Soils and Rice-Fields
Brian A. Whitton
Department of Biological Sciences, University of Durham, Durham DH1 3LE, UK
I. Introduction …………………………………………………………………………………………….234
A. Taxonomic Composition ………………………………………………………………………
B. Environmental Factors ………………………………………………………………………..234
1. Light …………………………………………………………………………………….
2. Water and Desiccation ……………………………………………………………….236
3. Salinity ………………………………………………………………………………….
4. pH ……………………………………………………………………………………….
5. Herbicides and Pesticides ……………………………………………………………
C. Nitrogen Fixation ………………………………………………………………………………238
D. Influence on Soil Properties and Roots ……………………………………………………..240
III. Subaerial Habitats ……………………………………………………………………………………..
1. Development of Subaerial Communities ……………………………………………
2. Dispersal in the Air ………………………………………………………………....…
3. Crust Communities in Semiarid Regions ………………………………………...…
4. Heavy Metal and Other Contamination …………………………………………..…
5. Sports Turf ………………………………………………………………………….....244
V. Practical Methods ………………………………………………………………………………….….247
A. Measurement of Abundance ………………………………………………………………….
B. Nitrogen Fixation ……………………………………………………………………………....
C. Assays for Fertility and Toxicity ……………………………………………………………...
VI.Concluding Comments …………………………………………………………………………….….
Cyanobacteria are an important component of many soils, including the surface crusts that sometimes cover
extensive areas in semiarid regions and mine spoil wastes. They are also abundant in many areas which are
wet or submerged for part of the year, especially rice-fields. Most soils forms have sheaths or mucilage and this
polysaccharide has important effects on the soil, mostly beneficial, such as improved soil structure, but
sometimes adverse where a dense surface layer impedes drainage. Nitrogen-fixing species often constitute half
or more of the species present in soils not enriched with nitrogenous fertilizer and these can contribute
combined nitrogen in several ways to adjacent vascular plants.
Attempts to enhance crop yield by adding cyanobacteria to soils have mostly focussed on paddy rice.
Although many studies have reported positive effects of such 'algalization', the number of locations where it has
been adopted as routine practice appear to be few, in contrast to the relatively widespread use of Azolla with
rice culture. Algalization is most successful where local species are used to prepare the inoculum, but there is
considerable scope for other improvements. It is important to obtain a much more detailed understanding of
cyanobacterial population dynamics over the whole annual cycle in agricultural systems where rice is grown for
only part of the year.
Cyanobacteria have been reported from a wide range
of soils, both on and below the surface. They are
also often a characteristic feature of other types of
subaerial environment and many intermittently wet
ones such as rice-fields. This chapter gives a brief
overview of their features. Other relevant
information is included in the chapters on
limestones, salts and deserts and some of the features
of cyanobacteria discussed there contribute to their
ability to compete in soils.
According to Granhall (1975), the major factors
(in addition to light) influencing the occurrence of
cyanobacteria in soil are moisture, pH, mineral
nutrients and combined nitrogen. Moisture was
especially important in favouring cyanobacterial
high cyanobacterial density in the loamy soil studied
by Zimmerman et al. (1980), where wet depressions
contained much higher populations than surrounding
dry areas. Tolerance of desiccation and water stress
is, however, widespread and cyanobacteria are
among the most successful organisms in highly
saline environments (Chapter 10). Cyanobacteria
have been reported to be infrequent in most soils
below pH 6.0 (Lund, 1947; Granhall and
Henriksson, 1969), though they are more frequent at
low pH values in tropical soils (Moore, 1963). Their
frequent occurrence on the surface of tropical soils
may also be favoured by the fact that the temperature
optimum for cyanobacteria is often higher by at least
several degrees than for most eukaryotic algae
(Castenholz and Waterbury, 1989). The ability to fix
dinitrogen is widespread in soil cyanobacteria (e.g.
Roger and Kulasooriya, 1980), species with this
ability having a competitive advantage where
combined nitrogen levels are low (Roger and
Kulasooriya, 1980; Howarth et al., 1988). Many
cyanobacteria tolerate high levels of ultra-violet
irradiation (Chapter 21) permitting them to survive
at the soil surface, whereas others photosynthesize
efficiently at low photon flux densities (van Liere
and Walsby, 1982), permitting effective
photosynthesis just below the surface.
Studies on the role of cyanobacteria in soils and
rice-fields have been hindered by a number of
problems. Most of these are considered in more
detail later in the chapter, but it is useful to be aware
of some of them straight away. The difficulty in
naming species has been a particular problem,
because many soil forms are morphologically simple;
what is probably the same organism may have been
given a variety of names, while the same name may
have been used for obviously different organisms. In
contrast, flooded rice-fields often have a diverse flora
of morphologically distinctive forms and this has led
to an extensive descriptive literature; a great deal of
useful information is held in such accounts, although
they tend to be ignored in the mainstream literature.
A lack of suitable methods for quantifying the
occurrence of cyanobacteria in soils and rice-fields
was at one time a problem, though the situation is
much improved (Whitton, 1996). Finally, because of
the importance of nitrogen-fixing cyanobacteria in
these environments, there have been many applied
studies aimed at enhancing their contribution to
nitrogen fixation. These have provided important
and interesting results, but, perhaps because of the
funding sources for such work, sometimes they have
led to uncritical papers and reports.
A. Taxonomic Composition
A detailed review of soil algae by Metting (1981)
gives many references to cyanobacteria, including a
list of those 37 genera with records for soil species.
Chapter 8 Soils and Rice-Fields
Both unicellular and filamentous forms are
represented, but the biomass usually consists largely
of filamentous forms. Examples of studies that
contain descriptions and figures of soil species are
given in Table 1. Anand's (1990) taxonomic account
of rice-field species in south India provides a
particularly useful guide to species likely to be found
in rice-fields everywhere.
B. Environmental Factors
Cyanobacteria growing on the soil surface often
show dark colorations - blue-black, brown, red-
brown or red. The darker colours usually result from
the presence of brown sheaths surrounding the
typical photosynthetic trichome and this colour is
much more pronounced in populations in open than
in shaded positions. The pigment reponsible for the
brown colouration, scytonemin, absorbs strongly in
the near ultra-violet region of the spectrum (c 370
nm in vivo: Garcia-Pichel and Castenholz, 1991)
and the evidence strongly suggests that scytonemin
production is an adaptive strategy for
photoprotection against short-wavelength solar
Table 1. Some examples of studies with detailed taxonomic and/or floristic information on soil cyanobacteria.
(See also Chapter 13, Table 1).
Czech Republic, Russia
Taxonomic account with illustrations
Morphology of soil species
Usar (alkaline) land floristics
Non-heterocystous species in rice-fields
Nostocaceae in rice-fields
Floristic account for rice-fields near Pusa
Floristic account for Kerala rice-fields
Detailed taxonomic account of rice-field species
Floristic account for Arunachal Pradesh rice-fields
Floristic account for Nagaland rice-fields
Floristic account of rice-fields
Survey of wide range of soil types
Guide to the older literature
Illustrations and floristic account
Soil flora of semi-desert
de Halperin et al. (1992)
Eldridge & Greene (1994)
Khan et al. (1994)
Economou et al. (1984)
Prasad & Srivastava (1968)
Tiwari & Pandey (1976)
Jha et al. (1986)
Anand & Hopper (1987)
Singh et al. (1997a)
Singh et al. (1997b)
Anderson & Rushforth (1976)
Ashley et al. (1985)
Russia and other former USSR
21). The darker colour may also enhance warming
of the substratum at times which are ecologically
important for some populations, as discussed by
Belnap and Harper (1995) (see below).
A number of studies have been made of the
vertical distribution of cyanobacteria (and eukaryotic
algae) in soil profiles. Most of the biomass usually
occurs at the surface, with some cells or filaments
penetrating several millimetres into the soil
(Schwabe, 1963), though the peak biomass
sometimes occurs just below the surface. Light
penetration through the substratum may be sufficient
for growth of filaments inside quartz-rich soils or
endolithic forms in deserts (Bell et al., 1986; Palmer
and Friedmann, 1990); the latter are described in
some detail in Chapter 13. The most detailed study
on light penetration is that of Garcia-Pichel and
Belnap (1996) on two desert soil crusts in S-E. Utah
formed by Microcoleus vaginatus, Nostoc and
Scytonema, where strong attenuation meant that the
euphotic zone of recently wetted crusts was only
about 1 mm below the surface of the crust. In frost-
sorted polygons on Signy Island, South Orkney
Islands, a large proportion of the microflora occurred
in the zone 0 -1 mm below the surface and few algae
occurred on the soil surface (Davey and Clarke,
1991). The authors suggested that such subsurface
colonization may be a desiccation - avoidance
strategy. Chlorophyll degradation products occurred
to depths of up to 8 cm.
