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water level of the lagoon. However storms and cyclones dislodge corals and set them down at a higher elevation, where the living coral dies. Such exposed boulders are the favoured sites of several species of nitrogen-tixing cyanobac-teria, such as Calothrix corallina and Scytonema sp. (Larkum et al., 1988a).
Finally inside the reef flat there is generally to be found a lagoon with a sandy bottom. Many cyanobacteria are found on the bottoms of such lagoons, although grazing by a multitude of grazing animaIs means that their presence is often not readily apparent.
PHYTOPLANKTON
THE CY ANüBACTERIA OF CORAL REEFS
Figure 7. Trichodesmiul11 erythraeum at a magni-fication of 1200 x, show-ing bundles of trichomes.
Photograph taken by J.O'Neill.
See color plates at the end of the volume.
Bulletin de l'/I1Sliful océanographique, Monaco, n° spécial19(1999)
Figure 8. A large Tricho-desmiwn bloom on the Great Barrier Reef (Capri-cornia Section) (area bet-ween Swains Reefs and Capricorn Group of Reefs) stretching for several hundred kilometers.
Taken by NASA astro-naut from space. Permis-sion of National Space and Aeronautics Admin-istration, USA.
155
ENVIRONMENT: ECOLOGY AND GLOBAL CHANGE
Nitrogen fixation
Trichodesmium spp. are ail non-heterocystous, nitrogen fixing cyanobacte-ria (heterocysts are specialised cells, where nitrogen fixation takes place, on filaments of certain cyanobacteria). Trichodesmium spp. can form very large blooms in the world's tropical oceans (Fig. 8) and thus large quantities of atmospheric dinitrogen can be injected into water bodies by this means. Very little is known of the triggers for such blooms but it can be assumed that P availability is a very important factor. In any case since Trichodesmium blooms are a common feature in waters off coral reefs (Glibert & O'Neill, this book) it may be assumed that P is available in sufficient quantities to sus-tain the blooms for significant periods of time. This is consistent with the pro-posaI that such waters are generally Iimited by the availability of inorganic nitrogen species. Thus the ability of Trichodesmium to fix atmospheric nitro-gen is ail important. There may also be other cyanobacteria present in such waters, which contribute additionally to nitrogen fixation. However there is
!iule documentation of this subject.
BENTHIC CYANOBACTERIA Nitrogen fixing cyanobacteria
The greatest role for cyanobacteria in the benthic communities of coral reefs is nitrogen fixation. Table 1 !ists the results of a number of studies which support the conclusion that there are many benthic cyanobacteria which carry out nitrogen fixation and that N2fixation by these organisms contributes mas-sive inputs of nitrogen into the food chains of coral reefs. The cyanobacteria involved maybe heterocystous filaments (e.g. Calothrix spp., Fig. 9), non-het-erocystous filaments (as in sorne Lyngbya spp.) or unicellular forms (as in Aphanothece spp., Fig. 10). In shallow reef systems dominated by shallow limestone communities, such as at One Tree Reef (Great Barrier Reef) results have indicated that nitrogen fixation contributed up to 15% of the total nitro-gen needs of the primary production of the reef (Larkum et al., 1988a).In a deep coral atoll lagoon at Tikehau (French Polynesia) similar calculations indicated an even greater contribution for the benthic communities (Charpy-Roubaud et al., 1997). However, in the latter situation the major primary pro-duction came from the phytoplanktonic cyanobacteria (Synechococcus sp., Charpy-Roubaud et al., 1997) in the water column. As explained in section 2 the overall budget in this situation is unclear.
Many of these Nrfixing species also play a role in structuring the epilithic algal community and in providing fixed carbon to many food chains through their high productivity.
Non-nitrogen fixing cyanobacteria
Il is becoming clear that more and more cyanobacteria are being shown to be capable of fixing atmospheric N2.Thus it is unclear how many non-N2 156 Bulletin de l'Institut océanographique, Monaco, n° spécial 19 (1999)
THE CY ANOBACTERIA OF CORAL REEFS
Figure 9. Filaments of the heterocystous nitrogen fixing cyanobacterium,Calothrix sp., from One Tree Island, Great Barrier Reef.
