Eur. I. Phycol. (1999), 3 4 : 3 7 1 -3 7 9 .
371
Printed in the U nited K ingdom
M arine cyanobacteria in tropical regions : diversity and eco lo g y
LUCIEN H O F F M A N N
U n iv e r s ity o f Liège, In s titu te o f B o ta n y (B .2 2 ), S a r t T ilm a n , B - 4 0 0 0 Liège, B e lg iu m
(R e ceiv ed 15 J a n u a r y 1 9 9 9 ; accepted 1 7 Ju n e 1 9 9 9 )
T r o p i c a l m a r in e e c o s y s t e m s a r e c h a r a c t e r i z e d b y a s p e c ific c y a n o b a c t e r i a l flo r a , t e m p e r a t u r e m o s t p r o b a b l y b e i n g t h e m a jo r f a c t o r li m it in g
t h e g e o g r a p h i c d i s t r i b u t i o n o f t h e s p e c ie s . W h e n c o m p a r e d w i t h t h e o p e n o c e a n , t h e h i g h e s t b i o d i v e r s i t y o f c y a n o b a c t e r i a is o b s e r v e d in
t h e li t t o r a l z o n e s w h e r e t h e y f o r m i n t e r t i d a l a n d i n f r a lit to r a l m a ts , liv e a s e n d o l i t h s in c a r b o n a t e s u b s t r a t e s o r f o r m s y m b i o t i c a s s o c ia tio n s ,
e s p e c i a ll y w i t h s p o n g e s a n d a s c id ia n s . T h e i r d i v e r s i t y , w h ic h e s p e c i a ll y in t h e le s s a c c e s s ib le i n f r a lit to r a l is s till l a r g e l y u n k n o w n , is a l s o a
s o u r c e o f d i v e r s e b i o a c t i v e c o m p o u n d s , s o m e o f w h ic h a r e i m p o r t a n t a s h e r b i v o r e d e t e r r e n t s . A s p h o t o s y n t h e t i c o r g a n i s m s , c y a n o b a c t e r i a
s e n su lato ( in c lu d in g P r o c h l o r o p h y t a ) a r e i m p o r t a n t c o n t r i b u t o r s t o b e n t h i c a n d o p e n o c e a n p r i m a r y p r o d u c t i o n , b u t t h e i r m a in r o le in t h e
tr o p i c a l m a r in e e c o s y s t e m s a p p e a r s t o b e a s n i t r o g e n fix e r s . O f p r i m a r y i m p o r t a n c e in t h e o f t e n o l i g o t r o p h i c tr o p i c a l o c e a n s is t h e n o n h e t e r o c y s t o u s , p l a n k t o n i c b l o o m - f o r m i n g T ric h o d e s m iu m , w h ic h p r o b a b l y r e p r e s e n t s a m a jo r n i t r o g e n s o u r c e f o r t h e m a r in e a n d g l o b a l
n i t r o g e n c y c le .
K e y w o rd s: b i o d i v e r s i t y , b i o g e o g r a p h y , C y a n o b a c t e r i a , C y a n o p h y t a , m a r in e , n i t r o g e n f ix a tio n , s e c o n d a r y m e t a b o l i t e s , tr o p i c s
Introduction
The existence of Precambrian fossil stromatolites con­
taining evidence of oxygenic photosynthesis and fossil
endoliths similar to living species (Golubic & Knoll, 1993)
indicates the long evolutionary and biochemical history of
marine cyanobacteria. Contemporary marine cyano­
bacteria still play important roles, especially in tropical
ecosystems (the phytogeographical subdivisions of the
oceans as defined by Van den Hoek (1984) for macroalgae
are applied here: the tropical oceanic area is thus limited
by the 20 °C winter isotherm of the seawater, whereas in
the temperate regions water temperature drops to 10 °C),
where they have a high biodiversity, are widespread, and
may sometimes occur in striking abundance. It was
probably a red-pigmented bloom-forming species of the
genus T richodesm ium which gave the Red Sea its name
(Fogg, 1982). The assessment of the biodiversity of
cyanobacteria depends on a reliable taxonomy in order
definitively to recognize genetically different entities in
nature. M odern molecular phylogenetic studies are cur­
rently restricted to axenic cultures and D NA mixtures
extracted from natural populations. Ecological research
will, therefore, continue to depend on the phenotypic
identification of cyanobacteria. O n the other hand,
taxonomic studies of cyanobacteria have neglected marine
environments, especially in tropical regions. Identification
manuals include only a small fraction of genuine marine
cyanobacterial taxa. Consequently, floristic surveys have
frequently applied names of freshwater taxa when re­
porting cyanobacteria from marine habitats.
