J.
P ~ J c o31,
~ . 2-18 (1995)
REVIEW
THE ECOLOGY OF NOSTOC
Walter K. Dodds, Dolly A. Gudder
Division of Biology, Kansas State University, Manhattan, Kansas 66506
and
Dieter Mollenhauer
Forschungsinstitut Senckenberg, AuBenstelle Lochmiihle, D-63599 Biebergemund-Bieber, Germany
ABSTRACT
Nostoc is a genus offilamentous cyanobacteria that
can form macroscopic or microscopic colonies and is com-
mon in both terrestrial and aquatic habitats. Much of the
success o f Nostoc i n terrestrial habitats is related to its
ability to remain desiccatedfor months or years and fully
recover metabolic activity within hours to days after re-
hydration with liquid water. Nostoc can also withstand
repeated cycles of freezing and thawing and, thus, is a n
important component of extreme terrestrial habitats in the
Arctic and Antarctic. The ability to j i x atmospheric N,
can provide a n advantage in nitrogen-poor environments.
Nostoc also has the ability to screen damaging ultraviolet
light in terrestrial and shallow benthic habitats. Thegenus
potentially could be important in paddy rice culture be-
cause itfixes nitrogen that may later be released and used
by plants; it also may play a role in soil formation and
may increase nitrogen input to natural aquatic and ter-
restrial ecosystems. The abilities to survive in terrestrial
habitats and fix N , are important in symbiotic interactions
with fungi (lichens), liverworts, hornworts, mosses, ferns,
cycads, and the angiosperm Gunnera. Nostoc is some-
what resistant to predation; this probably is related to
production of large amounts o f sheath material, synthesis
o f microcystin-like toxins by some strains, and formation
ofcolonies that are too largefor many algivores to consume.
Some organisms can subsist on Nostoc, although it may
not be a preferred food source. Lytic cyanophages also
infect Nostoc, but little is known about population control
of Nostoc in its natural environment, Late Precambrian
fossils resembling Nostoc have been described, and Nos-
toc possibly has been a n important component of many
terrestrial and aquatic communities since that time.
Key index words: desiccation; ecology; mutualism; nitro-
gen fixation; Nostoc; reproduction; symbiosis; systematics
The genus Nostoc Vaucher 1803 ex Bornet & Fla-
hault 1888 is one of the most widespread photo-
trophic taxa known. It is found in fresh waters, in
terrestrial systems, on tropical soils, and in both north
and south polar zones (Vincent 1988).Arboreal spe-
cies have been recorded, and Nostoc can be cultured
using atmospheric particles as a source of inoculum
(Singh 198I). As a heterocystous, nitrogen-fixing
2
cyanobacterium, Nostoc may maintain soil fertility in
many terrestrial systems, including rice paddies
(Rother and Whitton 1989). Its abilities to photo-
synthesize, fix atmospheric nitrogen, survive in ter-
restrial habitats, and disperse via hormogonia (mo-
tile trichomes) also have played roles in the formation
of symbioses. Nostoc-containing lichens can be the
dominant primary producers in some landscapes
(Seaward 1988). The taxon may be ancient; fossils
formed in late Precambrian, shallow, marine sedi-
ments are very similar to Nostoc (Weiguo 1987), and
fossils resembling filamentous cyanobacteria that
could be as old as 3.4 billion years have been de-
scribed (Schopf 1993).
Nostoc is both useful and a nuisance to humans.
Some species are regionally popular edible delicacies
(e.g. Emralino and Rodulfo 1987). Nostoc can be a
nuisance on sport turfs (Baldwin and Whitton 1992),
can cause unpleasant odors in drinking water (Moh-
ren and Jiittner 1983, Wnorowski 1992), and can
foul buildings (Whitton 1987). Human pathogens
(fungal and bacterial) are inhibited by phenolic ex-
tracts from Nostoc (de Can0 et al. 1990); it is possible
that Nostoc someday may provide biotechnologists
with unique medicinal compounds. Nostoc commune
has been shown to lower cholesterol in the serum
of rats (Hori et al. 1994) and, thus, has the potential
to become a “health food.”
Given the extreme diversity of interspecific inter-
actions of the genus, its relationship to human af-
fairs, and its importance in such a wide variety of
habitats, the publication of research on the ecology
of Nostoc found in many different types of journals
is not surprising. Extensive information on the his-
tory of studies of Nostoc, with special reference to
the European literature, can be found in Mollen-
hauer (1985a, b, 1986a, b). Our review attempts to
synopsize the diverse literature as it relates to ecol-
ogy with emphasis on physiological ecology, species
interactions, and ecosystems.
Systematics
Nostoc is a cyanobacterium (cyanophyte). Molec-
ular, physiological, and morphological characteris-
tics clearly indicate that it is prokaryotic, not a eu-
 NOSTOC ECOLOGY
karyotic alga. However, the fact that Nostoc and other
cyanobacteria (blue-green algae) exhibit oxygenic
photosynthesis and contain chlorophyll has led to
traditional systematic treatment by phycological tax-
onomists. More modern approaches are based al-
most entirely upon characteristics of pure cultures
of cyanobacteria and, rather than a specific epithet,
a strain number commonly is used. This system con-
tinues to receive broader application (Castenholz
1992). However, Mollenhauer (1 988) noted that
Nostoc with different colony morphologies collected
in the field often will yield distinct cultures as well;
thus, all data based on the morphotype of field ma-
terial are not necessarily useless.
Nostoc is filamentous, forms trichomes that are en-
cased in a sheath, generally divides by binary fission
in one plane only, and does generally not exhibit
true branching (Castenholz 1989), but branching
can occur (Mollenhauer 1970). Heterocysts and ak-
inetes are formed, and reproduction occurs by short,
motile trichomes (hormogonia). Detailed descrip-
tions of the different cell types and their relationship
to Nostoc systematics can be found in Mollenhauer
et al. (1994). T h e numerous trichomes often form
gelatinous aggregates or colonies, apparently of two
types. Some species of Nostoc form a mature colony
of trichomes entirely within a firm surface pellicle,
whereas others form looser colonies. Nostoc also may
be common in nature in the less obvious form of
single filaments (Mollenhauer 1986b), but little in-
formation is available on this topic.
T h e smallest colonies can consist of several tri-
chomes, but spherical colonies of up to 2.6 kg wet
weight have been described (Fig. l), and mat-like
colonies have been found up to 60 x 30 cm in size
(Smith 1933). English names for species of the genus
include “mare’s eggs” and “shot stars” (Dodds, pers.
observ.).
Data from 16s ribosomal RNA (rRNA) sequences
imply that Nostoc and other filamentous cyanobac-
teria originated from the “Synechocystis” rRNA
group; Synechococcus and the progenitors of chloro-
plasts were derived earlier from the same group
(Bonen et al. 1979). A mutant of Nostoc muscorum
Agardh exhibited true branching (Razdan and
Dikshit 1983), and true branching was reported by
Mollenhauer (1970), indicating an affinity t o
branching cyanobacteria. More recent analysis of
16s rRNA sequences showed that Nostoc shares phy-
logenetic affinity with other heterocystous cyano-
bacteria and that its ability to form hormogonia arose
fairly early (Giovannoni et al. 1988, Wilmotte and
Golubic 199 1).
T h e genus Nostoc is probably monophyletic, based
on DNA-DNA hybridization experiments (La-
chance 198 1) and comparison of cultured materials
(Rippka et al. 1979), but is related closely to Ana-
baena. Nostoc generally produces aggregated fila-
ments, whereas Anabaena produces isolated fila-
ments. Some studies have suggested that hormogonia
3
FIG. 1. Nostocpruniformr, a 2.6-kg wet weight colony collected
from Mare’s Egg Spring, Oregon. Results from growth experi-
ments indicate that the colony is between 9.4 and 14.3 years old
(Dodds and Castenholz 1987).
usually are produced by Nostoc but not by Anabaena
(Rippka et al. 1979, Castenholz 1989). However,
some strains of Nostoc (e.g. Nostoc MAC) are prone
to losing the ability to form hormogonia in culture
(J. Meeks, pers. commun.), and species of Anabaena
can form hormogonia upon germination of akinetes
(Braune 1980). Lack of hormogonia formation is
probably not a definitive systematic characteristic.
T h e basic characteristics of Nostoc are 1) well-de-
veloped hormogonial phases in the life cycle, often
rather long; 2) terminal heterocysts developing from
terminal hormogonial cells after settling and ces-
sation of movement; and 3) akinetes developing by
differentiation of one vegetative cell midway be-
tween t w o heterocysts, followed by “centrifugal”
formation of additional akinetes. T h e latter is the
main distinguishing difference from Anabaena (Ko-
mirek and Anagnostidis 1989).
Preliminary data on a cyanobacterial myoglobin
found in Nostoc commune (Potts et al. 1992) suggest
that myoglobin may serve as a biochemical marker
to distinguish Nostoc species related t o N . commune
from Anabaena and some Nostoc species less closely
related to N. commune (M. Potts, pers. commun.).
T h e genus Anabaena may contain some species that
should be reassigned to the genus Nostoc (Lachance
1981), including Anabaena azollae Strasb. (Meeks et
al. 1988, Peters and Meeks 1989, Peters 1991, Vag-
noli et al. 1992).
Distribution
Nostoc is distributed widely. In terrestrial systems,
the most common species reported are N . muscorum
and N . commune Vaucher (e.g. Jurgensen and Davey
1968). Colonies have been found from the extreme-
4 WALTER K. DODDS ET AL.
ly cold and dry habitats of Antarctic valleys (Potts
et al. 1987, Vincent 1988) and the Arctic, to hot
desert soils around the world (Johansen et al. 1983,
Budel and Wessels 1991, Arif 1992, Lange et al.
1992, Johansen 1993). Nostoc microscopicum (Carmi-
chael) Harvey ex Bornet & Flahault has been found
at a horizontal distance of 25 m from the entrance
of a large sandstone cave (Budel et al. 1993).
Seasonally inundated habitats (wetlands or estu-
aries) are suitable to Nostoc, where it may succeed
partially because of its ability to withstand desicca-
tion. Some summer meltwater streams in the Ant-
arctic are dominated by Nostoc spp. (Vincent and
Howard-Williams 1986, Vincent 1988). Estuaries
have cyanobacterial mats that can include Nostoc
(Maples 1982, Tracy and South 1989), although the
salinity at the microhabitat level in these cases is not
certain. Rice paddies, which are among the most
widespread types of tropical and subtropical wet-
lands in the world, commonly feature Nostoc spp.
when they are inundated (Stewart 1973). Nostoc com-
mune dominates the vegetation of shallow temporary