There are many reports of cyanobacteria occurring
at depths some way below the surface in agricultural
and other soils (Metting, 1981), but it is not clear to
what extent natural populations are able to persist or
even increase in the absence of light. Some soil
cyanobacteria can grow photoheterotrophically using
simple sugars, though apparently not fatty acids; for
instance, 8 out of 14 isolates from the waterlogged
bank of a Senegal lake showed photoheterotrophic
abilities (Reynaud and Franche, 1986). Some strains
can also grow heterotrophically (Khoja and Whitton,
1971; Rippka et al., 1979), but Calothrix marchica
was the only one of four Spanish rice-field soil
isolates capable of doing so (Prosperi et al., 1992).
The filamentous forms are probably all capable of
movement under some conditions and phototaxis has
been demonstrated in many cyanobacteria , including
strains isolated from soil (Castenholz, 1982).
Species differ, however, in the extent to which
filaments exhibit motility in nature. Actively
growing filaments of Phormidium autumnale and
some other Oscillatoriaceae are apparently motile for
much of the time, whereas motility in many typically
heterocystous forms (e.g. Nostoc and Calothrix) is
restricted to hormogonia, which lack heterocysts and
are formed under specific conditions, such as
addition of phosphate to P-limited filaments
(Whitton, 1992). The ability of some soil
cyanobacteria to move permits them to be viewed in
a semi-natural form by placing cover-slips in close
contact with the surface of moistened soil and then
incubating in the light (e.g. Broady, 1979; Davey,
1991). Motile organisms frequently attach
themselves to the cover-slip within a few hours,
while new colonies of these and non-motile forms
may develop within a week.
Most species occurring below the soil surface are
probably attached to soil particles. Davey et al.
(1991) investigated the influence of morphology,
mucilage production and soil texture as factors
influencing attachment of cyanobacteria and
eukaryotic algae isolated from Antarctic fellfield
soils. Phormidium autumnale showed the highest
attachment of any taxon under simulated flow
conditions; in contrast to the eukaryotic alga
Zygnema sp., Pseudanabaena catenata showed
greater retention to the substratum with the least
2. Water and Desiccation
Air-dried terrestrial and soil cyanobacteria can
survive prolonged dry periods, as has been shown in
many studies. Some of these have been based on
material stored deliberately, such as Trainor's (1985)
use of 25-yr old material, but most studies have been
made on samples kept for other purposes. Widely
quoted samples are an 87-yr record for Nostoc
commune (Lipman, 1941) and the 7 genera of
cyanobacteria which grew from 16 samples of
partially air-dried soils from England kept in sealed
bottles for 23 - 70 yr (Bristol, 1919). Parker et al.
(1969) reviewed old literature and carried out further
studies on materials from the Missouri Botanical
Garden. Some of the older studies were not rigorous
enough to rule out the possibility of aerial
contaminants, but it is clear that some akinete- and
non-akinete-forming cyanobacteria can survive for
very long periods. The most frequently mentioned
genera are Anabaena, Aulosira, Cylindrospermum,
Fischerella, Lyngbya, Nostoc, Plectonema and
Stigonema. A number of green algae and a few
diatoms are also mentioned, so this property is not
unique to cyanobacteria.
This ability can make it relatively easy to store
field samples, enrichment cultures or even pure
cultures in a dry state. Roger and Ardales (1991)
reported on studies conducted at the International
Rice Research Institute in the Philippines. Strains of
cyanobacteria, which had been inoculated onto
sterile soil and then allowed to dry, showed high
survival in viability tests: of 70 strains, 67 regrew
after 20 months. Some dried and powdered samples
of mass cultures regrew after 8 yr. Cultures
distributed from the International Rice Research
Institute were sent as dried material on paper strips,
because these remain viable for several months and
are easy to mail but this method is less efficient than
the other two methods. Viability under these
conditions was relatively short. Of 136 N2-fixing
strains, 30 were lost after 16 months storage and 129
after 30 months. J. W. Simon and the author
(unpublished data) tested the ability of 20 axenic
isolates from Bangladesh and Thailand rice-fields to
survive after the samples had been allowed to dry on
2-cm lengths of washed cotton: all the filamentous
forms, but not a Synechococcus strain, survived for
at least one year.
Most soil cyanobacteria survive periods of
desiccation with little obvious morphological change
other than that resulting from loss of water. Those
genera which form akinetes (e.g. Anabaena) do so
largely as a response to nutrient or other limitation
rather than desiccation (Whitton, 1987).
Physiological features of desiccation-tolerant
cyanobacteria have been reported in a number of
studies. For instance, two drought-resistant strains
accumulated sugars to high concentrations when
matric water stress was applied, whereas two strains
not showing drought resistance did not do so
(Hershkovitz et al., 1991). The most detailed studies
have been done on Nostoc (Chapter 17).
Although many soil and desert cyanobacteria are
highly tolerant of desiccation, they require to be
rewetted thoroughly for full metabolic processes to
resume. A study (Palmer and Friedmann, 1990) of
cryptoendolithic communities in deserts showed that
cyanobacteria photosynthesize only at high matric
water potentials (> - 6.9 MPa, 90% relative humidity
at 20° C) relative to green algal-containing lichens,
which began to photosynthesize at a much lower
potential ( - 46.4 MPa, 70% relative humidity at 8°
C). The rewetting of dried Nostoc commune leads to
physiological responses in the sequence, respiration,
photosynthesis and, lastly, nitrogen fixation (Scherer
et al., 1984). A non-colonial culture of N. commune,
which had been stored at -99.5 MPa, showed
increased nitrogenase activity and size of
intracellular ATP pool, when rewetted; the upshift in
nitrogenase activity was preceded by a lag (Potts and
There are many accounts of saline (Singh, 1961; Ali
and Sandhu, 1972) and semiarid (e.g. Smith et al.,
1990) soils containing a rich cyanobacterial flora.
Where the soil becomes thoroughly wetted at
intervals, crusts of photosynthetic microorganisms
frequently occur at or near the surface and
cyanobacteria are usually an important component of
such crusts (Section III). Singh (1950) proposed that
enhancement of cyanobacterial growths on saline
(usar) soils in India could provide a means of
improving soil quality and eventually reversing the
trend to increased salinity. His proposals were later
expanded into a book (Singh, 1961). Microcoleus
appears to be the most widespread cyanobacterium
on saline surfaces throughout the world (Whitton,
1990), where it can play an important part in
stabilization of the underlying soil (Anderson and
Rushforth, 1976). Buttars et al. (1998) have
developed a method for inoculating sterilized soil
crusts, which involves the escape of Microcoleus
from alginate beads and its subsequent growth on the
soil. If this method can be applied on a large scale,
it might be possible to accelerate the rate of recovery
of highly disturbed soils and add to the more
conventional methods suggested by Singh (1961).
As mentioned above, cyanobacteria are infrequent
below pH 6.0 in most temperate soils: they were, for
instance, entirely absent below pH 5.4 in several
samples from Ireland (Dooley and Houghton, 1973).
However, there are situations where they occur at
substantially lower pH values. These include
tropical soils (Moore, 1963) and the edges of small
pools (Section II.C). Values down to pH 4.2 or even
slightly lower have been recorded in both cases
(author's observations). There are also scattered
records of cyanobacteria in highly acidic
environments, but, wherever these have been
subjected to careful study they have proved to be
Cyanidium (or perhaps one of the other small
probable that the soils and waters at pH values just
above 4.0 and which include cyanobacteria are all
ones with weak buffering capacity.
Cyanobacteria may also influence the pH due to
their metabolic activity. In addition to the marked
changes which can take place in paddy fields and
temporary pools overlying soil, they can also occur
within surface crusts. Localized values of 10, 2-3
units above the soil pH have been found in desert
crusts as a result of photosynthetic activity (Garcia-
Pichel and Belnap, 1996).