Renewed interest in marine cyanobacteria was gener­
ated in conjunction with the study of marine picoplankton
and its contribution to oceanic primary production
(Waterbury et al., 1979; Johnson & Sieburth, 1979), while
planktonic filamentous cyanobacteria attracted attention
as important contributors to the nitrogen cycle in the
ocean as well as toxin producers (see e.g. Sellner, 1997). In
contrast, interest in marine benthic cyanobacteria has
mostly been limited to intertidal environments, which
were used as model systems for the interpretation of fossil
stromatolites.
Oxygenic photosynthetic prokaryotes have been
placed in two divisions: cyanobacteria (Cyanophyta)
characterized by the presence of chlorophyll a and
phycobiliproteins, and the Prochlorophyta, also called
Oxychlorobacteria, characterized by the possession of
chlorophylls a and b, and the absence of phycobilisomes.
Sequence analyses have shown, however, that the prochlorophytes are a polyphyletic group residing within the
cyanobacterial lineage (Turner, 1997). In the following
review, the term 'cyanobacteria' is used in a wide sense,
including all oxygenic, photosynthetic prokaryotes ( =
oxyphotobacteria sensu Murray, 1989). The nomenclatural
system followed is that of Geitler (1930-2).
Cyanobacteria occupy a wide range of niches in marine
ecosystems in tropical regions where they occur along
maritime coasts as well as in the open ocean. The
environmental constraints to which they are exposed vary
widely in these tw o habitat categories, so that their
biodiversity and ecology in the benthic and planktonic
environments will be considered separately.
Littoral cyanobacteria
C yanobacteria o f intertidal a n d supratidal zones
Benthic cyanobacteria are widespread along maritime
coasts, often forming visually conspicuous growths on
rocks and sediments as mats and epilithic growths. A
372
L. H offm ann
2
9
10
F ig s 1—1 0 . R ep resen tativ e cyanobacterial g en era of th e tropical
m arine b en th o s. Fig. 1. Borzia G o m o n t. Fig. 2. Oscillatoria
G o m o n t. Fig. 3. Hydrocoleum G o m o n t. Fig. 4. Lyngbya G om ont.
Fig. 5. Schizothrix G o m o n t. Fig. 6. Phormidium G o m o n t. Fig. 7.
F ig s 1 1 —1 5 . R e p resen tativ e g e n era of tropical m arine endolithic
cyanobacteria. Fig. 11. Hyella B ornet et Flahaut. Fig. 12. Solentia
Ercegovic. Fig. 13. Herpyzonema W eb er-v an Bosse. Fig. 14.
Mastigocoleus B ornet et Flahaut. Fig. 15. Kyrtuthrix E rcegovic.
Scytonema B o rn et et Flahaut. Fig. 8. Calothrix B ornet et Flahaut.
Fig. 9. Microchaete B ornet et Flahaut. Fig. 10. Microcoleus G om ont.
littoral fringe containing lichens and cyanobacteria is of
almost universal occurrence on rocky shores (Stephenson
& Stephenson, 1949) and has also been described from
tropical regions such as around the Seychelles (Taylor,
1968).
The occurrence of extensive mats of cyanobacteria is
observed on or in much tropical coastal sand and silt.
M any of the more complex types play an important role
in building and trapping sediments a n d /o r in carbonate
precipitation (Golubic, 1973). Some of these littoral
communities dominated by cyanobacteria are restricted to
warm waters ; this is especially true for those which form
well-developed stromatolites, which are lithified mats.
M any examples of stromatolites have been described
(Walter, 1976). They are most abundant in lagoons and
sheltered coastal localities; some of the best-developed
examples, such as those at Shark Bay (Western Australia)
or in the Persian Gulf, are found in hypersaline waters.
O n moving from the supralittoral down to the intertidal
zone, mats often show a zonation. The distribution of the
types of mats is determined by the frequency and duration
of subaerial exposure, wave energy, and the type and
amount of sediment transported by tidal currents (e.g.
Golubic, 1985). The surface morphology of mats depends
on the prevailing environmental conditions, but also on
the dominant species (Golubic & Focke, 1978; Zhang &
Hoffmann, 1982).