pools on limestone rocks from the tropics to polar
regions (Whitton and Sinclair 1975, Whitton 1992).
In aquatic environments, Nostoc is associated pri-
marily with the benthos but can form floating plank-
tonic masses (e.g. Joshi et al. 1981). Nostoc parme-
lioides and N . verrocusum attach to the benthos and
can be found over a wide geographic area in North
America (Sheath and Cole 1992) and the world. T h e
geographic distribution of Nostoc prunijorme Agardh
shows that this species is on all continents except
Australia and Antarctica (Mollenhauer 1970). T h e
lack of N . prunijorme in Australia and Antarctica is
probably accurate. T h e distribution map shows the
greatest occurrence in western Europe, an area that
coincidentally has a high concentration of univer-
sities with a long tradition of scholarly activity by
systematists. It is likely that distribution maps of
other species also would show a correlation between
collection sites and research universities. Nostoc mus-
corum may occur in hot springs (Greenwood and Steen-
bergen 1976), and N. prunijiome grows in water that
is constantly 4" C (Dodds and Castenholz 1987). Nostoc
has been reported in many lentic habitats including
(but not limited to) the benthos of ultra-oligotrophic
lakes (Reuter et al. 1983), swimming pools (Adamson
and Sommerfeld 1978), high-altitude Kenyan lakes
(e.g. D'hollander 1977), Antarctic lakes (Allnutt et al.
198 1, Vincent 1988), Antarctic streams(Vincent 1988),
and Icelandic lakes (Jbnsson 1987).
Reproduction
Nostoc is able to reproduce in several ways. 1) Sin-
gle cells of N . commune fragmented from filaments
can form new colonies. 2) Akinetes are resistant cells
that can disperse. 3) Hormogonia disperse and form
new colonies. 4) Large colonies can grow small at-
tached colonies (proliferations) that break off and
become separate colonies (e.g. Dodds and Casten-
holz 1987).
Considerable research has been conducted on ak-
inete formation, survival, and germination (see
Whitton 1987 for discussion of akinete formation
in cyanobacteria). In some species of Nostoc, all cells
in a trichome except heterocysts can form akinetes,
whereas in others, akinetes are never formed (no-
table in N . commune, an extremely desiccation-resis-
tant terrestrial species, Whitton 1987). Polyphos-
phate bodies disappear prior to akinete formation
in Nostoc linckia (Reddy 1983). This has been inter-
preted to suggest that phosphorus depletion may
play a role in akinete formation, but not all strains
of Nostoc sporulate with phosphorus deficiency. Ak-
inetes form from vegetative cells farthest from the
heterocysts in some strains of Nostoc (Whitton 1987).
This is interesting, because akinetes generally form
adjacent to heterocysts in the closely related Ana-
baena. Inorganic nitrogen inhibits formation of ak-
inetes in an unidentified species of Nostoc (Ahluwalia
and Kumar 1982). Combined with the observation
that akinetes form away from heterocysts, this sug-
gests that nitrogen deficiency within the trichome
initiates akinete formation in Nostoc. Further re-
search is required to establish this relationship.
Akinetes remain viable when separated from the
vegetative cells and may allow Nostoc to disperse aeri-
ally (Bhagawan and Pande 1988). Akinetes respire
at about one-fourth the rate of vegetative cells, can
photosynthesize at about one-sixteenth the rate of
vegetative cells, and incorporate SO,s+ into protein
and lipid, even before germination in Nostoc spon-
giaeforme Agardh (cultured from the field) (Thiel
and Wolk 1983). T h e akinetes do not appear to be
able to germinate in a medium in which sporulation
has occurred, and sporulation (akinete formation)
also is inhibited by compounds produced by the ak-
inetes themselves. Thiel and Wolk (1982) hypoth-
esized that this inhibition may be beneficial, because
germination can occur only when conditions for sur-
vival improve (when the inhibitory chemicals are
diluted by fresh water) or only when akinetes are
sufficiently dispersed. Light activation of C-phyco-
cyanin also may be prerequisite to akinete germi-
nation (Braune 1979).
When akinetes germinate (from Nostoc that was
originally cultured from cycad roots), cells rapidly
synthesize DNA (Favali and Caiola 1986), and RNA
synthesis starts within 1 h (Caiola and Favali 1982).
Sutherland et al. (1 985) similarly showed that Nostoc
PCC 7524 starts DNA and RNA synthesis within 1
h after germination. In addition, protein synthesis
began within 5 h, phycocyanin synthesis within 10
h, and chlorophyll synthesis and nitrogen fixation
within 20 h. Nitrogen fixation in the light is rees-
tablished only upon formation of heterocysts, which
occurs first at about 20 h in three-celled trichomes.
If germination occurs in a nitrogen-free medium,
heterocyst frequency can be as high as 35-40% in
 NOSTOC ECOLOGY
Nostoc PCC 6720 (Skill and Smith 1987). Presum-
ably, this frequency would decrease as trichomes
increase in length by vegetative cell division.
Extensive laboratory research has been conducted
on the formation of hormogonia and the develop-
ment cycle of Nostoc (Lazaroff 1973). Light control
is known to be important in their formation (Rob-
inson and Miller 1970). T h e action spectrum for
photoinduction of development from hormogonia
in dark-grown cells of Nostoc muscorum Agardh shows
a peak at 650 nm. T h e action spectrum for photo-
reversal of development peaks at about 500 nm (Laz-
aroff 1973). A midge larva (Cricotopus nostocicola)as-
sociated with Nostoc parmelioides Kutzing also may
initiate formation of hormogonia (Dodds and Marra
1989), as has been demonstrated for plant metab-
olites (Campbell and Meeks 1989).
It is possible that hormogonia not only disperse
but also, through chemotactic or phototactic re-
sponses similar to those common in motile cyano-
bacteria (e.g. Castenholz 1982), move to locations
more favorable for colony growth. Nostoc in Ant-
arctic moss beds moves into lighted portions of the
bed by means of hormogonia (Vincent 1988). Some
hormogonia, such as those of N. muscorum, not only
glide on solid substrates (Castenholz 1982) but also
form gas vesicles (Armstrong et al. 1983, Castenholz
1989). These vesicles probably allow species in
flooded soils to disperse more rapidly, although
studies have not shown this directly. T h e gas vesicles
are formed in response to lowered ionic concentra-
tions, consistent with conditions that occur when
soils are inundated with rain water (Armstrong et
al. 1983). Gas vesicle formation in hormogonia is
the normal condition in Nostoc prunforme (Mollen-
hauer 1970).
Fragmentation of colonies or budding also may
allow for reproduction. Nostoc cordubensis Prosperi
can reproduce by forming small buds that become
new colonies, or if the parent colony ruptures, frag-
ments containing trichomes and mucilage can form
new colonies. Low light seems to initiate budding
(Prosperi 1989). Nostoc prunforme also forms nu-
merous small buds in the field (Mollenhauer 1970,
Dodds and Castenholz 1987), and we have seen large
colonies break and deteriorate, leaving numerous
small colonies behind.
Physiological Ecology
Moisture. T h e ability of some strains of Nostoc to
withstand desiccation probably is crucial for success
in a variety of terrestrial habitats. This cyanobac-
terium, and others, can survive desiccation (Whitton
1987, Tomaselli and Giovannetti 1993), and phys-
iological activities such as photosynthesis and nitro-
gen fixation resume fairly soon after rewetting. One
case is known of a dried herbarium specimen grow-
ing when rehydrated after 107 years of desiccation
(Cameron 1962). This ability of Nostoc and other
5
cyanobacteria to withstand drying has been the sub-
ject of numerous investigations (see review by Whit-
ton 1987). Although Nostoc can recover function
after drying, rehydration with liquid rather than
atmospheric water (Lange et al. 1992) appears to be
necessary.
T h e initial problem encountered as water evap-
orates is osmoregulation. Nostoc muscorum 7 119 ac-
cumulates sucrose in response to increased NaCl and
can grow in media containing up to 0.2 M NaCl
(Blumwald and Tel-Or 1982). This mechanism is
shared by widely divergent species of cyanobacteria,
but some strains in the Anabaena/Nostoc group use
different organic solutes to regulate osmotic pres-
sure (Stal and Reed 1987). Salt stress increases ab-
scisic acid in Nostoc and other cyanobacteria. Abscisic
acid is important in desiccation tolerance of some
higher plants, but its role in cyanobacteria is not
known (Hartung and Gimmler 1994).
As drying occurs, nitrogenase activity is lost be-
fore the adenosine triphosphate (ATP) pool in Nos-
toc commune UTEX 584 (Potts et al. 1984), possibly
because 0, can readily invade the drying cells and
inactivate the nitrogenase. DNA is modified with
drying as evidenced by an alteration in the staining
properties of the nuclear region with acridine or-
ange (Mel’nikova 1985). When desiccation occurs in
the light, “nicks” in the DNA of N . commune UTEX
584 are observed (Stulp and Potts 1987) that do not
appear in the dark. After 24 h of drying, little change
occurs in messenger RNA (mRNA) pools, but after
5 years of desiccation, pool sizes of a field-collected
N. commune are considerably reduced (Jager and Potts
1988). Unique proteins are synthesized by field-col-
lected N . commune upon repeated desiccation, and
presumably these proteins increase desiccation tol-
erance (Scherer and Potts 1989). Changes in phos-
pholipid fatty acid profiles accompany drying, with
similar changes observed in N . commune colonies col-
lected from China, Germany, and Antarctica. Cel-
lular organization of N. commune UTEX 584 is pre-
served at the ultrastructural level, as indicated by
electron microscopy (Peat and Potts 1987) and im-
munogold labeling of nitrogenases (Peat et al. 1988).
Rehydration brings rapid recovery of metabolic
function (Table 1). Although many of the studies
used field material (as opposed to more reproducible
work using established laboratory cultures) and do
not carefully report controlled conditions of the
dried Nostoc (e.g. humidity of storage conditions),
some general trends emerged. T h e first metabolic
activities to recover are synthesis of ATP, glycogen,
and mRNA. This recovery generally occurs in less
than 30 min. Positive net photosynthetic rates often
are measurable within an hour and increase over
the 10-24 h following wetting. Nitrogenase activity
recovers more slowly, with several hours of lag be-
fore activity is measurable, and maximal rates are
reached in a day or more. T h e lag times increase as
the desiccation period increases (Fig. 2C). Repeated
6 WALTER K. DODDS ET AL.