Figure 1O.Ap/1anothece sp., a nitrogen fixing unicellularcyanobacteriumofcoral reefs.
See color plates at the end of the volume.
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Table1.Comparison of nitrogen fixation rates of various communities of coral reefs.
Place Methods mgm-2 Source
day-l
Barbados C2H2red;15N2 1.8 Patriquin&Knoweles (1975) GBR (Central) C2H2red 1.1-8.5 Wilkinson et al. (1984) Same sites (muds) C2H2red 4.4-8.6 Corredor& Capone (1985) Same sites (sands) C2H2red 0.3-2.4 Corredor&Capone (1985)
on
(sand) C2H2red;15N2 0.25-0.5 Larkum et al. (l988a) Bermuda (sand) C2H2red 0.13-4.08 D'Neil& Capone (1989) Puerto-Rico C2H2red 0.71-5.17 D'Neil& Capone (1989) San Salvador C2H2red 0.07-0.69 D'Neil& Capone (1989) Australia C2H2red 0.2-1.3 D'Neil& Capone (1989) Australia C2H2red; 15N2 2.7-6.7 O'Donohue et al. (1991) GBR (sand) C2H2red 3.36 (c) Capone et al. (1992) Eilat (Red Sea), sand C2H2red 32.79 Shashar et al. (1994) Tikehau (Iagoonal sand) C2H2red;15N2 0.4 - 3.9 Charpy-Roubaud et al. (1997) DT!, Limestone C2H2red;15N2 3.12-6.22 (c) Larkum et al. (1988) Eilat, Limestone. C2H2red 93.16 (c) Shashar et al. (1994)Tikehau (Limestone) C2H2red;15N2 2.12 Charpy-Roubaud et al., in press DT! (beach rocks) C2H2red;15N2 0.19-0.38 (c) Larkum et al. (1988a)
Lizard Island (beach rocks) C2H2red;15N2 1.9-8.4 Burris (1976)
Tikehau (beach rocks) C2H2red;15N2 1.4 - 8 Charpy-Roubaud et al. (1997) Tikehau (ES) C2H2red;15N2 1.44 Charpy-Roubaud et al. (1997) Tikehau (EM) C2H2red;15N2 8 Charpy-Roubaud et al. (1997) GBR=Great Barrier Reef; OTI
=
One Tree Island; EM=
exposed mats; ES=
exposed beach sand.Eilat is in the Gulf of Aqaba, Red Sea; Tikehau is in French Polynesia; One Tree Island and Lizard Island are on the Great Barrier Reef.
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fixing cyanobacteria actually exist. Little attention has been focused, up ta the present time, on roles of cyanobacteria, other than N2fixation.Itseems likely that a number of non-N2 fixing cyanobacteria do exist and that these play various, but little-studied, roles on coral reefs. These gaps in our knowledge need serious attention.
In addition to their presence on the abundant limestone surfaces cyanobac-teria are also present on the sand surface of lagoons and the outer slope and also as epiphytes on algae and benthic animais. For example, Laurencia spp.
(Rhodophyta) can be densely coated with Lyngbya majuscula at times and high rates of nitrogen fixation have been observed (unpublished obs.). The contribution of such communities have not been fully characterised. In terms of primary production the cyanobacterial communities of lagoon sand sur-faces are very important because they are often the predominant algae present. However because these communities are tumed over rapidly, by a variety of grazers, such as holothuria, mollusca, and crustacea, they are rarely abundant and have not attracted the attention that they deserve.
Calcifying and Carbonate-Binding Cyanobacteria
Beach rock is one of the typical features of many coral cays (Fig. Il).
Large consolidations of limestone occur on the beach at about mid-tide level.