5. Herbicides and Pesticides
The influence of herbicides and pesticides on
cyanobacteria has been investigated in many studies
(Padhy, 1985; Roger, 1996b; Vaishampayan et al.,
1998), though most have been restricted to
laboratory cultures. Cyanobacteria are in general
quite sensitive to herbicides, because they share
many of the physiological features of higher plants
(Leganés and Fernandez-Valiente, 1992), which
form the site of herbicide action. The pre-emergence
herbicide, benthiocarb, was highly toxic to strains of
Nostoc and Anabaena (Zaitseva, 1979). However,
N2-fixing cyanobacteria are mostly relatively tolerant
to 2,4D (2,4-dichlorophenoxy acetic acid), at least
under field conditions (Stratton, 1987; Leganés and
Fernandez-Valiente, 1992). Differences have been
found between the tolerance to herbicides of
cyanobacteria and that of other organisms.
Anabaena, Nostoc and Oscillatoria formed visually
obvious growths in Italian rice-fields treated with
Fentin derivatives and sodium dithiocarbamate to
control green algae (Bisiach, 1970). A study
(Peterson et al., 1997) carried out in liquid culture
showed that hexazinone was less toxic to
cyanobacteria than to green algae, diatoms and a
duckweed, whereas the cyanobacteria were more
sensitive to diquat than the green algae. A number
of herbicide-resistant mutants of cyanobacteria have
been isolated from rice-fields or obtained in
laboratory studies (Singh et al., 1986; Modi et al.,
1991; Tiwari et al., 1991). However, there appear to
be no data on the rate at which resistance can build
up in the whole population of a species at a
Fungicides may also be quite toxic (Tarar and
Shewale, 1984), though resistant mutants are known
to occur (Vaishampayan and Prasad, 1981). There
are also a few reports of insecticide-tolerant strains,
but the extensive literature on pesticide tolerance of
cyanobacterial strains largely fails to consider
whether the particular strains used for experimental
studies have developed genetic tolerance to the
pesticide in question. However, it seems clear that
the influence of the pesticides used to combat insect
and nematode problems is usually much less than
that of herbicides and probably also fungicides,
though it differs according to the agent applied and
the species or strain tested. For instance, a
comparison of the effect of the carbamate pesticide,
carbofuran, on nine heterocystous cyanobacteria
showed that Anabaena fertilissima and Nostoc
commune were the most sensitive (Rath and
Adhikary, 1995). Three other pesticides (based on
carbaryl, dimethoate or endosulfan) tested on
heterocystous genera also showed wide differences
between species (Das and Adhikary, 1996). The
application rates recommended for field use probably
do not significantly reduce the growth of
cyanobacteria, but double the levels of Sevin
(carbaryl) and Hildan (endosulfan) might well be
harmful. Several field studies (e.g. Grant et al.,
1983; Simpson et al., 1994) have indicated that the
application of pesticides to paddy rice can enhance
cyanobacterial growths, presumably due to the
reduced activity of grazers.
C. Nitrogen Fixation
Cyanobacteria growing at the soil surface usually
form distinct colonies or aggregates. It is therefore
easy to collect material for assays of N2 fixation
using 15N2 or of nitrogenase activity using the
acetylene reduction methodology (see Section VB).
Many soil species have been reported to be N2-fixers
(e.g. Kabli et al., 1997) and some of the lichens
making up the crust communities of arid regions also
contain nitrogen-fixing cyanobacteria (Belnap, 1996;
Lange et al., 1998).
The literature includes quantitative data on N2
fixation by soil communities from diverse sites,
though the values have to be treated with caution
because of the near impossibility of making sufficient
measurements to consider all aspects of temporal
change and spatial heterogeneity. Another problem
is that it is seldom clear how much of the measured
activity is due to the cyanobacteria and how much to
closely associated heterotrophic bacteria. Crusts or
mats dominated by Microcoleus have been reported
to fix nitrogen in desert (Belnap and Harper, 1995),
estuarine and marine populations (Pearson et al.,
1979; Stal, 1988).
Although Pearson et al. (1979) included studies
with an axenic strain, Steppe et al. (1996) failed to
find evidence for a nifH gene sequence in four
isolates from a terrestrial crust and marine mats and
the authors concluded that Microcoleus spp. appear
to be incapable of fixing N2 and that it is epiphytic
bacteria which are responsible for N2 fixed in soil
crusts and marine mats dominated by Microcoleus.
One possibility is that the strain used by Pearson et
al. should be referred to another genus (Chapter 3),
but more isolates need to be studied before it is
concluded that there are no N2-fixing strains of
Microcoleus. Some of the illustrations of the
organisms isolated by Smith et al. (1990) from arid
soils in Central Australia) and which were shown to
fix nitrogen, do look quite like Microcoleus. Soils
inoculated with Microcoleus from pellets eventually
showed significant nitrogenase activity (Buttars et
al., 1998). It is clear that N2 fixation is important in
some Microcoleus-dominated crusts and mats, even
if it is due to heterotrophic bacteria.
The majority of nitrogen-fixers reported from soils
are heterocystous forms. The factors influencing
nitrogenase activity in Nostoc commune have been
investigated at many sites. A study (Solheim et al.,
1996) at Kongsflorden, Spitsbergen (79 °N), showed
that heterocystous cyanobacteria were the most
important sources of biologically fixed N in the area.
This was due either to Nostoc colonies on moist
sparsely vegetated ground or to cyanobacteria
epiphytic on mosses. In another study on
Spitsbergen, the activity of sheets of Nostoc
commune assayed in situ was shown to have a linear
relationship with their moisture content and the
assay temperature (Liengen and Olsen, 1997).
Among nitrogen-fixing cyanobacteria lacking
heterocysts (Gallon et al., 1991), most soil forms
appear to be associated with conditions such as
waterlogging, which lead to reduced ambient oxygen
concentration (Rother et al., 1988; Rother and
Among the wetland area communities which
would repay detailed study is the association of
Hapalosiphon with submerged growths of
Sphagnum. This was widely reported in the older
literature (e.g. West and Fritsch, 1927), yet appears
to have received no critical study. Growths of
Hapalosiphon are frequently associated with
Sphagnum cuspidatum at the edge of small pools in
the 'flow country' of N-E. Scotland, where pH values
of of pool waters mostly lie in the range 4.0 - 4.3 (V.
Standen and the author, unpublished data). There
are apparently no records of Hapalosiphon among
Sphagnum in northern England. In view of the
relative absence of
Fig. 1. Colonies of cyanobacteria (Anabaena, Cylindrospermum, Lyngbya, Porphyrosiphon notarisii,Scytonema mirabile and Tolypothrix
byssoidea) developing on moist soil in a deepwater rice field at Sonargaon, Bangladesh, several weeks before the arrival of the flood water.
Visually obvious communities will cover about half the surface of the field by the time the flood arrives. (Width of figure is 30 cm.)
atmospheric pollution in the flow country and the
high levels of deposition of atmospheric N in
northern England, it would be of interest to establish
whether atmospheric N2 deposits can lead to the loss
of the nitrogen-fixing cyanobacteria associated with
some species of Sphagnum.
Nostoc commune in and on a loamy soil in Russia
was found to fix 3.3 kg N ha-1 yr-1 (Pankratova and
Vakrushev, 1971). Apart from Nostoc-dominated
sites, most studies have been on the whole
community, including cyanobacteria and
heterotrophic bacteria. The importance of the
cyanobacteria in a moist Bangladesh rice-field prior
to the arrival of the floods (Fig. 1) was evident from
the fact that nitrogenase activity at mid-day was one
to three orders higher where there was a
cyanobacterial cover than where the soil was bare
(Rother and Whitton, 1989). Nostoc always showed
higher activity than Tolypothrix, whether expressed
per unit area or biomass. Most values for paddy
fields summarized by Roger and Kulasooriya (1980)
and Kaushik (1998) fall in the range 10 - 30 kg N
ha-1, though rates up to 80 kg N ha-1 were reported
from Mali (Traore et al., 1978). Values for Spanish
rice fields ranged from 0.23 to 75.5 kg N ha-1 yr-1
(Quesada et al., 1997), though dense cyanobacterial
growths were excluded, so the rates for the whole
community were probably sometimes even higher.
Studies on rice fields generally do not consider N2
fixation during the period of the year when the land
is not cultivated for rice, so the annual total may be
higher than that quoted. According to Belnap
(1996), the reported values for the crust communities
(Section III) of S-W. USA range from 0.02 - 365 kg
N ha-1 yr-1. (Belnap's summary is based on the
following: Mayland et al., 1966; MacGregor and
Johnson, 1971; Rychert and Skujins, 1974; Eskew
and Ting, 1978; Jeffries et al. 1992.)