1. Metabolic recovery of Nostocfollowing rehydration.

TABLE
Strains/species, Dehydration
collection location length Response Rcfemnm

N . commune UTEX 584
N . commune UTEX 584
N . commune, field, Hunan,
China
N . commune, N . sphaericum,
field, Aldabra Atoll, Indian
Ocean
N . commune, field, Tarn Moor,
England
N . commune UTEX 584
N . commune, N . jlagellifrme,
Nostoc sp., field, China
N . commune, N . jlagell forme,
field, China, Germany
Nostoc commune, field, Hunan,
China
Nostoc commune, field Wuhan,
China
Nostoc commune, field, Alberta,
Canada
24 h Messenger RNA pool does not change from predesic- JSger and Potts 1988
cation composition.
days? Lipid synthesis within hours. Taranto et al. 1993
5 years Low levels of in vitro translation associated with JPger and Potts 1988
mRNA extracted from desiccated material.
1 year Twelve-hour time lag before significant nitrogenase Whitton et al. 1979
activity, constant rate after 24 h, 80% water satura-
tion within 5 min (N.commune) or 1 h ( N . sphaeri-
cum).
several days? Less than 3-h time lag before nitrogen fixation rates Whitton et al. 1979
reach steady state, 10 h to reach 80% water satura-
tion.
2 days Nitrogen activity after 4 h, constant rate after 8 h. Potts and Morrison 1986
ATP resynthesized in minutes.
2 years Rewetted within 10 rnin (N. commune) or 3-4 h (N.p a - Scherer et al. 1984
gellijiorme, N o s h sp.). Respiration rates reach maxi-
mum by 20 min. Full recovery of photosynthesis in
500 min, some photosynthetic activity within 20 min
(N. commune) to 100 min (N. flagellijorme). Nitroge-
nase activity in N. commune measurable after 5 h, re-
covered to maximum in 4-5 days (see Fig. 2).
2 months-5 Dry samples have low ATP, high ADP. Within 6 h, Scherer et al. 1986
years adenine pools recover, with recovery rates in N . p a -
gellijorme similar in material dry for 6 months and 5
years.
2 years Fe protein of nitrogenase (NifH) remains undegraded Peat et al. 1988
and is immunolabeled in discrete areas 5 min after
cells are rewetted.
< I year? Glycogen doubles within 4-6 h; most of carbohydrate Ernst et al. 1987
present in dry samples postulated to be sheath mate-
rial.
< 1 year? Detectable nitrogenase activity after 1 h, still increas- Coxson and Kershaw
ing after 12 h. 1989