The intertidal zone is often dominated by sheathproducing taxa of filamentous non-heterocystous
(L y n g b y a , M icrocoleus, P horm idium , S chizothrix) andheterocystous (R ivu la ria Bomet et Flahaut, C alothrix, Scyto n em a )
genera (Figs 1—10). Vertical sections of mats usually
include various groups of prokaryotes in discrete coloured
layers. The surface layer is often dominated by the
cosmopolitan L y n g b y a aestuarii Gomont. This species
seems to be protected from excessive radiation by the
brown extracellular sheath pigment 'scytonem in' (GarciaPichel & Castenholz, 1991). /m other common and
geographically widespread member of microbial mats is
M icrocoleus chthonoplastes Gomont.
M angrove forests, common along many tropical and
some subtropical coastal lagoons are inhabited by diverse
cyanobacterial communities which reside on leaf and root
litter, live roots, and often form extensive mats on the
surrounding sediments (e.g. Potts, 1979, 1980; Potts &
Whitton, 1980; Sheridan, 1991; Hussain & Khoja, 1993;
Toledo et a l, 1995; Phillips et a l, 1996); many of these
communities are capable of N 2 fixation. The genera
O scillatoria, L yn g b ya , P horm idium and M icrocoleus are
widespread in these habitats, as are heterocystous genera,
such as Scytonem a, in some areas (Potts, 1979). Vertical
373
Tropical marine cyanobacteria
T ab le 1. Floristic su rv ey of m arine cyanobacteria in P apua N e w
G uinea (H offm ann, 1989, 1993; H offm ann & D em oulin, 1991,
1993).
CHROOCOCCALES
N o . of
N o . of species
N o . of
g e n e ra
a n d subspecies
n e w ta x a
14
20
C h am aesip h o n ac eae
2
4
C h ro o co c cace ae
1
1
-
D erm o ca rp ellacea e
1
1
-
H y d ro c o c c a c e a e
4
7
M ic ro c y sta c e a e
4
5
-
P ro ch lo ra ceae
1
1
-
X enococcaceae
1
1
9
41
17
O SC IL L A T O R IA L E S
O sc illato riacea e
5
2
3
-
9
41
17
5
13
3
M icro c h aeta ceae
1
2
N o sto c a c e a e
1
2
-
R ivulariaceae
2
7
1
S c y to n e m a ta c e a e
1
2
1
S T IG O N E M A T A L E S
3
3
-
M astig o c lad ac eae
2
2
-
N o sto c h o p s id a c e a e
1
1
N OSTO CA LES
1
zonation is often observed on the pneumatophores or
prop roots.
Cyanobacteria that live inside limestone rocks are also
an important feature of intertidal habitats (Radtke et al.,
1997). The colonization of marine rocks by endoliths can
be very rapid (Perkins & Tsentas, 1976; Potts & W hitton,
1980). The cyanobacterial endolithic assemblages exhibit
a well-defined zonation pattern which is recognized by
changes in the dominance and abundance of the different
species and can be correlated with differences in tidal
range and the vertical distribution of the macroflora and
macrofauna (Hoffman, 1985; Radtke et aí., 1996; Taton &
Hoffmann, 1999). The upper ranges are generally dom­
inated by H erp yzo n em a , H o rm a th o n em a Ercegovic,
S cyto n em a , Solentia and K y rtu th rix , whereas M a stigocoleus
(Figs 11—15) generally appears only in the lower intertidal
zone. The major difference between temperate and tropical
carbonate coasts seems to lie in the presence and often
dominance of H erp yzo n em a interm edium W eber-van Bosse
in tropical regions (Hoffman, 1985; Taton & Hoffmann,
1999), whereas in temperate regions such as the M edi­
terranean Sea (Le Campion-Alsumard, 1979), H yella balani
Lehmann seems to occupy the niche of the latter species in
the intertidal zone.
C yanobacteria o f the infralittoral zone
Conspicuous growths of sublittoral benthic mats are
frequently recorded from warmer waters, where films of
filamentous species overlying sand in shallow water
appear to be relatively common. In contrast to those
found in the intertidal, they are simpler, generally do not
show a vertical zonation, and consist of films of in­
terwoven filaments, often of single species. Thick mats can
extend to the lower part of the shore in sheltered,
moderately hypersaline conditions (Potts & W hitton,
1980; Bauld et a l, 1992) and can even form stromatolites
(Golubic & Browne, 1996). M ats with cyanobacteria have
been observed to depths of 50 m, but in general growth
appears to be most rapid in depths of less than 10 m.