D. Influence on Soil Properties and Roots
Roger and Kulasooriya (1980) described the
properties of rice-field soils which may be enhanced
by the development of cyanobacteria, though they
seem equally likely to apply to other soils. The
properties include improved organic content,
improved water-holding capacity, addition of
combined nitrogen, release of vitamins or plant-
stimulating hormones, formation of extracellular
polysaccharides leading to improved soil aggregation
and solubilization of phosphates. Some of these
effects have been studied in considerable detail,
though mainly for rice-field soils (Roger and
Kulasooriya, 1980), whereas others (e.g. vitamins
and hormones) require further study before being
accepted as proven.
Changes in the properties of the upper 0.7 cm of
experimental columns of a brown earth silt loam
incubated in the light were attributed to an increase
in the cyanobacterial population by Rao and Burns
(1990). The cyanobacterial counts eventually
reached about 106 g-1 dry soil, whether or not the
columns were inoculated deliberately. Significant
improvements were measured in soil aggregation
properties, and increases in dehydrogenase, urease
and phosphatase activities were also detected. All
three enzyme activities were however low compared
with activities in arable soils, perhaps reflecting the
adverse effect of waterlogging.
The production of extracellular polysaccharides by
cyanobacteria has also been shown to improve soil
properties such as aggregation in a number of other
studies (Bailey et al., 1973; Roychoudhury et al.,
1980; de Winder et al,. 1989; de Caire et al., 1997).
A study (Falchini et al., 1996) of the effects of
Nostoc strains on two clay soils from Tuscany
showed not only the beginning of aggregation, but
also protection of soil porosity due to reduction of the
damaging effect of the addition of water. However,
there was no significant improvement in the stability
of the water - soil structure.
polysaccharides can also have an adverse effect, if
they are associated with thick surface mats which
reduce the penetration of water into the soil. A study
(Katznelson, 1989) of effluent penetration into the
ground at the Dan Wastewater Reclamation Project,
Israel, showed that Phormidium autumnale had a
very marked clogging capacity. This was ascribed to
the release of copious mucus; two other
cyanobacteria, which formed less polysaccharide,
had a much lower clogging capacity.
An ability to mobilize insoluble forms of inorganic
phosphate is apparently widespread. All but one of
18 strains tested by Bose et al. (1971) solubilized
tricalcium phosphate; other materials utilized as P
sources by cyanobacteria include Mussorie rock
phosphate (Roychoudhury and Kaushik, 1989) and
hydroxyapatite (Cameron and Julian, 1988). Several
authors (e.g. Natesan and Shanmugasundaram,
1989) have implicated extracellular phosphatases in
solubilization of fixed soil phosphates, but more
critical studies are needed on this topic. However,
most cyanobacteria can mobilize organic phosphates
in their environment by means of cell-bound
('surface') phosphatases and often also extracellular
phosphatase; this is usually an inducible activity
(Healey, 1982). All 50 strains, including some soil
isolates, assayed for their ability to grow with
organic phosphates as their sole P source used
phosphate monoesters, almost all used diesters, but
only some used phytic acid (Whitton et al., 1991).
Most strains released part of their
phosphomonoesterase extracellularly, but never the
phosphodiesterase. There is some evidence that
cyanobacteria may be particularly effective at
increasing phosphorus availability in saline soils
(Singh, 1961; Kaushik and Subhashini, 1985), but it
is unclear which cyanobacterial features are
responsible for this property.
Cyanobacterial growths in flooded rice soils have
been reported (Das et al., 1991) to influence the
forms in which Mn, Fe and perhaps also Zn occur in
the soil. Their presence led to a decrease in
ammonium acetate - extractable forms of Mn and Fe
and increases in other forms of these elements.
These changes were considered to be due to release
of oxygen, addition of organic matter and especially
extracellular material. The decomposition of the
cyanobacterial biomass led to further changes in the
various fractions, which were ascribed to the
development of reducing conditions and the
formation of organic acids. A decreased content of
readily available Fe might help to minimize Zn
deficiency in rice.
Examples have been reported of higher plants
which stimulate or inhibit the growth of soil
cyanobacteria (e.g. Parks and Rice, 1969). Several
laboratory studies have shown that cyanobacteria
may not only be associated closely with the surface of
some roots, but may also occur intracellularly in rice
(Kozyrovskaya, 1990), wheat and other species. The
most detailed studies have done on wheat. In
addition to loose associations of Anabaena with root
hairs of wheat, Gantar et al. (1991a, b) found that
there were much tighter associations with some
Nostoc isolates; the latter penetrated both the root
epidermis and cortex. Experiments on joint
cultivation of cyanobacteria and crop plants were
extended by Svircev et al. (1997) to corn (maize),
bean, sugar beet and two rice cultivars. Where
effects were found, they tended to be greater in liquid
than sand cultures.
Cyanobacteria are sometimes conspicuous on the
surface of aquatic roots of deepwater rice (Whitton et
al., 1989) and there is evidence from 15N2 studies
(Kulasooriya et al., 1980) that part of this nitrogen
reaches the rice plant either as the result of release of
extracellular combined nitrogen or indirectly
following grazing or parasitism. These various
observations suggest that careful studies should be
made to determine whether or not intracellular
cyanobacteria are of quantitative importance in the
roots of plants at field sites where cyanobacteria are
conspicuous at the soil surface.
There are numerous other reports of free-living
cyanobacteria influencing the growth of adjacent
vascular plants. Many of the positive effects have
been ascribed to enhanced nitrogen availability,
either due to release extracellularly or following
decay of the cyanobacteria. The majority of studies
have been with agricultural crops, especially rice
(Section IV), but there have also been studies on
natural ecosystems. In the case of slow-growing
communities, convincing evidence depends on the
use of 15N2, as used to demonstrate transfer of fixed
nitrogen from a semiarid crust (Mayland et al.,
1966) and from a sand-dune crust (Stewart, 1967).
Kleiner and Harper (1972, 1977) found more
extractable P in soils with a cyanobacterial cover
than in nearby soils without such a cover.
The gelatinous sheath material of half the
cyanobacterial species studied by Lange (1976) was
able to chelate elements essential for their growth
(Fe, Cu, Mo, Zn, Co, Mn) and Belnap and Harper
(1995) considered the possibility that the sheaths
may also influence the availability of elements to
other organisms. Four of the five genera listed by
Lange as having this ability are represented by
common species in the soil crusts of western North
American desert soils. Belnap and Harper (1995)
showed that the effects of the soil crust on semiarid
soil in S-E. Utah (Section III) on vascular plant
species depended on both the element and the plant.
The elements N, P, K, Mg, Ca and Fe were present
in significantly greater concentrations in Festuca
octoflora growing on soils heavily encrusted with
cyanobacteria and cyanolichens than in plants on the
same soil where the crust had been destroyed. In the
case of Mentzelia multiflora, N, Mg and Fe were
present at significantly higher concentrations, but P
was present at significantly lower concentrations.
The authors suggested a variety of possible reasons
for these differences. As described above,
cyanobacterial N2 fixation is likely to increase the
availability of N to adjacent plants. The reduced
uptake of P by Mentzelia was probably due to direct
competition of its near surface root layer with the
surface crust. Cyanobacterial sheaths reduce particle
erosion (Section III) and may adsorb charged
nutrient cations Chelating compounds present in
sheaths may be responsible for the enhanced uptake
of Fe. Well-developed crusts are much darker than
areas without them, so soil surface temperatures may
be warmer and hence metabolic activity higher at the
time of year when usable moisture is most likely to
Many of the earlier studies which showed an
influence of cyanobacteria on seed germination or
growth of young rice (see bibliography in
Kulasooriya and Roger, 1980) were ascribed to
growth-regulating substances such as hormones and
vitamins. However, there has been no study in
which a cyanobacterial regulator has been isolated
and characterized. It also seems likely that only
positive results have been published, following the
screening study by Pedurand and Reynaud (1987) on
135 non-axenic cyanobacterial isolates on the
germination and growth of rice. 30% strains had no
effect on germination and 30% caused inhibition.