desiccation may increase desiccation tolerance
(Scherer and Zhong 1991).
The ability to metabolize rapidly after extended
desiccation periods is probably a necessity in terres-
trial environments for an organism that has no way
to access belowground reserves of moisture. The
ability to withstand desiccation is not an exclusive
property of Nostoc (Whitton 1987). Other hetero-
cystous forms (Scytonoma, Fischerella) tolerate desic-
cation as well as or better than Nostoc (Tomaselli and
Giovannetti 1993). The feature that may lead to so
much interest in Nostoc rehydration is the dramatic
rehydration of conspicuous macroscopic colonies in
terrestrial systems soon after rain. We should note
that not all species of Nostoc are desiccation-tolerant.
We have observed the degradation of colonies of
Nostoc prunifOrme that were rewetted following only
a few days of atmospheric exposure.
Temperature. Species of Nostoc rapidly recover
physiological abilities upon thawing, with nitroge-
nase activity detected within 6 h after thawing at
25" C and 12 h at <20" C (DuBois and Kapustka
1983). The ability to withstand freezing may be
linked to desiccation survival because both involve
osmotic stress and decreased availability of liquid
water (Hawes et a]. 1992). Avoiding damage from
ice crystal formation is also necessary. Photosynthe-
sis has been documented at -1" C for N. commune
collected in the Antarctic (Becker 1982). One strain
of N . muscorum may survive at 60 k 5" C in hot
springs (Greenwood and Steenbergen 1976) (sur-
vival of Nostoc at such high temperatures has not
been confirmed by any other researchers; R. W.
Castenholz, pers. commun.), whereas another strain
of the same species cultured grew at 45" C but died
at 48" C (Al-Mousawi and Whitton 1983).
Nutrition. Some strains of Nostoc may be faculta-
tively heterotrophic. About two-thirds of the 13 Nos-
toc strains tested by Rippka et al. (1979) were able
to grow on glucose, fructose, ribose, or sucrose.
Huang and Chow (1988) tested 18 strains of the
genus for dark growth on sugars, combined nitro-
gen, and yeast extract, and only five did not grow.
The five that failed to grow in the dark also did not
exhibit nitrogenase activity in the dark, even in the
absence of combined nitrogen. Some organic com-
pounds (a-ketoglutarate, pyruvate, ribose, succi-
nate, acetate, sorbose, and formate) were shown to
inhibit chemoheterotrophic growth of Nostoc linckia
Roth, but glucose, fructose, and sucrose supported
growth (Mishra et al. 1985). When some strains of
Nostoc are grown in the dark on sugars, they form
aseriate packets (Lazaroff 1973).
Nostoc is able to use a variety of nitrogen sources
 NOSTOC ECOLOGY
including inorganic nitrogen (NO,-, NO,-, and
NH4+), amino acids (established by Vaishampayan
1982 with non-nitrogen-fixing mutant strains of N .
muscorum) and N, gas. T h e ability to fix N, gas
allows the genus to be successful in many environ-
ments low in combined nitrogen.
Several factors influence the rate of nitrogen fix-
ation. Temperature is important, with measurable
fixation rates by terrestrial N . commune sustained at
very low temperatures (Davey and Marchant 1983),
and activity increasing with temperatures up to 35"
C (Coxson and Kershaw 1983). Moisture also con-
trols rates of N, fixation of N . commune in mixed
grass prairie (Coxson and Kershaw 1983) and Nostoc
sp. in tallgrass prairie (DuBois and Kapustka 1983).
Increased day length (in Nostoc muscorum isolated
from an estuary, Yunes et al. 1990) and lack of cloud
cover (in Nostoc sp. from a California stream, Horne
1975) lead to increased rates of nitrogen fixation.
Ammonium additions lower nitrogen fixation rates,
but nitrate has little effect on N . muscorum 1453/12
(Rodgers 1982).
Michaelis Menten kinetic parameters for ammo-
nium uptake by Nostoc calcicola Brkbisson are V, =
41.0 nmol NH,+.mg protein-'.min-' and K, = 10
p M NH,+. This value for K, is 5-50 times higher
than values for mixed phytoplankton assemblages
from N-deficient conditions (Dodds et al. 1991) and
is similar to values reported for planktonic cyano-
bacteria from eutrophic lakes (Goldman and Horne
1983). Possibly, the species typical of oligotrophic
systems have a higher affinity for NH4+,or the abil-
ity to fix atmospheric N, makes it unnecessary to
compete for extremely low levels of dissolved in-
organic nitrogen. However, loss of NH, by outward
diffusion may be unavoidable in low N media or in
the atmosphere (Raven 1980, Kleiner 1985), and
uptake of NH,+ may be necessary to help offset this
loss even in cells actively fixing N,. It is tempting to
speculate that the sheath material surrounding Nos-
toc heterocysts retards the outward diffusion of NH,
or NH4+,but hard evidence of this is lacking.
Phosphate-limited cells of Nostoc calcicola are less
able to compete for ammonium (Prasad and Kash-
yap 1991). Addition of phosphorus (which also may
increase the ability to compete for ammonium) to
natural stream assemblages can promote growth of
Nostoc over some other periphyton species (Elwood
et al. 1981).
Some forms of organic phosphorus can be used
by Nostoc. Nostoc commune UTEX 584 has phospho-
monoesterase and phosphodiesterase but is unable
to use phytic acid (Whitton et al. 1990). Nostoc sp.
can store phosphate in polyphosphate bodies (DuBois
et al. 1984) and presumably take advantage of tran-
sient pulses of excess phosphate. An unidentified
species of Nostoc may have a high affinity for phos-
phate relative to that expressed by Selenastrum
(Brown and Harris 1978).
Other elements related to maintenance of growth,
7
photosynthesis, or nitrogenase activity include bo-
ron, which is required as a cofactor for growth and
nitrogenase synthesis in Nostoc UAM 205 and other
heterocystous cyanobacteria (Bonilla et al. 1990);
molybdenum as a cofactor for nitrogenase and ni-
trate reductase in N . muscorum (Vaishampayan 1983);
and vanadium, which allows nitrogen fixation by
Nostoc linckia in the absence of molybdenum but can-
not substitute for molybdenum as a cofactor in NO,-
reductase (Mishra and Kumar 1984). Certainly, many
other factors are also important.
Inorganic carbon may limit productivity of Nostoc,
especially in aquatic environments where rates of
diffusion are generally lower than in habitats with
direct exposure to the atmosphere. Cyanobacteria
can actively transport inorganic carbon up to 1000
times the external concentration (Pierce and Omata
1988, Badger and Price 1992). Nostoc calcicola has
been reported to utilize both carbonate and bicar-
bonate (Sarma and Garg 1985). Maberly (1992) sug-
gested that carbonate cannot be used by photosyn-
thetic organisms, even when it is the major form of
inorganic carbon available. However, Marcus et al.
(1992) present evidence that cyanobacteria (Synecho-
cystis) can utilize carbonate. Bicarbonate addition to
lake periphyton communities can remove any limi-
tation by inorganic carbon and causes Nostoc to be
replaced with other taxa, implying that Nostoc can
be a good competitor for inorganic carbon (Fair-
child et al. 1989).
Hydrological considerations. Some species of Nostoc
inhabit running waters and, thus, may be subject to
high turbulence and flow. In aquatic habitats, Nostoc
is often functionally a benthic macrophyte, and data
on how other macrophytes cope with flow (Raven
1992) are probably applicable. Flow can scour Nostoc
from the surface, and attachment to solid surfaces
is beneficial in such situations (Dodds and Marra
1989).
T h e metabolism of Nostoc is influenced by flow
effects on the diffusion boundary. As water velocity
increases, the thickness of the diffusion boundary
decreases (Fig. 3). This translates into lower O2ten-
sions in the top 100 pm of the colony (Fig. 2), and
the lowered 0, tensions allow for greater photosyn-
thetic rates (Dodds 1989). Increased amounts of in-
coming inorganic carbon also may allow the pho-
tosynthetic rate to increase (Dodds 1989). In very
slowly moving waters (several replacements per day),
water replacement may still have a direct positive
effect on growth of N . prunqorme (Dodds and Cas-
tenholz 1988a).
Photosynthesis and light. Nostoc, like other cyano-
bacteria, contains phycobilins that can absorb a broad
portion of the visible spectrum not used by green
algae, diatoms, and so forth (Cohen-Bazire and Bry-
ant 1982, Carr and Wyman 1986). Nostoc prunqorme
continues t o grow in low-light situations under ice
in the winter (Dodds and Castenholz 1987). A cave-
dwelling species (Nostoc microscopicum) has been de-
8 WALTER K. DODDS ET AL.
0.5 - I
' 0
nl 1 -
6 I
100 200 300 400
Incubation time (min)
C T r