These superficial mats become established where rates of
sediment movement and turnover by grazers and es­
pecially by burrowers are low (Whitton & Potts, 1982).
In the infralittoral zone a very high biodiversity is
found, especially near coral reefs, where the oscillatoriacean genera (O scillatoria, H ydrocoleum , M icrocoleus) are
represented by many taxa, some of which remain to be
described (e.g. Hoffmann & Demoulin, 1993; see also
Table 1). Little information is available about their
ecology, including their interactions with herbivores,
although some reports mention that they are heavily
grazed, for instance by holothurians (Sournia, 1976).
Epiphytic cyanobacteria (especially C alothrix, M ic r o ­
chaete, L yngbya) are present on pelagic macroalgae such as
S argassum C. Agardh (Phlips et a l, 1986), and on benthic
macroalgae and seagrasses (e.g. Brouns & Heijs, 1986;
Klumpp et a l, 1992; Hoffmann, 1993), together with
diatoms, Chlorophyta and Rhodophyta. These epiphytic
communities are important contributors to the overall
productivity (Moncreiff et a l, 1992) and are a major food
source for macroinvertebrate grazers (Klumpp et a l, 1992 ;
Mukai & Iijima, 1995). M any of these epiphytic cyano­
bacteria are heterocystous and thus fix N 2, which may
contribute to the marine nitrogen budget (e.g. the
estimated nitrogen input by epiphytic cyanobacteria on
S argassum amounts to 0.018 IO9 g N year-1, Capone &
Carpenter, 1982).
The tropical regions are also characterized by par­
ticularly diverse endolithic cyanobacterial communities
(including e.g. the genera H yella, Solentia) (Figs 11, 12)
which can be found in the skeletons of living and dead
coral (Le Campion-Alsumard et a l, 1995) and in other
limestone substrata, contributing substantially to the
dissolution of carbonates of coral reefs (Chazottes et a l,
1996) and to the bioerosion of limestone coasts. Recent
studies demonstrate a high diversity of endolithic cyano­
bacteria in shallow tropical and subtropical seas. Many
new taxa, especially within the genus H yella, have thus
been described in the last 20 years, for example from the
Bahamas, Florida and the Arabian Gulf (Golubic et a l,
1996 and references cited therein).
Black-band disease is a widespread phenomenon found
on coral reefs (Richardson, 1996). The disease consists of
a microbial community dominated by the filamentous
cyanobacterium P h orm idium corallyticum (Rützler &
Santavy, 1983) associated with bacteria and fungi. It
normally forms a band 1 mm thick between the coral
skeleton and the living coral tissue. Black-band disease can
cause the death of entire coral colonies due to tissue
destruction as the bands migrate, and is thought to be a
factor contributing to the observed global degradation of
coral reefs (Williams & Bunkley-Williams, 1990).
374
L. H offm ann
A notew orthy feature of tropical regions, especially of
coral reefs, is the presence of a number of cyanobacterial
species belonging to the genera A p h a n o ca p sa Nägeli,
Prochloron Lewin ex Florenzano et al., Synechocystis
Sauvageau, Borzia and O scillatoria, which live in symbiosis
with sponges (Wilkinson, 1992) or ascidians (Pardy &
Royce, 1992). Recently, a new type of unicellular oxygenic
photosynthetic prokaryote was isolated from a tropical
colonial ascidian, Lissoclinum patella, and provisionally
named A ca ryochloris m a rin a Miyashita et Chihara gen. et
sp. inedit. (Miyashita et a l, 1996). Its most distinctive
feature is the presence of a unique light-harvesting system
which uses chlorophyll d as the major antenna pigment
and chlorophyll a as a minor pigment. Like other species
commonly included in the Prochlorophyta (Goericke &
Répéta, 1992; Larkum et a l, 1994), it also contains a
chlorophyll c-like pigment (Miyashita et a l, 1997) which is
absent in cyanobacteria sensu stricto. Some of these
organisms, especially Prochloron and A caryochloris, are
interesting models for the studies on the origin of the
different algal plastid types (Lewin & Cheng, 1989;
Matthijs et a l, 1994; Turner, 1997).