Among 8 strains of Anabaena stimulating growth,
only one remained effective after it had been made
III Subaerial Habitats
1. Development of Subaerial Communities
Subaerial communities of cyanobacteria and algae
were first described in detail from Sri Lanka
(Ceylon) by Fritsch (1907a,c) and his general
account (1922) of sites in a number of countries is
still worth reading. He concluded that the first
colonizers of rock surfaces are colonial
Aphanocapsa), often accompanied by Nostoc. The
stratum formed by these genera is sooner or later
colonized by filamentous forms (Lyngbya,
Scytonema, Stigonema and Hapalosiphon), usually
possessing sheaths which are firmer and less
gelatinous. These filamentous forms initially
produce a dense tangle on the rock, but often
eventually give rise to a tufted mode of growth, the
surface of which in extreme cases acquires a velvety
It is unclear how much the succession described by
Fritsch really does represent the sequence of changes
taking place on rock surfaces in the wet tropics or
merely reflects a comparison of different types of
community with increasingly favourable conditions
for growth. An extensive cover of tufted forms, for
instance, appears to be restricted to sites which are
very humid throughout the year. However, in the
case of lava and ash deposits from recent volcanic
activity, it is possible to observe true succession. The
widely quoted observation of Treub (1888) that
species of Tolypothrix, Anabaena, Symploca and
Lyngbya formed a gelatinous layer over the surface
of lava and cinders on Krakatau within three years of
eruption has led some ecological texts to regard this
as a general phenomenon. While cyanobacteria
certainly are important in the early stages of
colonization of volcanic deposits and other bare
surfaces such as mine spoils, they are not always the
dominants. During the colonization of Surtsey (off
the coast of Iceland), cyanobacteria were important
in some areas such as depressions, but overall were
less important than on Krakatau (Brock, 1973).
They were absent altogether during the pioneer stage
on the volcanic ash of Katmai, Alaska (Griggs,
1933). Brock attributed these differences in the
relative importance of cyanobacteria to temperature.
An enrichment study of surface materials from
different zones around a volcano in Hawaii did not
indicate that cyanobacteria were especially abundant
in early stages here (Carson and Brown, 1978), in
spite of the tropical location. The diversity and
quantity of soil cyanobacteria increased with nutrient
levels and organic status at the sites, with
cyanobacteria mainly being found in climax forest.
However, three genera were found nearer the
volcano, including Tolypothrix which was observed
directly among volcanic ash. This study would be
well worth repeating, this time including controls to
estimate the contribution from the air spora and
using a much less nutrient-rich medium.
2. Dispersal in the Air
Since cyanobacteria are frequent components of the
air spora (Schlichting, 1961, 1964; Tiberg et al.,
1983), they are likely often to be recovered from soil
enrichment cultures. Both the species of
cyanobacteria (Phormidium ambiguum,
laminosum) found on styrofoam blocks in a British
Columbia tree nursery also occurred in the local air
flora (Ross and Puritch, 1981). Sixty-three
cyanobacterial species were found during the
monsoon season in the air flora at Poona, India
(Balakrishnan and Gunale, 1980). Some aerial
organisms probably originate from soil surfaces
(Brown et al. 1964), but, especially in the tropics,
many are likely to come from aerial habitats such as
the surfaces of buildings and trees (John, 1988;
Garty, 1990; Mrozinska, 1990). Novelo-Maldonado
and Gonzalez-Gonzalez (1981) attempted to
distinguish between the soil and airborne algal
(including cyanobacteria) floras at a site in
Tehuacan, Mexico, by sampling simultaneously the
air, superficial and deep soil floras.
3. Crust Communities in Semiarid Regions
The most detailed accounts of subaerial communities
with abundant cyanobacteria come not from the wet
tropics, but from arid regions, such as the volcanic
soils in S-W. USA, where Microcoleus and Por-
phyrosiphon are important (Shields, 1957). Crusts
consisting of cyanobacteria, eukaryotic algae,
lichens, mosses and heterotrophs are conspicuous
components of the surfaces of arid and semiarid soils
worldwide (West, 1990). In cold deserts the crusts
cover interspaces between and under vascular plants,
and often constitute 70% of more of the living
ground cover (Belnap, 1996). (Belnap terms the
deserts of some parts of S-W. USA 'cold', whereas
the sames ones are termed 'hot' in Chapter 13 to
provide a contrast with the deserts of Antarctica.)
Such communities (often termed 'cryptobiotic') are
initiated by the growth of cyanobacteria during the
episodic events supplying moisture, leading to a
network of filaments and a matrix of extracellular
slime (Belnap and Gardner, 1993). If the largely
cyanobacterial communities remain undisturbed,
they may eventually give rise to the more complex
cryptobiotic communities. The presence of these
communities has marked effects on the properties of
the soil. Three of these have already been discussed,
the soil temperature at times critical for plant growth
(Section II.B.1), nitrogen fixation (Section II.C) and
ion chelation (Section II.D).
Belnap (1995) has shown how important the
cryptobiotic communities are for maintaining soil
stability and nutrient cycles and how harmful are
activities which disrupt the communities, such as
cattle and human trampling and off-road vehicle use.
Soil compaction and disturbance of the cryptobiotic
communities can result in decreased water
availability to vascular plants through decreased
water infiltration and increased albedo with possible
decreased erosion and decreased diversity and
abundance of the soil biota. The marked effects of
disturbance on the erodibility of these communities
were made clear by comparing the threshold values
of wind velocity leading to disruption of disturbed
and undisturbed sites in S-E. Utah (Belnap and
Gillette, 1997) and New Mexico (Marticorena et al.,
1997; Belnap and Gillette, 1998). In the last study
the threshold values for well-developed communities
were shown to be well above those of wind forces
occurring at the sites, whereas the values for
disturbed sites were below them and hence these
sites can be eroded by wind action. The use of a
wind tunnel to compare the ability of various
phototrophic communities growing on sand to resist
erosion showed that only cyanobacteria, especially
Nostoc commune, provided considerable protection
(Neuman et al., 1996). The need to manage
semiarid regions carefully in order to minimize
damage to the soil crust community also became
evident in a study of rangeland in S-W. Queensland
(Hodgins and Rogers, 1997).
The frequency of disturbance by a different
environmental factor, burning, has a similar effect
on soil shear strength in coppice woodland in
Zimbabwe (Belnap et al., 1996). The effects of the
following treatments were compared: no-burn; burn
every 2 years; burn and mattock every 2 years; burn
every 4 years; burn and mattock every 4 years.
(Mattocking involves chopping woody vegetation
into small pieces and distributing across the plot.)
The 4 year burn-mattock treatment resulted in the
greatest cyanobacterial cover, the greatest
cyanobacterial biomass and the greatest soil shear
Nutrient cycles are also altered when cryptobiotic
crusts are degraded. Changes include the reduction
of C and N inputs, slowing of the breakdown of
organic matter and a reduction in the nitrogen-fixing
capacity of the soil (Belnap, 1995). The last may
take at least 50 years to recover. In a study (Belnap,
1996) at sites near Moab, Utah, the nitrogenase
activity of crusts dominated by Microcoleus
vaginatus on sandy soils was more susceptible than
crusts with the lichen Collema tenax. Although
disturbance may actually lead to an increase in the
abundance of free-living cyanobacteria, as shown for
sites on the Colorado Plateau (Evans and Belnap,
1999), it leads to a decrease in the abundance of
lichens, some of which are also N2-fixers (Section
II.C), and thus an overall decrease in nitrogenase
activity. Nitrogenase activity was 250% greater at
pristine sites on the Colorado Plateau than at ones
intermittently disturbed 30 years ago. The decrease
in N input from fixation and an enhanced loss of
gaseous N has caused a 25 to 75% decrease in soil N
Although it has been widely considered that crust
communities dominated by cyanobacteria are also
the major source of fixed nitrogen in hotter deserts,
Zaady et al. (1998) showed the importance of
heterotrophic N2 fixation associated with litter
breakdown in the vicinity of vascular plants. For
instance, where macrophyte patches covered 25% of
the soil surface, they contributed 40% of the total N2
fixed in this part of the desert.
4. Heavy Metal and Other Contamination
Cyanobacteria are sometimes abundant on and near
the surface of soils contaminated by various
pollutants or naturally enriched by heavy metals.