1 tip diameter of the cathode type 0, microelectrode was 6 pm;
20 40 60 80 100 120 140 160 1,J
Time (h)
FIG.2. Time course of rewetting of Nostoc commune collected
in Hunan and Guanshi Provinces and stored dry for 2 years. Plots
show A) water uptake, B) photosynthesis and respiration, and C)
acetylene reduction (nitrogen fixation). Curves in C show the
response of N . commune dried for 2 years and 2 days. Curves fit
by lowess. Data replotted from Scherer et al. (1984).
scribed that can subsist 25 m from the cave mouth
in very low light levels (Biidel et al. 1993). Nostoc in
lichens may be extraordinarily shade-adapted (Green
et al. 1991). Ward (1985) suggested that interme-
diate light levels lead to maximum biomass of N .
parmelioides in the field.
Terrestrial and aquatic species in shallow waters
must be able to tolerate very high light levels and
high ultraviolet light (UV) flux rates. T w o com-
pounds that may be important to cyanobacteria in
this tolerance are the external sheath pigment scy-
tonemin (Garcia-Pichel et al. 1992) and the myco-
sporine-like amino acids (Vincent and Roy 1993).
Both of these compounds work in concert to screen
2 300
8
*
g 200
2 100
cw
E
a 0
mg 0 2 L-l
I
mg 0 2 L 1
FIG.3. Profiles of 0, concentration measured with microelec-
trodes above (top panel) and below (bottom panel) the top surface
of a Nostoc pannelioides colony as a function of water velocity. The
water velocity 1 mrn above the Nostoc colony was determined with
a thermistor probe (LaBarbera and Vogel 1976).
UV (Garcia-Pichel and Castenholz 1993). Nostoc (four
separate species tested) has scytonemin, with higher
concentrations on the outer layers of the colony
(Garcia-Pichel and Castenholz 1991). T h e one strain
of Nostoc tested (Nostoc microscopicum) did not have
mycosporine-like amino acids (Garcia-Pichel and
Castenholz 1993), but Nostoc muscorum collected from
Toolik Lake, northern Alaska, may have mycospo-
rine-like compounds (Vincent and Roy 1993). An
unidentified, water-soluble, UV protectant com-
pound has been extracted from Nostoc commune col-
lected from the field (Scherer et al. 1988). UV re-
sponse may be quite important in habitats such as
Antarctic streams, where Nostoc is a dominant pri-
mary producer (Vincent and Quesada 1993).
Given high extinction coefficients in the dense
thallus, a steep light gradient exists between the top
and the bottom of a Nostoc colony. Measurements
with fiberoptic light probes revealed that 90% of the
incoming light was absorbed within 100 Fm of the
surface of a colony of Nostocparmelioides. These steep
light gradients lead to lower rates of photosynthesis
and lsNpincorporation at the decreased light levels
in the colony interior (Dodds 1989).
 NOSTOC ECOLOGY
Interactions with Other Organisms
Heterotrophic bacteria and viruses. Nostoc has both
positive and negative interactions with heterotro-
phic bacteria. Antibiotic production has been re-
corded for N . muscorum LP23 (Bloor and England
199l), N . muscorum N' 791 (de Cano et al. 1986), and
N . linckia CALU 892 (Gromov et al. 1991). Given
that Nostoc certainly has coexisted and interacted
with bacteria over a significant portion of its evo-
lutionary history, the fact that it has evolved mech-
anisms to keep undesirable bacteria from growing
near or within colonies is not surprising. Interac-
tions between heterotrophic bacteria and cyanobac-
teria are not uncommon (Paerl 1982), and the effect
on cyanobacteria can range from inhibitory to stim-
ulatory.
Gantar (1986) conducted a study on the relation-
ships between Nostoc sp. and heterotrophic bacteria
isolated from fish pond water. Sixty strains of het-
erotrophic bacteria were grown individually with
Nostoc. Some species of bacteria accumulated around
Nostoc trichomes, some were not affected, and other
species were inhibited near Nostoc. Stimulation oc-
curred most commonly in nitrogen-free medium,
implying that nitrogenous compounds leached from
the Nostoc stimulated growth of the bacteria. In a
reciprocal experiment, Gantar (1985) tested for the
effects of the heterotrophic bacteria on Nostoc. He
noted that gram-negative asporogenous bacteria and
coryneforms were more likely to stimulate Nostoc
growth, whereas endospore-forming bacteria inhib-
ited it. In some cases, bacteria lysed Nostoc. T h e
ability of heterotrophic bacteria to grow in the pres-
ence of Nostoc on media without organic nitrogen
was related to stimulation of growth; possibly, the
bacteria secreted a compound that increased growth
and production of ammonium by the Nostoc.
Cyanophages have variable effects on the physi-
ological activity of Nostoc. T h e N-1 cyanophage de-
presses photosynthetic redox modulation, nitroge-
nase activity, and respiration rates in N . muscorum
(Amla et al. 1987, Kashyap and Singh 1989). Some
cyanophages can infect both Anabaena and Nostoc
(Bancroft and Smith 1988). No studies have been
published regarding the importance of infection in
natural populations.
Fungi. Certainly, the most obvious and important
interaction of Nostoc with fungi is in the formation
of lichens. This association is common in many hab-
itats. T h e facts that Nostoc can withstand repeated
drying, is photosynthetic, and is able to fix atmo-
spheric N, make it an ideal symbiont for fungi. Nu-
merous reports discuss the ecology of lichens (see
Galun 1988a, b, c, Werner 1992b), so it will not be
covered here.
Nostoc also forms an unusual endosymbiotic part-
nership with the fungus Geosiphon pyrgorme (Mollen-
hauer 1992, Werner 1992b). This association occurs
when the hyphae of G. pyrqorme incorporate Nostoc
9
by endocytosis and form bladders that contain nu-
merous Nostoc trichomes. Studies have shown that
some of the CO, assimilated by Nostoc is later incor-
porated into the fungi (Kluge et al. 1991) and that
Nostoc retains the ability to fix nitrogen as an en-
dosymbiont (Kluge et al. 1992).
Extracts of N . muscorum inhibit growth of Sclero-
tinia sclerotiorum (a plant pathogen), Rhizoctonia so-
lani, Candida albicans (a human pathogen), and Cun-
ninghamella blakesleana (de Mu16 et al. 1991). T h e
exact nature of the bioactive compounds is not
known. T h e presence of the inhibitory compounds
implies that a selective pressure by fungi on Nostoc
has existed during a part of its evolutionary history
and that such negative interactions (possibly com-
petition for nutrients or pathogenesis by fungi) are
still important to the ecology of Nostoc.
Plants. Nostoc interacts symbiotically with a variety
of plants, and presumably such interaction is facil-
itated by nitrogen fixation and the desiccation tol-
erance that allows Nostoc to be dispersed between
hosts. Plants do not need to rely on Nostoc for pho-
tosynthate. Researchers also have hypothesized that
formation of hormogonia plays a role in establish-
ment or maintenance of the functional symbiosis
(Campbell and Meeks 1989, Peters 1991) and that
chemotaxis may be important (Meeks 1990). Gantar
et al. (1993) showed that wheat exudates promote
formation of hormogonia in Nostoc 259B and that
subsequent attachment to the host root surface may
initially involve fimbriae and subsequent tight bind-
ing by the mucilaginous sheath. T h e variety of plants
(Table 2) that associate with Nostoc establishes the
genus as one with the most broad symbiotic com-
petence. These interactions are reviewed by Peters
(1991) and Rai (1990). Except for Gunnera (Berg-
man et al. 1992), the cyanobacteria associated with
plants are extracellular, but specialized morpholog-
ical modifications often occur that facilitate inter-
action between the plant and the cyanobacterium
(Peters et al. 1986). T h e heterocyst frequency usu-
ally is increased from 3-5% of the cells in material
cultured from the host to 30-50% when the Nostoc
is associated with the symbiont (Peters 1991). Such
an increase in heterocyst frequency leads to fewer
photosynthetic vegetative cells. In such cases, the
plants must supply much of the photosynthate if the
energetically expensive process of N4 fixation is to
continue (Steinberg and Meeks 1991).
Interactions between plants that are associated less
intimately with Nostoc also are probably common.
T h e plants growing in an area with a significant
amount of free-living Nostoc may benefit from fixed
nitrogen leaked from the cyanobacterium, but little
documentation exists of positive effects on the Nos-
toc. Direct experimental evidence for these less in-
timate associations is scarce. For example, Nostoc of-
ten is found growing close to mosses, but relative
nitrogen input directly to the mosses (Meeks 1990)
has not been quantified. Also, wheat growth rates
10 WALTER K. DODDS E T AL.