Coral reefs are one of the tropical marine habitats in
which cyanobacterial diazotrophs appear to play a critical
role in ecosystem functioning. Cyanobacteria are found in
monospecific mats, mixed 'algal' turfs and as macroalgal
epiphytes. Cyanobacteria play an important role in the
nitrogen budget of coral reefs (Mague & Holm-Hansen,
1975; W ebb et a l, 1975; Wiebe et a l, 1975; Burris, 1976),
where N 2 fixation can account for 20—40% of the annual
nitrogen requirements (Borowitzka & Larkum, 1986). The
estimated annual contribution of coral reefs to the global
nitrogen cycle amounts to 2.8 Tg, with a mean areal N 2
fixation rate of 25 g n T 2 year-1 (Capone & Carpenter,
1982).
Although benthic cyanobacteria are periodically very
common in reef habitats subject to high levels of
herbivory, and although they lack structural defences (e.g.
calcification) like various macroalgae, they seem to be a
low-preference food item for many marine herbivores.
Some of these cyanobacteria, such as the genera H o rm o ­
th a m n io n Bomet et Flahaut (Pennings et a l, 1997) and
L y n g b y a (Pennings et a l, 1996; Nagle et a l, 1996; Orjala
& Gerwick, 1996), are unpalatable to most, but not all,
potential consumers, probably because of the presence of
secondary metabolites which effectively deter feeding.
Marine cyanobacteria have been a productive source of
novel secondary metabolites (Moore, 1981; Faulkner,
1995) with varying bioactivities. They present a diversity
of structural classes : cyclic peptides, depsipeptides, linear
peptides, guanidines, phosphonates, purines, lipids and
macrolides. They often contain nitrogen (in striking
difference to those found in macroalgae) and often are
halogenated (e.g. brominated pyrrole derivatives, chlorin­
ated amides) (Moore, 1981). Some secondary metabolites
from marine cyanobacteria have been examined for
pharmacological activity (e.g. cytotoxicity to tumour
cells, inhibition of proteases) (Shimizu, 1996). Several
bioactive peptides found in cyanobacteria have structural
features of metabolites described from ascidians and
sponges living in coral reefs (Namikoshi & Rinehart,
1996), which suggests the latter compounds may be
derived from dietary or symbiotic cyanobacteria (Williams
et a l, 1993), but transfer of genes cannot completely be
ruled out (Shimizu, 1996).
One of the richest cyanobacterial source of secondary
metabolites is the benthic filamentous L y n g b y a m ajuscula
Gomont (Mermaid hair) (Moore, 1981; M oore et a l,
1984; Sitachitta & Gerwick, 1998; Graber & Gerwick,
1998 ; Hooper et a l, 1998), one of the largest cyanobacteria
known, which caused an outbreak of severe contact
dermatitis in fishermen due to the presence of prenylated
amino acid derivatives, called lyngbyatoxins (Cardellina et
a l, 1979). A nother L y n g b y a species, L. bouillonii, recently
described from coral reefs in Papua New Guinea (Hoff­
mann & Demoulin, 1991) where it forms extensive mats,
strongly attached to madrepores in the infralittoral,
proved also to be a rich source of novel macrolides and
peptides (Klein et a l, 1996, 1997, 1999). H o rm o th a m n io n
enterom orphoides contains a series of at least 15 related
cyclic peptides (Gerwick et a l, 1989). Their chemical
defences thus are probably a key factor allowing these
cyanobacteria to persist in reefs.
Planktonic cyanobacteria
In contrast to their abundance in freshwater habitats, there
are few truly planktonic cyanobacterial species in the sea.
There are four groups of cyanobacteria known to be
present in the plankton of tropical oceans in numbers
sufficient to make a measurable ecological contribution:
the picoplanktonic Synechococcus and Prochlorococcus (see
e.g. Ferris & Palenik, 1998) and the filamentous genera
T richodesm ium (Capone et a l, 1997) and Richelia (Villareal,
1992) (Figs 16—20). There are, of course, many other
reports of cyanobacteria of various genera (Soumia, 1970),
such as K a tagnym ene (Wille, 1904), but none of these
seems to make a consistent major input into the ecosystem.
F ig s 1 6 —2 0 . R e p resen tativ e cyanobacterial g en era of th e tropical
m arine plankton. Fig. 16. Katagnymene Lem m erm ann. Fig. 17.
Trichodesmium E hrenberg ex G o m o n t. Fig. 18. Richelia Schm idt.
Fig. 19. Synechococcus N ägeli. Fig. 20. Prochlorococcus C hisholm et
al.
