced by green algae, mainly Mougeotia.
menon were not grazed, which suggests that the Gloeotrichia It was suggested that the very tough sheath of Gloeotrichia
culture had lost its colonial structure. Unicellular Chroo- may protect it from grazing. A laboratory experimental study
coccales were ingested, but subsequently excreted. Nematodes (Osa-Afiana and Alexander 1981) showed that established
are sometimes frequent in old colonies of Rivularia biaso- populations of Calothrix and Tolypothrix were not grazed by
lettiana, but their possible role in destroying colonies has not the ostracod Cypris sp., whereas Aulosira and, to a lesser
been studied. The possibility of putting grazing to practical extent, Anabaena were. However, when the cyanobacterium
use as food for the apple snail Pomacea patula catemacensis and ostracod were inoculated together, the ostracod increased
584 B.A. Whitton and P. Mateo

in biomass just as much with Calothrix as with Anabaena. main waterbody and included not only cyanobacteria, but
Presumably Calothrix and Tolypothrix formed sheaths in older populations affiliated with Proteobacteria, Bacteriodetes,
cultures, though the authors did not discuss whether this was Acidobacteria, Fusobacteria, Firmicutes and Verrucomicrobia
a factor reducing the effects of grazing. (Eiler et al. 2006). Fan (1956) reported that the hyphae of
Rivularia colonies sometimes persist for very long periods, certain fungi parasitize the cells of Calothrix and the cells or
which can be as much as 10 years in the case of R. haematites trichomes usually die. Although cyanophage activity is
(Pentecost and Whitton 2000). As the presence of calcite important for many other bloom-forming cyanobacteria, no
crystals does not appear to inhibit grazing, at least by studies have been reported for Gloeotrichia echinulata.
molluscs, toxicity was suggested as a likely factor. Several
studies have now reported studies indicating its probable
importance for at least some Rivulariaceae. The need for 22.7 Geological Record and Environmental
colonies to survive for many months under P-limited condi- Change
tions with only slow growth during that period (Sect. 22.5)
would add to the value of any means of detering grazers. The As it is increasingly becoming possible to relate genera and
toxicity of calcified cyanobacterial communities from often also particular species of modern-day Rivulariaceae
Spanish streams to stream invertebrates was investigated by to particular types of environment, their presence in the
Aboal et al. (2000, 2002). Rivularia was abundant in these fossil record is also becoming important in interpreting
communities, though other cyanobacteria were also well past environments. If the interpretation of molecular data by
represented. The latter study, which generated index values Domínguez-Escobar et al. (2011) is correct (see Sect. 22.3.1),
for routine monitoring assays based on macroinvertebrates then Calothrix and Rivularia originated about ~1,500 Ma
and diatoms, showed a clear inverse relationship between the (Mesoproterozoic) and Gloeotrichia about and 400–300 Ma.
dominance of cyanobacteria and the values obtained for the (Carboniferous) This means that the doubts of Golubic
indices. Evidence for microcystin production by Rivularia and Campbell (1981) about fossil Rivulariaceae (mostly
in populations from N-E. and S-E. Spain was reported by concerning Palaeorivularia) may not be justified. Palaeocalothrix,
Aboal et al. (2005), Aboal and Puig (2009): MC-LR, MC-RR described from the Precambrian by Zhao-Liang (1984a, b) has
and MC-YR were predominant. Microcystin-LR was also a basal heterocyst, large akinete, trichome tapered toward the
reported for Gloeotrichia echinulata (Carey et al. 2007). apex and a sheath, all of which are features of Gloeotrichia and
Among 19 cyanobacteria isolated from the sediments of possibly a few species of Calothrix. Assuming structures had a
R. Nile and adjacent channels, all of which were toxic to similar physiological significance then as in modern Calothrix,
Artemia, extracts from Calothrix parietina and Phormidium then Palaeocalothrix lived in a well oxygenated environment
tenue caused neurotoxic symptoms to mice within 10 h; five with a marked variation in some nutrient, probably P.