2. Plants reported to associate with Nostoc.

TABLE

Plant Common name Comments Referenm

Porella navicularis, Anthoce- Liverworts, Contained in mucilaginous cavities within the gameo- Duckett et al. 1977, Dalton
ros, Blasia, Cavicularia, hornworts phytic thallus or in Porella in crevices and curled and Chatfield 1985, Meeks
and Phaeoceros margins of leaves. Nostoc fixes nitrogen actively and et al. 1985
transfers it to host.
Bryum, Ceratodon, Rhacomi- Mosses Nostoc calcicola and N. muscorum have been identified Broady 1979, Henriksson et
trium, and Calliergidium as associated epiphytically with mosses, where they al. 1987
actively fix nitrogen. An unidentified Nostoc sp.
grows endophytically in Rhacmitrium canescens.
Azolla Water ferns Symbiont may be Anabaena or Nostoc. Tomaselli et al. 1988, Peters
1991
Ceratozamia, Dioun, and Za- Cycads Many species of cycads have Nostoc and other cyano- Lindblad et al. 1989, Osborne
mia bacterial species associated with corraloid roots. et al. 1991, Peters 1991,
Bergman et al. 1992
Gunnera Angiosperm (wa- All known Gunnera species support Nostoc as an endo- Bonnett and Silvester 198 1,
ter-milfoil) symbiont. Nostoc supplies fixed nitrogen to the host. Towata 1985a. b. Lindblad
et al. 1991, Bergman et al.
1992
Lemna trisulca Angiosperm Nitrogen-fixing Nostoc and other genera of cyanobac- Duong and Tiedje 1985
(duckweed) teria associated with lower epidermis of leaves.
Triticum vulgare Angiosperm Nostoc can associate with root epidermis and may stim- Reynaud and Metting 1988,
(wheat) ulate crop production. Gantar et al. 1991a, b

have been observed to increased upon association
with Nostoc (Gantar et al. 1991a, b).
Animals. Nostoc produces a variety of toxins that
affect animals, and such toxins could be evolutionary
responses to predation. Nostoc linckia (NT 69-43)
produces a toxin that is acutely toxic to the proto-
zoan Paramecium caudatum (Ransom et al. 1978). A
hepatotoxic microcystin with properties similar to
hepatotoxins produced by other cyanobacteria has
been isolated from Nostoc sp. 152 (Sivonen et al.
1990). Although such toxins are produced, some
species of Nostoc are consumed by humans (Emralino
and Rodulfo 1987). Perhaps some strains of species
do not produce toxins in significant amounts.
Many species of animals graze upon Nostoc (Table
3). However, the dense mucilage associated with the
trichomes and the toxins produced may make Nostoc
a less preferred food source than other algae. Cla-
dophora is preferred over Nostoc in some streams
(Dudley and D’Antonio 1991). Colony size also may
allow Nostoc to escape predation by oligochaetes
(Moore 1978), and this could be true for other po-
tential grazers on Nostoc.
Effects less direct than grazing also have been re-
corded. Nostoc in streams may compete for space
with larvae of the dipteran Blepharicera but provide
attachment space for the larvae of the midge Rheo-
tunytarsus (Dudley et al. 1986).
An interesting mutualistic interaction occurs
where larvae of the chironomid midge Cricotopus
nostocicola live inside colonies of N . parmelioides until
pupation occurs. The mutualism was described first