375
Tropical marine cyanobacteria
Trichodesmium
During the past few decades, Trichodesmium has been one
of the most intensively studied cyanobacteria of the open
tropical oceans. The main reasons for this interest are that
Trichodesmium can occur in great abundance (as surface
blooms) and it can fix N 2 (Dugdale et a l, 1961) during the
day without the formation of thick-walled heterocysts
(Bergman & Carpenter, 1991).
Trichodesmium includes a number of filamentous forms
which, apart from their general tendency to aggregate in
bundles, closely resemble species of Oscillatoria. Five
marine species are included in the genus Trichodesmium,
distinguished by trichome dimensions and colony mor­
phology. O n the basis of ultrastructure Qanson et a l,
1995b), T. erythraeum Gomont and T. tenue Wille, with
spherical colony shape and narrow trichomes, can be
distinguished from T. thiebautii Gomont, T. hildebrandtii
Gomont and T. contortum Wille. The presence of several
distinct m orphotypes is consistent with the results from
nitrogenase nifFl and 16S rDNA sequence analyses
(Capone et a l, 1997), which also show that all Tri­
chodesmium clones studied so far form a monophyletic
group.
Species of Trichodesmium are primarily found in tropical
and subtropical surface waters, especially during calm
conditions. These waters have low nutrient concentrations
and deep euphotic zones (Capone et a l, 1997). Under calm
conditions, filaments accumulate as surface blooms known
to sailors as 'sea sawdust'. Such blooms are often large
enough to be detected by satellite.
The positive buoyancy of Trichodesmium depends on
the presence of very strong gas vesicles (Walsby, 1978), a
possible adaptation to the great hydrostatic pressures to
which Trichodesmium can be exposed at depth in the sea
(e.g. about 20 bars at 200 m). W hen highly gas-vacuolated,
they can migrate to the surface at a velocity of 0.5—3 mm
s-1 (40—250 mm day-1). In addition to providing buoy­
ancy, the gas vacuoles may shield the cells from
excessively strong radiation (Janson et a l, 1995b).
Trichodesmium is well adapted to living in oligotrophic
waters. It fixes atmospheric nitrogen, thus avoiding
nitrogen limitation, and uses buoyancy reversals to
migrate below the nutricline to acquire phosphorus
(Carpenter & Romans, 1991; Karl et a l, 1992). In
oligotrophic waters removed from terrestrial influences
and unaffected by upwelling, where N 2-fixing planktonic
or benthic cyanobacteria are of importance, additional
nutrient limitations may occur. In particular the availability
of iron, essential for N 2 fixation, N 0 3- assimilation and
photosynthetic activity, may be restricted (Rueter et a l,
1992; Paerl et a l, 1994).
The enigmatic situation of having an oxygen-gen­
erating photosystem II functioning at the same time as the
highly oxygen-sensitive process of nitrogen fixation is
one of the most interesting traits of Trichodesmium. At
least in certain Trichodesmium species, cells containing
nitrogenase are clustered into groups Qanson et a l, 1995b).
A recent model (Fredriksson & Bergman, 1997) proposes
(a) that Trichodesm ium is capable of differentiating a cell
type which is specific for nitrogenase; (b) that these
nitrogenase-containing cells are grouped into small sub­
sets, possibly one or more subsets in each filament; and (c)
that these cells are structurally and functionally modified
to harbour the oxygen-sensitive nitrogenase.
Trichodesm ium aggregates often harbour diverse
eukaryotic and prokaryotic organisms: bacteria, cyano­
bacteria, diatoms, dinoflagellates, fungi, protozoa,
hydroids and copepods (O'Neil & Roman, 1992; Siddiqui
et a l, 1992). The association of most organisms with
Trichodesm ium colonies appears to be mutualistic, but
larger planktonic and nektonic organisms (fish, crabs) may
graze on Trichodesm ium filaments. There are also associ­
ations of the juvenile harpacticoid copepod M acrosetella
gracilis with Trichodesm ium . It not only ingests T ri­
chodesm ium colonies but rapidly incorporates cyano­
bacterial organic matter into its own cellular material
(O'Neil, 1998). The neurotoxins identified for some
Trichodesm ium blooms (Ffawser et a l, 1991; Ffawser &
Codd, 1992) may have a role in determining the
susceptibility or resistance of Trichodesm ium to grazers
(Ffawser et a l, 1992).
A rapid disappearance of Trichodesm ium blooms has
been observed in the natural environment. Though the
grazing action of Zooplankton is considered a potential
cause, recent observations (Ohki, 1997) suggest that
Trichodesm ium harbours a temperate virus leading to lysis.