other species showed hepatotoxicity (Mohamed et al. 2006). There are convincing records of Rivulariaceae for most
A different group of compounds was investigated by geological periods from the Pleiocene onwards. These are a
Höckelmann et al. (2009). This was the range of sesquiter- few examples. Dragastan et al. (1996) compared presumed
penes formed by the axenic geosmin-producing cyanobacte- Rivularia haematites from the Pleistocene and modern
rium, Calothrix PCC 7507, together with a comparison of material. Based on tube dimensions and morphology they
their abundance in old versus very old standing cultures. appear to be essentially the same. A 20-m core of Middle
Among the quantitatively important products, eremophilone Pleistocene travertine showed encrustations of Phormidium,
differed from the others in being mainly excreted into the Dichothrix and Rivularia (Casanova 1984). Various Pliocene
medium, so bioassays were conducted on its toxicity to three and Pleistocene deposits appear to include oncoids (see below)
invertebrates. Acute toxicity to Chironomus riparius (insect) or similar structures formed by cyanobacteria (Casanova
occurred at 29 mM and to Thamnocephalus platyurus (crus- 1982, 1984). Celyphus rallus is almost certainly an Early
tacean) at 22 mM, whereas no toxic effects were observed on Cretaceous Rivulariaceae (Batten and Van Geel 1985).
Plectus cirratus (nematode). Neither 6.11-epoxyisodaucane Among the microfossils associated with Late Cretaceous
nor isodihydroagarofuran exhibited toxicity to any of these freshwater stromatolites in Sonora, Mexico, Beraldi-Campesi
at concentrations up to 100 mM. et al. (2004) listed Calothrix estromatolitica. The use of
cyanobacteria as biomarkers of hydrological changes in the
Late Quaternary sediments of the South Kerala Sedimentary
22.6.4 Bacteria and Fungi Basin in India, was assessed by Limaye et al. (2010).
A study of three different types of modern Rivularia
Sequencing and phylogenetic analysis of 16S rRNA genes of colony (see Sect. 22.5.3) led Obenlüneschloss and Schneider
bacteria attached to Gloeotrichia echinulata colonies in Lake (1991) to several conclusions relevant to interpreting fossil
Erken showed a diverse community different from that in the material. Once the organic matter has decomposed, it is
22 Rivulariaceae 585

impossible to make direct conclusions on the trichome and frequent Dichothrix being intermingled with abundant
sheath morphology based on the calcification structures. Schizothrix fasciculata (Fig. 22.10 ): see also article by
As several different calcification mechanisms occurred in B. Kennedy et al. (2012) in online supplement to this book.
these colonies, it is doubtful whether different calcification In larger calcareous lakes, such as the Bodensee (Lake
structures in fossil analogues can be attributed to different Constance), benthic rocks can have a thick calcareous layer
calcification mechanisms. with a furrow or brain-like pattern (Müller-Stoll 1986), which
The possibility that carbonaceous meteorites might also is formed mainly by Schizothrix fasciculata and Rivularia
contain fossil cyanobacteria has been presented in a number haematites in the Bodensee; the author lists reports of other
of papers by Hoover, with the latest (2011) arguing the case lakes with similar structures. Oncoids form where detached
in detail. It includes the suggestion that several tapering calcareous growths are moved around by weak currents, such
structures with a smooth basal body in the Orgueil CI1 carbo- as the floor of the Untersee of Lake Constance, where they
naceous meteorite resemble the filaments with a heterocyst consist of Phormidium and Calothrix and/or Dichothrix
of a modern Calothrix, though the organism shown for com- (Schäfer and Stapf 1978). A study (Van Geel et al. 1984) of
parison from White River, Washington, does not resemble Lateglacial deposits near Usselo, The Netherlands, gives
typical Calothrix, including the fact that the filament is detailed records of changes in “Gloeotrichia-type”, though the
only 0.8 mm wide, apparently well below the limit for other authors did not give details of the structures counted. The
records in the genus. The paper includes much of interest and sequence, which started in an oligotrophic shallow pool with
led to rapid and vigorous internet discussion, some of it very low organic production in a barren sandy-landscape, had
highly critical. It seems likely the debate will continue for an early phase at about 12,600 B.P., but lasting several hun-
some time before there is any scientific consensus about the dred years, characterized as the Gloeotrichia-type, where
possibility of these meteorites containing cyanobacteria, Characeae were also important. The authors suggested N2
let alone that some of these resemble Rivulariaceae. fixation may have initiated nutrient availability.