Most records for heavy metals are for wastes
associated with lead-zinc mining (Whitton, 1980;
Whitton et al., 1981), but there are also records for
soils rich in copper and other metals (Ernst, 1974;
Rana et al., 1971). The dominants are usually
narrow forms of Oscillatoriaceae such as Plectonema
and Schizothrix and tend to occur mainly at the
surface (Plate 23d). Older communities in Zn-rich
areas develop a mixture of Plectonema and
protonema of species of the moss Dicranella and this
in turn gives rise to intermingled Plectonema and
leafy Dicranella (Plate 23f), and sometimes also
lichens, especially Collema spp. The younger stages
of such communities have many similarities with the
cryptobiotic crusts of semiarid regions (see above),
although they can develop under conditions of high
rainfall. Old sheaths of Plectonema and decaying
parts of the moss appear to play the main role in
developing a true soil on many spoil heaps, though
species of Collema and Peltigera with cyanobacterial
symbionts sometimes occur at these sites and
contribute fixed nitrogen to the ecosystem (author's
There are many records of cyanobacteria tolerating
contamination by oil or perhaps even being favoured
by its presence, though these deal mostly with
shallow waters rather than soil. Several studies have
noted the occurrence of the nitrogen-fixer Nostoc
commune in or on soils naturally contaminated by oil
(tar sands of Alberta: M. Hickman and the author,
unpublished data) or polluted by petroleum products
(e.g. Atlas et al., 1976). The extensive list of
cyanobacteria growing on coal tar reported by
Barhate and Tarar (1982) does not include any
heterocystous forms, but no studies were done to
establish whether any of the species listed were non-
5. Sports Turf
Soil cyanobacteria in golf courses and other amenity
grasslands may reach densities sufficient to have
favourable effects on soil properties, but surface
growths can also be extensive enough to cause
management problems (Baldwin and Whitton,
1992). Two different types of situation have been
recognized. One is where the development of
Nostoc commune colonies is large enough to cause a
risk of people slipping. (Eukaryotic algae are,
however, in general a bigger problem in this
respect.) The other is associated with the
phenomenon of 'black layer', which sometimes
results from unsatisfactory drainage when coarse
sand is used to cover a poorly draining soil. An
anoxic black subsurface layer develops with a
characteristic bacterial community (Lindenback and
In some situations a dark layer including
filamentous non-heterocystous cyanobacteria also
develops at the surface in the region where there is
an underlying anoxic layer (Hodges, 1987a, b). The
arguments concerning the role of cyanobacteria in
this phenomenon are not fully resolved. It has been
suggested that the initial development of surface
cyanobacterial growths as a layer occurs subsequent
to the formation of an underlying anoxic zone. The
presence of cyanobacteria may subsequently enforce
the stability of this underlying zone (Baldwin and
Whitton, 1992), presumably in a similar manner to
that described above by Katznelson (1989).
However, experimental studies by Hodges (1992)
with two Oscillatoria spp., Nostoc sp. and
Desulfovibrio spp. in sand columns showed that
blackening occurred only when cyanobacteria and
Desulfovibrio were both present. Blackening was
most intense in response to added sulphur, chelated
iron or a mixture of the two.
Cyanobacteria were first reported to be abundant in
rice-fields by Fritsch (1907a, c) and their importance
in helping to maintain rice-field fertility due to N2
fixation was suggested by De (1939). Cyanobacteria
are especially evident in wetland rice-fields, which
supply 86% of the world requirement for rice (Ladha
and Reddy, 1995). Many rice-field soils not only
contain a high density of cyanobacteria, but possess
visually obvious growths of cyanobacteria at (or
floating above) the surface, at least during some
seasons. Typically, about half the cyanobacterial
genera present are heterocystous (Anabaena,
Aulosira, Calothrix, Cylindrospermum, Fischerella,
Gloeotrichia, Nostoc, Scytonema, Tolypothrix,
Wollea). However, there is a lack of critical studies
on changes during growth of the rice crop and
Kulasooriya (1998) has stressed how this makes it
difficult to compare results from different sites.
However, general comments can be made when the
data comes from a wide enough range of sites. For
instance, a survey of 102 soils from four countries
showed that the abundance of heterocystous forms
was correlated positively with pH and the available P
content of the soils (Roger et al., 1987), though
nitrogen-fixing cyanobacteria can still be important
in acid rice soils (Kulasooriya, 1991). Mandal et al.
(1993) also showed that the abundance of
heterocystous species in Bangladesh rice-field soils
was significantly correlated with available P in the
The influence of light on cyanobacterial
communities in rice-fields near Valencia, Spain, was
investigated by Quesada et al. (1998). Light had a
significant effect on the relative abundance of the
dominant genera. The abundance of non-
heterocystous forms was three times more at high
than low (about 52% versus 7%) incident irradiation.
The three main heterocystous genera (Anabaena,
Calothrix, Nostoc) all responded differently to levels
of irradiation. Higher abundance of Nostoc
coincided with lower abundance of the other two
genera. The nitrogenase activity of the communities
became adapted to the light regime to which they
had been exposed for the previous month, though the
community exposed to, and subsequently assayed at,
the highest irradiation showed the highest activity.
In view of the many floristic studies on rice-fields,
there have been surprisingly few studies on the
ecology of particular species, though this information
would be useful for assessing the nutrient status of
fields and also how to manage them. A comparison
of the cyanobacterial flora of rain-moistened fields in
Bangladesh (Fig. 1) with that present after the flood
waters had arrived showed that most species were
different (Rother and Whitton, 1989; Whitton et al.,
1989). However, mats of Scytonema mirabile were
sometimes abundant both on the moist soil and
floating in the same field when flooded. Many of the
rice-field species form akinetes, so it would be useful
to know what factors lead to akinete formation in
particular species. A strain of Fischerella muscicola
isolated from a field at the Cuttack Rice Research
Institute formed akinetes under P limitation (Mishra,
1985) as do about half the strains of cyanobacteria
isolated from diverse habitats (Whitton, 1992).
However, not all rice-field species form akinetes in
response to P limitation (Reddy, 1983). A study
(Whitton, 1991) of surface phosphomonoesterase
activity of macroscopic colonies in paddy fields in
the Philippines showed that Aphanothece stagnina
tended to have low activity, whereas Gloeotrichia
always showed high activity. Among Nostoc, N.
commune had high activity, whereas other species
tended to have less activity.
phosphomonoesterase activity is enhanced in all
these species under conditions of P limitation, it was
concluded that Aphanothece typically grew under P-
rich conditions, whereas Gloeotrichia grew under
conditions where growth was P-limited.
Surface application of fertilizers to rice-field soils
without standing water generally leads to
conspicuous growths of algae (Roger and
Kulasooriya, 1980), with cyanobacteria usually
forming an important component unless nitrogenous
fertilizer is in excess. Replacement of the
cyanobacteria as dominants by masses of filamentous
green algae is an indication of high quantities of
nitrogenous fertilizer available at the surface
(Whitton and Roger, 1989). According to Roger et
al., (1980) deep placement of nitrogen fertilizer in
the form of urea supergranules not only prevents the
growth of the green algae, but also prevents the
inhibition of cyanobacterial growth and its associated
N2 fixation. However, Fernndez-Valiente et al.
(1997) found that the highest level of ammonium
fertilizer (140 kg N ha-1) deep-placed in rice-fields
near Valencia, Spain, did lead to a significant
reduction in nitrogenase activity. The partial
reduction in activity increased over the cultivation
cycle, being highest at the end.
It is difficult to assess the impact of P fertilization
on cyanobacteria in rice-fields, because other
fertilizers are almost always added at the same time,
and, even in experimental studies with potassium
phosphate, controls are seldom included to consider
the possible effects of K. However, the highly
significant increases in cyanobacterial biomass
resulting from phosphate addition found by Bisoyi
and Singh (1988) in plots enriched with Aulosira,
Aphanothece or Gloeotrichia was almost certainly
due to added P.
Many studies have been reported on the use of
dried cyanobacteria to inoculate soils as a means of
aiding fertility (Roger and Kulasooriya, 1980:
Metting, 1988). The term 'algalization' was initially
applied to the use of defined mixtures of species
(Venkataraman (1972), but has since come to refer
to any planned addition of material. The effects of
such addition on rice yield were first reported for
Japan by Watanabe et al. (1951), when there was a
25% increase in yield after inoculation of poorly
drained paddy with Tolypothrix tenuis. Studies on
the use of inocula have been discontinued in Japan,
but numerous studies have been made elsewhere,
especially in India (Kaushik, 1998) and more
recently in Egypt (e.g.Yanni, 1992 a, b).
Unfortunately there are no recent detailed accounts
for India in the literature. It has been widely
accepted (Agarwal, 1979; Venkataraman, 1981) that
algalization can lead to gains in yield, though some
of the evidence is equivocal (Whitton and Roger,
1989; Roger et al., 1993). A summary of the results
from all studies to 1980 (Roger and Kulasooriya,
1980) showed that there was a mean increase in
grain yield due to algalization of 28% in pot
experiments and 15% in field experiments. The
authors pointed out that most experiments had been
designed simply to obtain data about grain yield and
little was known about N elsewhere in the ecosystem.