3. Organisms reported to consume Nostoc.

TABLE

Organism Comments Rcfcrcncn

Ciliata (Paramecium and Colpoda)
Amoeba (Mayorella sp.)
Calanoid copepods (Boeckella triarti-
culata, B. hamata, and B. dilatata)
Ostracod (Cyprinotus carolinensis)
Snail Indoplanorbis exustus (De-
shayes)
Ephydridae (Scatella stagnalis Fall-
en, Setacera atrovirens Loew, and
Setacera pacijica Cresson)
Chironomid midge larvae Cricoto-
pus nostocicola
Culex
Silver carp Hypophthalmichthysmoli-
trix Val.
Protozoa may stimulate Nostoc spp. nitrogen fixation, while Ghabbour et al. 1980
reducing chlorophyll a and carbon fixation by grazing
on the vegetative cells.
Reproductivue rates varied in relation to diet of mixed cul- Laybourn-Parry et al. 1987
ture including Nostoc sp.
Survival was significantly better with diet of Nostoc sp. than Burns and Xu 1990a, b
in the absence of food or when N. calticola was fed.
Grazing on Nostoc sp. was a linear function of ostracod Grant et al. 1983
size.
Snails fed lettuce leaves and N. muscorum grew better and Jantataeme et al. 1983
produced more egg clusters than those fed lettuce leaves
alone.
Shore fly larvae utilize 17 species of algae, including N. Foote 1977, Zack and Foote
muscorum; some species were found on Nostoc. 1978
Midge eats N. parmelioides but may provide benefits to alga Brock 1960, Dodds and Marra
as well. 1989
Nostoc and other cyanobacteria were able to serve as food Theivendirarajah and Jeyaseelan
sources in pure culture for developing mosquito larvae. 1977
Twenty-five percent of food spectrum was cyanobacteria Hochman 1985
(Anabaena, Aphanisomenon, Microqstis, Nostoc).
 NOSTOC ECOLOGY
by Brock (1960), who noted that larvae of this spe-
cies of midge were found only inside colonies of N .
parmelioides. T h e interaction occurs over a wide-
spread geographical area, with both partners oc-
curring in mountain streams in North America from
boreal forests to California (Sheath and Cole 1992,
R. Sheath, pers. commun.). Brock (1960) verified
that the midge larvae were eating the colonies and
suggested that they received protection from pre-
dation, but the benefit to the cyanobacterium was
less obvious. Photosynthetic rates of Nostoc colonies
with the midge are higher than those of colonies
without (Ward et al. 1985), and this has been as-
cribed to the fact that colonies with the midge ex-
tend farther into the flow, promoting outward dif-
fusion of inhibitory 0, and inward diffusion of
limiting CO, (Dodds 1989).
T h e larvae attach Nostoc onto rocks with silk,
thereby increasing resistance to scouring (Dodds and
Marra 1989). T h e pupating midge larvae also may
induce formation of hormogonia and, thus, promote
a flush of new, uninhabited colonies for their off-
spring (Dodds and Marra 1989). It remains to be
seen how the young larvae enter the colonies, be-
cause the laying behavior of the adult females has
not been studied. T h e interaction is probably not
an example of coevolution between the midge and
the Nostoc; rather, the midge larva has evolved to
take advantage of the Nostoc, and both members of
the mutualism have benefitted. Mutualisms have not
been described often between stream organisms.
Community- and Ecosystem-Level Interactions
Succession. Terrestrial Nostoc and nitrogen-fixing
cyanobacteria-containing lichens have several key
characteristics that may make them important as
early successional species. Early successional habitats
can be low in nitrogen and, thus, select for nitrogen-
fixing forms. Also, early successional habitats usually
have high solar irradiance but are poor at retaining
moisture. T h e ability of Nostoc to withstand desic-
cation and high light could allow it to do well in
disturbed habitats.
In the Hawaiian Islands, volcanic activity creates
disturbed areas that have soil with little or no or-
ganic C or N content. In this system, Nostoc occurs
only in mid- to late succession, but Stereocaulon vul-
cani, a nitrogen-fixing lichen that contains Nostoc,
occurs on the most recently and heavily affected
areas (Carson and Brown 1978). In the newly formed
volcanic ashes of Heimaey, Iceland, Nostoc was an
early successional inhabitant, commonly associated
with mosses (e.g. Englund 1978). In this environ-
ment, N. muscorum may prepare the soil for colo-
nization by other plants. Lichens containing Nostoc
also may be important in soil formation in other
habitats (Jones 1988).
It has been postulated that Nostoc is important in
soil formation in sea-margin tundra communities in
the far north. As the land very slowly (over thousands
11
of years) gains elevation after release from the weight
of glaciers, the more recently exposed terrestrial
systems are very nitrogen-poor, whereas the older
inland soils are richer in nitrogen. Nitrogen fixation
by terrestrial and wetland Nostoc probably increases
the amount of nitrogen in the systems (Bliss et al.
1990, Chapin et al. 199 1). Similarly, in a freshwater
habitat, when levels in a Polish reservoir were low-
ered, the exposed mud developed an algal com-
munity that shifted from species typical of periph-
yton to soil algae, including Nostoc punctiforme
Kiitzing, Nostoc edaphicum Kondrat., and N . commune
(Sieminiak 1984).
Ancient (900-700 Ma, late Precambrian) fossils
similar to extant Nostoc colonies have been described
for shallow marine sediments (Weiguo 1987). We
speculate that terrestrial analogs related to Nostoc
could have been some of the earliest terrestrial pho-
tosynthetic organisms and important in formation
of soils.
In streams, Nostoc may be considered a late suc-
cessional species that is affected little by grazing but
heavily by flow-related disturbance (Dudley and
D’Antonio 1991). Some species can form extensive
basal crusts and, thus, compete well for space, but
once scour starts removing the crusts, they are easily
washed away, and succession begins anew. Similarly,
Nostoc is dominant in Antarctic streams, and scour
disrupts succession (Vincent et al. 1993).
Importance in ecosystems. Nitrogen fixation by Nostoc
could be of considerable importance from a sys-
tems/dynamic approach in systems where little oth-
er input of “new” nitrogen occurs. Flooding rice
paddies allows for establishment of free-living col-
onies of Nostoc and the water fern A d a , which con-
tains heterocystous Nostoc (or Anabaena, Meeks et al.
1988, Peters and Meeks 1989). When the fields are
drained, the green compost may enrich the soil with
nitrogen and increase rice yields. This may be re-
sponsible for centuries of successful rice cultivation
without external addition of manure or other fer-
tilizers (Grist 1986), and such a strategy is used to
fertilize approximately 2 million hectares of land
(Werner 1992a). Critical studies on the importance
of cyanobacteria in rice culture are still needed
(Whitton 1987).
Nostoc associated with mosses can provide 2-58%
of the nitrogen input to northern tundra, and Nostoc
nitrogen fixation in Antarctic moss turfs supplies
4 2 4 4 % ; much of the remaining nitrogen is con-
tributed by precipitation or penguin excretion
(Christie 1987). Cyanophilous lichens may provide
the bulk of the fixed nitrogen in some ecosystems.
In the old-growth Douglas fir forests in the Pacific
Northwest of North America, Lobaria provides much
of the incoming nitrogen each year (Seaward 1988).
Lichens also may contribute significant portions of
fixed nitrogen in desert crusts and the Stereocaulon
heaths of the far north (Seaward 1988).
Nitrogen fixation by the benthic N . pruniforme
12 WALTER K. DODDS ET AL.