The presence of Rivulariaceae in relatively recent calcare- As mentioned in Sect. 22.5.3, Rivulariaceae sometimes
ous deposits has been reported by many authors based on calcify in the marine environment. This was reported for
both molecular (Sigler et al. 2003) and morphological data. Dichothrix at Highbourne Cay, Bahamas (Planavsky et al.
Calothrix was among the cyanobacteria of stromatolitic sta- 2009), but the filaments were not preserved to form lithi-
lagmites at the entrance to a cave in Slovenia (Mulec et al. fied microbialites. In contrast, adjacent cyanobacterial mats
2007). The calcified remains of Rivularia colonies, espe- formed well-laminated stromatolites. However, Dichothrix
cially R. haematites, often persist in or around streams and contributed to one of the types of thrombolite described by
lake margins when they become exposed. Spherical or sub- Mobberley et al. (2011) and carbonate-trapping stromatolites
spherical oncoids in small calcareous streams usually consist in the marine environment can be formed by D. bornetiana
predominantly of Rivularia (Rott 1991) or almost entirely (Monty 1967).
so, such as those at Sunbiggin, Cumbria, UK (illustrated in
Whitton and Potts 2000). Based on the living algae found in
Little Conestoga Creek, Roddy (1915) concluded that the cal- 22.8 Discussion
careous structures all the way down the stream were formed
largely by Rivularia, and possibly also the calcareous struc- Although molecular data show that the Rivulariaceae are a
tures forming deep deposits under soil in the catchment. heterogeneous group, field and experimental observations
Oncoids had disappeared from this stream by the time it was indicate that they are all well adapted to environments with
resurveyed by Golubic and Fischer (1975), mostly likely marked variation in ambient P, often organic P in particular.
because of acidic industrial effluents. Most records of the In flowing waters and the marine intertidal this variation is
decrease (Kann 1982) or loss of calcifying Rivularia are, temporal, but it is both temporal and spatial in Gloeotrichia
however, probably due largely to P enrichment (Pentecost echinulata. The periodicity of temporal variation in Calothrix
and Whitton 2000). It also seems possible that atmospheric is much shorter than in colonial forms and in Dichothrix
N deposition leading to increases in stream water N might probably shorter and more irregular than in most Rivularia.
shift away from N2-fixers to eukaryotic algae adapted to When ambient P concentrations drop, stored polyphosphate
environments with high N:P (Mateo et al. 2010). is metabolized and surface phosphatase activities increase,
The Rivulariaceae are usually frequent together with nar- permitting efficient use of organic phosphates in the envi-
row sheathed Oscillatoriaceae in calcareous deposits on sub- ronment. Hormogonia formation ceases when internal P
merged rocks in shallow, highly calcareous lakes, where the concentrations fall below a particular level. Taxa differ con-
deposits are sufficiently thick and well-laminated to justify the siderably in the relative extent of their P-rich and P-limited
term stromatolite. The calcified layers forming stromatolites periods. G. echinulata in the eutrophic Lake Erken is probably
in Lough Corrib, Ireland, provide striking examples, with P-rich for much of the time it is growing actively, but there
586 B.A. Whitton and P. Mateo

may be longer periods in other lakes when the species is at ecology of Rivulariaceae to comment on the environment of
least moderately P-limited. fossil material and old lake plankton records in some detail.
Rivularia is at the other extreme and in temperate region
streams it is P-limited for much of the year. In this case the Acknowledgements We thank Prof. Yuwadee Peerapornpisal and her
students at the Department of Biology, Chiangmai University, Thailand,
long periods of presumably low metabolic activity and the for helping B.A.W. to visit the Queen Sirikit Botanic Garden with its
persistence of colonies for many years at some sites makes it conspicuous floating cyanobacterial colonies. We much appreciate
important for grazing activity to be minimized; their forma- helpful comments on a draft of this chapter by Dr Allan Pentecost.
tion of microcystins needs to be studied in detail. The presence
of more than one genotype in the colonies of at least some
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