The methodology to prepare inocula was described
by Venkataraman (1981). Cyanobacteria are grown
from March to May (in India) in open-air shallow
tanks, into which farm soil, superphosphate, starter
inocula and sometimes also insectides are added. If
necessary, lime is added to adjust the soil pH to 7.0
to 7.5. A thick cyanobacterial mat develops withing
15-20 days and the contents of the trays are then
allowed to dry, producig flakes which are harvested
for distribution. A tray with a surface area of 1.6 m2
produces sufficient material each season to inoculate
one hectare. Typically the inocula are added one
week after the rice has been transplanted (Sharma
and Gupta, 1983). Roger and Watanabe (1986)
reported that algalization was adopted in only two
states of India and that the inoculated fields
comprised only a few percent of the total area under
Roger (1991) made a statistical analysis of the data
on algalization and concluded that the effects of
inoculation are erratic and limited. He also
suggested that farmers had probably not bothered to
report unsuccessful results. The best results appear
to have been obtained where mixed inocula are
produced from local stocks (Venkataraman, 1981)
and where the inocula are added with reduced or no
nitrogenous fertilizer (Kaushik, 1998, quoting results
from the 1981 All India Coordinated Rice
Improvement Project). Experiments which appear to
have been well designed and the results of which
reported increased straw or grain yield and/or N
content include those of Sharma and Gupta (1983),
Ahmed and Ahmedunnisa (1984) and Singh and
Singh (1985, 1987). Among more recent studies,
Ghosh and Saha (1997) reported that inoculation of
soil during the period when the rice was growing
rapidly with a soil-based mixture of four
heterocystous species led to a significant increase in
soil N and total N uptake by the crop. Although
there was only a small increase in grain yield, N
uptake by the grain increased by 30%.
It is difficult to find data to support the claim by
Agarwal (1979) that the cyanobacteria introduced as
a result of algalization can establish themselves
permanently if inoculation is done repeatedly for 3-4
cropping seasons. The one detailed quantitative
study on what happened to strains following
inoculation is that Reddy and Roger (1988). The
fate of five laboratory-grown heterocystous strains
representing 75% of the inoculum was studied in 1-
m2 plots of five different soils. During the month
following inoculation , the strains multiplied to some
extent in all soils, but rarely dominated the
indigenous cyanobacteria and did so only when the
growth of the indigenous species was poor. The
material was then dried, the natural insecticide,
neem, added to control grazers, and used for
reinoculation. The population changes were
followed for a further two months, when it was clear
that the inoculated strains still played only a minor
A number of studies have to be reported on the
selection of natural or mutant strains with properties
which would in theory maximize the amount of
combined nitrogen available for rice or other plants.
These are either strains showing especially high
rates of nitrogenase activity in laboratory studies or
ones which release much of the nitrogen fixed
extracellularly (Spiller et al., 1986). Although
mutant strains of cyanobacteria releasing ammonia
can lead to transfer of 15N and hence improved
growth of rice in pot experiments (Albrecht et al.,
1991; Kamuru et al., 1997, 1998: see review by
Vaishampayan et al., 1998), it is open to question
whether they can compete effectively with other soil
strains under field conditions. However, one
possible approach is to give the special strains a
competitive advantage under flood conditions by
immobilizing them on polyurethane foam
(Kannaiyan et al., 1997). This study included a field
experiment, the results of which indicated that foam-
immobilized Anabaena azollae excreted considerable
amounts of ammonia into the flood water and that
this led to increased rice grain and straw yields.
(Although the strain was isolated from Azolla,
evidence was not included to confirm that it was in
fact the endosymbiont.) Anabaena strains were also
immobilized on sugarcane waste (bagasse),
suggesting that it might be possible to make the
method economically worthwhile.
Algalization seems likely to be most useful where
there are marked seasonal changes in land use, such
as when the ground is ploughed many times before
planting a winter crop, so that the natural soil
inoculum is much reduced by the time of the new
rice season (Whitton and Roger, 1989). However,
few studies have been made on the fate of
cyanobacteria as rice paddies dry or, subsequently,
during the part of the year when the land is
cultivated for other crops. Kaushik (1998) states
(without references) that in paddy fields the death of
algal biomass is most frequently associated with soil
desiccation at the end of the cultivation cycle. As
most heterocystous species form akinetes, it is
presumably in this form that these species persist
until the next period favourable for growth, which
may not occur until the next paddy crop. Large-scale
mortality of species of Oscillatoriaceae a result of
desiccation would contrast with the ability of
cyanobacteria in many other alternately wet-dry
habitats to survive the dry periods well (Section II
A problem requiring further study is suggested by
the observations of Rice et al. (1980) that decaying
rice straw inhibited cyanobacterial growth and N2
fixation, apparently due to phenolic compounds. In
view of the current interest in barley straw in
controlling cyanobacterial blooms in lakes (Welch et
al., 1990; Gibson et al., 1990; Martin and Ridge,
1999), it is strange that no-one appears to have taken
this study on the effects of rice straw further. On the
one hand it suggests that rice straw might also be
used as an aid for controlling cyanobacterial blooms,
while on the other it suggests that ploughing barley
straw into soils might have an adverse effect on soil
The use of Azolla with its symbiotic nitrogen-
fixing Anabaena (Chapter 14) has been investigated
in many studies (Lumpkin and Plucknett, 1980;
Whitton and Roger, 1989; Kannaiyan, 1992;
Whitton, 1993). The Azolla is used in a variety of
ways. One approach is to add a large inoculum with
irrigation water to fields at an early stage in the rice
crop, leaving the Azolla to grow for a few weeks for
a few weeks, then partially draining the fields and
ploughing the Azolla into the soil. Another
approach is to grow Azolla on its own and then
compost the plants and plough the decaying material
into the soil. Either way, most of the nitrogen fixed
by the symbiont eventually reaches the soil or the
flood water and thus some becomes available for the
rice (Kannaiyan, 1993; Roger, 1996a).
V. Practical Methods
A. Measurement of abundance
Cyanobacterial abundance in soils has mostly been
determined by one or more of three methods - direct
observation, plating techniques and measurement of
pigments (Roger and Kulasooriya, 1980). Direct
counting of soil cyanobacteria has been most
successful where the organisms are frequent. Saito
and Watanabe (1978) reported a quantitative study
where rice-field flood water carrying suspended soil
particles was filtered on membrane filters and a
gelatinized suspension of the particles was smeared
on glass slides. In most circumstances where
quantitative data are required, it is important to
combine direct microscopy with epifluorescence
microscopy, as fluorescence of chlorophyll a makes
it easy to distinguish the smaller cyanobacteria from
bacteria. Combinations of excitation and
suppression filters may be chosen to distinguish the
accessory pigments phycocyanin and phycoerythrin
(Wynn-Williams, 1988), while the fluorochrome
Auramine O can be used to differentiate living from
dead cells. Hawes and Davey (1989) reported that
viable cells of Phormidium fluoresced yellow, while
non-viable cells retained only the red fluorescence.
Cultured material stained much better than field
material, suggesting that this method requires
further development before being put to routine use.
Plating techniques for counting cyanobacteria
depend on the suitability of the chosen medium for
growth of cyanobacteria (Reynaud and Roger, 1977)
and the reliability of the dilution method used. A
general guide on choice of methods for quantifying
soil cyanobacteria is given by Whitton (1996). It
seems probable that most soil cyanobacteria grow
relatively easily if plated on suitable nutrient agar.
The absence of cyanobacteria reported in the
literature for soils of several regions (e.g. parts of
Japan: Watanabe, 1959) was perhaps due to the use
of a culture medium with a higher pH than that of
the soils tested. It would be well worth making an
extensive study of low pH tropical soils using plating
techniques and taking care not only to control the
pH, but also the buffering capacity of the test
Plating techniques may also overlook or
underestimate the abundance of particular species at
a site unless a wide enough range of temperatures is
tested. The need for this is shown by a study of a
single soil sample (total of 0.7 g dry wt) from a dry
rice field in the Iraqi marshes (Al-Mousawi and
Whitton, 1983). Use of a temperature gradient plate
permitted enrichment cultures to be grown over the
range 20° to 50°C. Forty-two species were found,
with 28 cyanobacteria and 14 eukaryotic algae, but at
no single temperature were more than two-thirds of
the species observed. There were marked differences
in the temperature at which particular species
predominated in the mixed community and these
values sometimes differed from the optimum for
unialgal or axenic cultures of the same species.
Substantial growth of a mixed cyanobacterial
community occurred at 45°C, but none at 48°C.
Similar care should be taken to employ a range of
light conditions during plating studies.