As for the picoplanktonic Synechococcus (Suttle & Chan,
1994), viruses may play an important role in this
component of the food web of the oligotrophic tropical
ocean (Fuhrman & Suttle, 1993).
There seems to be little doubt that Trichodesmium is the
principal source of N 2 fixation in marine pelagic eco­
systems, contributing an estimated 80 Tg (Capone et a l,
1997) of fixed nitrogen per year, which could support up
to half of the new production in oligotrophic oceans (Karl
et a l, 1997).
Richelia intracellularis an d other cyanobacteria—diatom
sym bioses
Two types of cyanobacteria—diatom symbioses are com­
mon in the tropical marine plankton. The most frequently
reported is the association of the heterocystous fila­
mentous cyanobacterium generally referred to as Richelia
intracellularis Schmidt (Nostocaceae) with the diatom
genera R hizosolenia, H em iaulus, Bacteriastrum and C haeto­
ceros (Villareal, 1992). Besides R . intracellularis, an ad­
ditional taxon, C alothrix rhizosoleniae (Rivulariaceae), was
described by Lemmermann (1905). The similarity of the
two symbionts may have led to misidentifications and it
would be interesting to establish their genetic relationship.
R. intracellularis has short unbranched filaments with
heterocysts at one end or, less commonly, both ends.
There are usually two to four filaments per diatom cell but
the number increases with the size of the host (up to 32;
L. H offm ann
Sundström, 1984). The cyanobiont is usually located at
the apex of the host R hizosolenia cell outside the host
cytoplasm and there is no evidence for the presence of gas
vesicles Qanson et al., 1995a). The filament breaks into two
halves, one half migrating into each daughter cell (Taylor,
1982). The division cycles of the diatom host and of the
R ichelia symbiont seem to be largely uncoupled (Villareal,
1989).
R ichelia is primarily found in warm tropical and
subtropical waters, with a latitudinal range from approxi­
mately 38°N to 36°30'S (Sournia, 1970; Villareal, 1992).
Its abundance varies with season, being low in winter (10
cells V1) and high in late summer (IO4 cells V1) in the
central N orth Pacific gyre (Venrick, 1974).
Together with T richodesm ium these intracellular diatom
cyanobionts contribute to nitrogen fixation in oligo­
trophic tropical oceans (Mague et a l, 1974; Venrick, 1974;
Carpenter & Romans, 1991). Nitrogenase is found only in
heterocysts in R ichelia and nitrogen is fixed during the day
with rates ranging up to 18 m g N m-2 day-1, supporting
up to 36% of total phytoplankton production during
some blooms (Sellner, 1997).
A second type of symbiosis occurs between unicellular,
coccoid cyanobacteria and the diatom genus N eostrepto­
theca, an association for which few data are available
(Villareal, 1992).
Synechococcus and Prochlorococcus
Picoplanktonic cyanobacteria are an important component
of the marine plankton community (e.g. Ferris & Palenik,
1998). Biomass and photosynthesis measurements in
different tropical and equatorial oceans show that the bulk
of the chlorophyll a is in organisms of less than 1 ¡um and
3 ¡um respectively, and that this contributes 20-90% of
the photosynthetic productivity (e.g. tropical N orth
Atlantic: Platt et a l, 1983; eastern tropical Pacific Ocean:
Li et a l, 1983; subtropical Ffawaiian waters: Takahashi &
Bienfang, 1983). These cyanobacteria are an important
food source for planktonic heterotrophic flagellates and
ciliates, as well as macroinvertebrates (Yahel et a l, 1998).
The two important picoplanktonic groups are Synecho­
coccus, discovered 20 years ago (Waterbury et a l, 1979;
Johnson & Sieburth, 1979), and Prochlorococcus (Chisholm
et a l, 1988; Chisholm et a l, 1992), identified 10 years ago.
Prochlorococcus is a unicellular oxygenic photosynthetic
prokaryote that contains divinyl chlorophyll b as its main
pigment (Goericke & Répéta, 1992) rather than the
phycobiliproteins typical of cyanobacteria. At least two
ecotypes, adapted to grow at either low or high light
intensities, can be distinguished (Moore et a l, 1998).