TABLE 4. Nitrogenfixation rats in assemblages containing mostly Nostoc (in Method, A = acetylene reduction, N = direct measurement with 15N2
or calibration of acetylene reduction with "N). Acetylene reduction values were corrected to moles of N e d in cases where 'W was not used, by the
relationship 3 moles of acetylene reduced to 1 mole of Nzfixed (Hardy et al. 1968). Rates (area) are reported in pmol N.m-2,h-1. calculated from
annual estimates when possible. Rates (biomass) are reported in nmol Nsrng-'. h-l. +Converted assuming 1% chlorophyll a, 6% N by weight.

MCth- Rate
Species Habitat od Rate(area) (biomass) Comments References
Nostoc commune Sarcpa Lake, Northwest A 5.91 k 2.90 - Fixation in wet soils along the Karagatzides et al. 1985
and other sp. Territories shore bv Nostoc associated
with mosses; summer rates,
48-hincubations.
N. commune Vestfold Hills, Antarc- A 1.87-9.93 - Rates controlled by tempera- Davey and Marchant
tica ture and moisture; 2-h mid- 1983
day incubations, summer
rates.
N. muscorum Signy and South Orkney A 0.75-3.14 - Minimum from dry moss turf, Christie 1987
Islands, Antarctica maximum from wet moss
carpet. Calculated from lab-
oratory incubations, extrap
olated using weather data to
surface conditons.
Nostoc spp. Ellesmere Island, Alex- A 0.53-0.85 7.6 Nostoc spp. were considered Henry and Svoboda
andra Fiord and Sver- the major Np-fixingagents 1986
drup Pass in the studied sites. Yearly
rates based on 36-h incuba-
tions throughout the sum-
mer.
N. commune Stipa-Bouteloa grassland, A 0.96-7.42 0.97 Rapid response of nitrogenase Coxson and Kershaw
southern Alberta activity to both small precip 1983
itation events and dewfall
hydration periods. Mean
rates for favorable summer
periods, diurnal incubations
used.
N. commune, N . p a - Aldabra Atoll, Indian A 31 3-3972 1.54* Light rates for Nostoc colonies. Whitton et al. 1979
gellijorme (Berk. Ocean Marked variation in CIH,
& Curtis) Born production throughout the
& Flah. day, peaks in early after-
N. sphaericum noon, light rates about 4 x
Vaucher dark rates. Midday incuba-
tions, variety of seasons.
N. commune Eniwetok Atoll, South A 230-408 0.94' Assume 10-h days, no season- Mague and Holme-
Pacific ality. Hansen 1975
N. punchiforma French West Indies, A 344 7.3' Used 1 mole C4H4:4.2 of N, Sheridan 1991
mangrove community assume 12 h/day activity for
250 days.
N. prunifonne Mare's Egg Spring, N 15.9 0.87 Monthly measurements over Dodds and Castenholz
Klamath County, Ore- the year, 24 h acetylene re- 1988b
gon duction incubations, rate
corrected with lSN4incorpa-
ration.
Nostoc sp. Rocky Creek, California A 0.24-2.07 1.2 Minimum in shaded area, Home 1975,Horne
maximum in sunny area. Es- and Carmiggelt 1975
timates with seasonal data,
short diurnal measurements
of rates, maximum rates in
day, but detectable fixation
during night.

provides 3.4% of the total nitrogen input in an oli-
gotrophic cold water pond (Mare's Egg Spring, Or-
egon). This may be relatively more important to the
biological community than nitrogen from other
sources. Much of the combined nitrogen in the spring
water flows rapidly through the system, and much
of the biological activity is centered on the benthos
that is covered by Nostoc colonies (Dodds and Cas-
tenholz 1988b).
Numerous measurementshave been made on rates
of nitrogen fixation by assemblages containing
mainly Nostoc (Table 4). References that compare
rates are available for Arctic and alpine systems
(Henry and Svoboda 1986, Christie 1987) and other
aquatic and terrestrial systems (Horne and Carmig-
gelt 1975, Whitton et al. 1979). Often, the acetylene
reduction method is used and not calibrated with
ISN, uptake. The rate of nitrogen fixation can be
estimated from rates of acetylene reduction using a
conversion factor of 3 moles of ethylene produced
 NOSTOC ECOLOGY
for every 1 mole of N, fixed (Hardy et al. 1968),but
this ratio may vary widely between systems. Even a
ratio of 4:1 to account for H, production is suspect,
because the relative amount of H2 production may
show diurnal variation (Turner and Gibson 1980).
For the purposes of this paper, a ratio of 3:l was
used to convert estimates.
In general, total annual amounts of nitrogen fixed
in temperate terrestrial systems exceed those in more
polar systems, almost certainly because of the length
of time that temperature and light are at levels ad-
equate for active nitrogen fixation. Studies that do
not consider the dark time and/or winter rates con-
sistently report higher rates of nitrogen fixation than
those that sample throughout the year or extrapo-
late to account for periods of low or no activity
(Table 4).Rates for temperate aquatic systems are
consistent with those for temperate terrestrial sys-
tems. T h e only tropical data reported give high rates
of nitrogenase activity (Mague and Holme-Hansen
1975, Whitton et al. 1979, Sheridan 1991);how-
ever, when rates of N2 fixation are normalized to
biomass, the trend of high rates in tropical systems
is not evident (Table 3).
Conclusions and Recommendationsfor
Future Research
Nostoc is one of the most complex cyanobacteria,
featuring colonial and multicellular growth forms
and specialized cells for nitrogen fixation and dis-
persal. These adaptations, among others, probably
make it one of the most broadly successful cyano-
bacterial genera. Adaptations such as nitrogen fix-
ation, akinete and hormogonia production, desic-
cation and freezing resistance, UV tolerance, and
grazing resistance are not limited to this genus of
cyanobacteria. Rather, the combination of these at-
tributes leads to its success. This success is evidenced
by the variety of habitats with Nostoc, the large num-
ber of symbiotic or mutualistic interactions in which
it participates, and its importance in succession and
soil formation. Some species seem to be adapted to
fluctuations and are able to withstand changes in
chemistry, temperature, and moisture. However,
Nostoc prunijorme colonies have been shown to dom-
inate and reach impressive biomass in very constant
spring waters (Dodds and Castenholz 1987);thus,
environmental extremes are not necessarily require-
ments for all species.
Areas for future research include 1) additional
study of the systematics of the genus, with further
application of molecular techniques to both cultures
and field populations; 2) increased attention to sys-
tematics and ecology of Nostoc with smaller thalli
(Mollenhauer et al. 1994);3) research on controls
of natural populations in the field, including the
importance of cyanophages and grazing; 4) docu-
mentation of ecophysiological mechanisms used to
survive environmental extremes; 5)increased study
of the ecophysiology of Nostoc species other than N .
13
muscorum, which is a rapidly growing “laboratory
weed” and may not be representative of other mem-
bers of the genus; 6)more complete studies on the
importance of nitrogen fixation to ecosystem-level
nitrogen budgets; 7)more complete documentation
of the vital roles in succession and soil development
in terrestrial polar environments; and 8) more in-
formation on the use of Nostoc in sustainable agri-
cultural practices, in addition to the current use in
rice production.
We thank R. W. Castenholz, J. C. Meeks, M. Potts, J. A. Raven,
W. F. Vincent, B. A. Whitton, and an anonymous reviewer for
helpful comments, T. Barkley for translating, and E. S. Barkley
for editing. W.K.D. thanks R. W. Castenholz for the introduction
to Nostoc in particular and microbial ecology in general. This is
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