To enhance the reproducibility of counts, it may be
necessary to homogenize the soil sample, though this
leads to its own problems. Some species exist
typically as aggregates and/or colonies tightly held
together with mucilage, making them difficult to
disrupt without damaging many cells. Filamentous
forms may be broken into smaller units and, in the
case of some moniliform filaments, quite easily into
individual cells (Roger and Kulasooriya, 1980),
though probably with some loss of cell viability.
Other filamentous forms, such as most
Oscillatoriaceae, are very difficult to separate into
individual cells. As a result the extent to which the
colonies developing on agar reflect individual
colonies, aggregations, filaments or cells in nature is
influenced heavily by the homogenization and
dilution methodology. If accurate cell counts are
required, it is often essential to combine direct
counts for some species with plating techniques for
others. However, P. A. Roger and co-workers have
shown (e.g. Reddy and Roger, 1988) that useful
comparisons can be made based on counts of colony-
forming units (CFU) estimated by plating
techniques. A survey of the literature (Roger et al.,
1987) showed that the CFU of nitrogen-fixing
cyanobacteria in rice-field soils range from 10 - 107
g-1 dry weight of soil, with a mean of 2.5 x 105.
A further problem in interpreting the data
concerning CFUs on an agar surface results from the
fact that many cyanobacteria rapidly undergo cell or
filament division on transfer to nutrient-rich media
(Whitton, 1992). The release of motile hormogonia
is frequent. In some cases (e.g. Calothrix) these
show a tendency to aggregate, whereas hormogonia
from Nostoc move some distance from the original
source and each one develops a new colony.
Nevertheless, a number of interesting studies have
been reported based on CFUs. Kaushik (1991,
reproduced in Kaushik, 1998) compared the numbers
of units of potential nitrogen-fixing cyanobacteria in
soils from 11 sites in Sri Lanka. The values ranged
over three orders of magnitude, the highest being
almost 107 CFUs g-1 dry soil. Roger and Reynaud
(1976, 1977) used plating techniques to quantify
biomass in Senegal rice-field soils by determining
the mean volume of the 'count unit' (colony, filament
or cell) for each species. This involved direct
examination of the first dilution and then
multiplying the CFU counts by the corresponding '
volume unit'. Quantitative data on CFUs are
especially valuable when trying to assess changes
taking place as a result of algalization (Section IV),
as done by Reddy and Roger (1988) in the
comparison of changes in populations of inoculated
and indigenous cyanobacteria in rice-field
microplots. Pigment analysis is useful for
quantifying surface growths dominated by
cyanobacteria (Davey, 1988; Rother and Whitton,
1989), but is less suited for sparse populations
dispersed throughout the upper part of the soil
column. Cores or other types of sample have usually
been frozen until required for analysis in order to
avoid pigment degradation; this also maximizes
extraction efficiency (Hansson, 1988); useful
practical details are given by Stal (1988). The use of
television image analysis with epifluorescence
microscopy for cyanobacteria and other
microorganisms in Antartic fellfields has been
described in detail by Wynn-Williams (1988, 1990).
If it is important to relate a process such as N2
fixation to biomass, chlorophyll a (Garcia-Pichel and
Castenholz, 1991) is usually the only variable easy to
quantify in mixed samples, though it may be possible
to obtain simultaneous measurements of chlorophyll
a and dry weight for a few samples. Otherwise,
some indication of dry weight may be obtained by
using values from laboratory studies in the literature.
Islam and Whitton (1992a) reported that the
chlorophyll a content of a rice-field Calothrix in
batch culture ranged from 0.25 - 2.8 % dry weight.
Values above 1% only occurred for a short period
when cellular P was at its maximum (Islam and
Whitton, 1992b). In the absence of other data a
value of 0.5% dry weight can be used as an
approximate estimate for healthy field material,
though this is open to considerable error.
Satellite sensor images provide a completely
different approach to quantifying surface crusts, as
was found during collection of data for a 'normalized
difference vegetation index' in semiarid areas of
Israel (Karnieli et al., 1996). This led to the use of
the unique spectral features of the phycocyanin in the
cyanobacteria present in the crusts to develop a
spectral crust index for semiarid regions and the
suggestion that the approach could be extended to
agricultural lands (Karnieli, 1997).
B. Nitrogen Fixation
Nitrogen fixation has been quantified in many
cyanobacterial dominated soils and subaerial
communities (Sections IIC, IID). An overview for
rice fields was provided by Roger and Ladha (1992)
and the application of standard methods to
cyanobacterial studies has been described by Mague
(1978) and Stal (1988). In the case of 15N2
measurements, Mague recommended that assays
should be made for 30 - 120 min, depending on the
rates of N2 fixation expected; most studies have used
7-ml serum bottles or similar for the incubation
studies. For measurements of nitrogenase activity
using the acetylene reduction assay methodology, a
variety of transparent containers have been employed
for measurement of soil nitrogenase activity, such as
plastic bags (Yoshida, 1984), perspex cylinders
(Reddy and Roger, 1988), glass jars, universal bottles
or serum bottles incubated at an angle (Rother and
Whitton, 1989). Larger containers are needed if it is
essential to maintain the structure of the upper part
of the soil column. An assay period of 1 h was found
suitable for soil communities in the subtropics
(Rother and Whitton, 1989).
Because of the greater nitrogenase activity shown
by most species in the light than in the dark,
quantitative studies related to field conditions should
ideally be carried out in situ over 24-h periods
(Rother et al., 1988), although this has been done in
relatively few studies. Measurement over a 24-h
period requires a series of experiments, each carried
out over short periods. Because of the heterogeneity
of the cyanobacterial communities associated with
many soils (Fig. 1), quantitative data often needs a
high number of replicates, so biomass needs to be
quantified by a simple method. Chlorophyll a is the
usual variable chosen for this purpose (see above).
C. Assays for Fertility and Toxicity
A methodology for using algae to assess the nutrient
status of soils was developed by Tchan (1959; Tchan
et al., 1961) long before a similar approach was used
for water. This made use of a mixed inoculum,
though apparently mostly green algae. However,
Nostoc commune was selected by Pederson and
Shubert (1992) for assaying the toxicity of substances
likely to contaminate soil. This involves growing the
organism on membrane filters superimposed on the
surface of nutrient agar containing various
concentrations of the substance under test; this
technique maintains the air-solid interface important
for many soil surface cyanobacteria. Presumably the
method could be modified such that the membrane
with the Nostoc colony is placed directly on the
surface of a soil sample.
VI. Concluding Comments
This review has covered much less than half the
literature in mainstream journals and widely
available reports and no doubt important topics have
been overlooked. More than most aspects of the
ecology of cyanobacteria, there is still much of
interest in the older literature, though this needs to
be read critically in the light of modern studies. The
real insight into the subject, however, has come
largely from the few research groups that have both
treated taxonomic identification as a serious matter
and have adapted well-known research techniques to
quantify organisms and processes occurring in or on
soils. Reliable identification has been hindered by
the lack of availability of the one book in English
(Desikachary, 1959), which might have benefited
people at the many institutes and colleges with
limited access to the literature. The production of a
good and cheap identification manual for soil and
rice-field studies in the tropics and subtropics would
greatly improve the situation.
Most quantitative studies have dealt with only one
process, nitrogen fixation, combined with some
measure of biomass, usually chlorophyll a. This is
partly because of the possible or known importance
of the contribution by cyanobacterial nitrogen
fixation in many ecosystems, but also because of the
relative ease of measuring nitrogenase activity using
the acetylene reduction assay methodology.
Unfortunately, most studies on nitrogen fixation
have at best been fragmentary and seldom attempted
to quantify the process over a whole season. Only a
few studies have combined measurements of carbon
dioxide and nitrogen fixation. Nevertheless, many of
the techniques used for measuring processes and the
microenvironment in marine mats (Chapter 4) can
be applied to the more distinct soil cyanobacterial
communities, as shown by Garcia-Pichel and Belnap
(1996) for desert crusts.
Some of the equipment needed for measuring
processes and the microenvironment is relatively
specialized and unlikely to become available to
everyone working on soil cyanobacteria. However,
the techniques for counting colony-forming units
developed by P.A. Roger, initially with ORSTOM in
West Africa and later at IRRI (International Rice
Research Institute), are less demanding and can be
applied anywhere there is an autoclave and a good
microscope. They can produce results which provide
considerable insight on the influence of
environmental factors and seasonal changes in
populations, as shown by the research group at IRRI
during the 1980s and since then by some of the
people who have moved from there, such as S.A.
Kulasooriya in Sri Lanka. The lack of quantitative
studies on population dynamics of cyanobacteria in
rice-field and other soils, however, still applies in
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