While the coccoid Synechococcus is virtually ubiquitous
in all marine environments, ranging in abundance over
three orders of magnitude from 500 to 500 000 cells ml-1,
Prochlorococcus is virtually ubiquitous in the latitudinal
band 40°N—40°S where it comprises a significant pro­
portion of the photosynthetic biomass (Campbell et a l,
1994). N orth of 40°N and south of 40°S it can still be
376
found but its concentrations decline fairly rapidly
(Partensky et a l, 1999). It is found throughout the photic
zone, but in contrast to Trichodesm ium often dominates the
deep chlorophyll maximum at densities of IO4—IO5 cells
ml-1 (Post & Bullerjahn, 1994). It was suggested (Vaulot et
a l, 1995) that, in contrast to Synechococcus, Prochlorococcus
may not be severely limited by nutrients, including iron.
Geographical distribution of tropical cyanobacteria
The study of the distribution of cyanobacteria is hampered
by difficulties in recognizing the different taxa due to their
simple morphology. To date, only floristic lists using the
traditional geitlerian approach and Drouet's system
(Drouet, 1981) (e.g. Ffumm & Wicks, 1980; Zaneveld,
1988) have appeared in the literature. However, it has
been shown that the latter system does not reflect the
natural cyanobacterial diversity (e.g. Stam, 1978; W ater­
bury & Stanier, 1978). The main identification guide is still
Geitler (1930—2), which mostly deals with taxa described
from temperate regions. M any taxonomists working on
tropical collections and encountering populations which
did not correspond well to any described species often
simply referred these to the most similar taxon known
from temperate regions (Komárek, 1985). Such mis­
interpretations led to an overestimate of the distribution
area of many species originally described from temperate
zones. This situation will improve with the new edition of
the Süssw asserflora von M itteleu ro p a , which also includes
non-European species as is already the case in the first
published part treating the unicellular cyanobacteria
(Komárek & Anagnostidis, 1999). Notwithstanding these
methodological difficulties, it seems that apart from
cyanobacterial species with a (sub)cosmopolitan distri­
bution (e.g. L y n g b y a aestuarii, M icrocoleus chthonoplastes
Gomont), as confirmed by a phenotypic and phylogenetic
analysis of M . chthonoplastes by Garcia-Pichel et al. (1996),
some seem to be limited almost exclusively to warm­
water regions (e.g. the planktonic genera Trichodesm ium
(Capone et a l, 1997) and Prochloroccus (Partensky et a l,
1999) and the benthic genera Prochloron (Lewin & Cheng,
1989), H erp yzo n em a and H o rm o th a m n io n (Hoffmann,
1993)). The distribution of these taxa suggests that
temperature is probably a major factor limiting their
distribution (Hoffmann, 1994). This has been confirmed by
culture studies, for example, of tw o clones of the genus
Prochlorococcus that showed minimum grow th tempera­
tures of 15 and 12.5 °C, respectively (Moore et a l, 1995).
In the same way, the growth and activity of the genus
Trichodesm ium , which is occasionally found in waters
colder than 20 °C, are usually restricted to waters above
20 °C (Capone et a l, 1997).
Conclusions
As photosynthetic organisms, cyanobacteria sensu lato are
important contributors to benthic and open ocean primary
production, but their main role in tropical marine eco­
systems appears to be as nitrogen fixers. O f primary
377
Tropical marine cyanobacteria
importance in the often oligotrophic tropical oceans is the
non-heterocystous, planktonic bloom-forming Tricho­
desm iu m . N 2 fixation associated with Trichodesm ium prob­
ably represents a major nitrogen source to the marine and
global nitrogen cycle. Tropical marine ecosystems are
characterized by a specific cyanobacterial flora and nature
seems to have provided all possible combinations of
photosynthetic pigments, thus presenting interesting
model systems for the study of the evolution of plastids.
The largely unknown biodiversity, especially in the less
accessible infralittoral, may also in the future be an
important renewable source for hitherto undescribed
bioactive compounds, some of which may have potential
as antibiotics, antitumour agents and related pharma­
ceuticals (Rossi et al., 1997).
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A cknowledgem ents
p o lita n cy a n o b a c te riu m . A p p l. Environ. M ic ro b io l, 62 : 3 2 8 4 —3 2 9 1 .
The author is a research associate of the Belgian National
Fund for Scientific Research whose financial support is
also acknowledged in the framework of FRFC grants
2.9006.86, 2.9001.90 and 2.4521.96 which allowed the
author, in cooperation with professor V. Demoulin, to get
acquainted with the tropical marine cyanobacteria of
Papua N ew Guinea.
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