This beach rock may be extremely eroded, the result being pitted structures which may be several metres in depth and width, but in other cases beach rock is smooth and coated with a slime of algae. There has been much discus-sion as to the origin of beach rock. Close inspection shows that they are com-posed of consolidated fragments of weathered corallimestone. Cyanobacteria are abundant both on the surface and as boring algae in the first few millime-tres of rock. The important question is how the beach rock is formed. A recent investigation concluded that cyanobacteria were not essential agents in lithi-fication (Meyers, 1987). Other investigations have concluded that cyanobac-teria are a) agents of lithification and binding (Davies& Kinsey, 1973) and b) agents of dissolution (Krumbein, 1979).
BORING ALGAE
A well-recognised boring alga of limestone surfaces on coral reefs are spe-cies of the genus Ostreobium (arder: Caulerpales; Division: Chlorophyta) (Fork& Larkum, 1989). However in addition, a number of cyanobacteria have also been identified (Le Campion-Alsumard et al., 1995; Charpy-Roubaud et al., this volume). A scanning electron microscope view of the appearance of these organisms in situ is shown in Fig. 12. The activities ofthese algae are not weil defined. Presumably for much of the time they exist under low light conditions because the epilithic algal community absorbs a major portion of the light. Our own measurements of light penetration show that light is reduced to below 0.1%at a depth of 2 mm (Larkum& Koch, unpublished) but measurements of absorption by the epilithic algae community alone are not available.
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ENVIRONMENT: ECOLOGY AND GLOBAL CHANGE
Figure 11. Beach rock ar One Tree Island, Great Barrier Reef.
Figure 12. Scanning electron microscope image of endolithic organisms (Hye!la) in limesrone derived from coral on an exposed facies of a coral reef. Photograph raken by Le Campion-Alsumard.
160 Bul/elin de l'ln-'Iilui océanographique, Monaco, n° spécial19(1999)
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SYMBIOTIC CYANOBACTERIA
Cyanobacteria are well-known as symbionts of coral reef animals. They are found as endosymbionts in radioJaria, Pori fera (sponges), and Ascidia (ascidians or tunicates). While cyanobacteria are found as symbionts in hydrozoans, there is no substantial report of their presence in either hard or soft corals, where their place has been taken by zooxanthellae.
Many sponge-cyanobacterial symbioses have been recorded (Wilkinson, 1978, 1980; Larkum et al., 1988b). In many of these it appears that the sponges augment their heterotrophic feeding activities by the autotrophic activities of the cyanobacteria symbiont, part of the fixed carbon being passed on to the host (Cheshireet al., 1997). There are other sponge-cyanobacterial associations, which are obligate and strongly autotrophic. Cyanobacterial genera found to undergo symbiosis in sponges include:Anabaena, Aphano-capsa, Oscillatoria, Synechocystis, Phormidium.
Most of these are typical cyanobacteria. But sorne have interesting proper-ties. In a number of largely deep-water sponges a group of cyanobacteria occur which possess a different range of phycobiliproteins to that found in the majority of cyanobacteria. In the latter the phycourobilin chromophore is found in addition to the more common phycoerythrobilin chromophore (Lar-kum et al., 1987; Larkum et al. 1988b) (Fig. 13). This is an adaptation for more efficient light harvesting in these deep-water forms.
Figure 13. Electron microscope view of a filament of the symbiotic cyanobacterium Oscillaloria spong-elliae found in the hostcells of the sponge Dysidea herbacea. (Photo-graph taken by G.c. Cox).
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CYANOBACTERIAL MATS AND STROMATOLITES
Cyanobacterial mats occur in many regions of the world ranging from polar regions to the tropics They have been variously defined (Cohen el al., 1976). In the general sense they are associations of organisms dominated by cyanobacteria but in association with photosynthetic bacteria, sulphur bacte-ria and other microorganisms. They generally form fiat, extensive mats, which are several millimetres in thickness on sand or mud. These mats occur rarely on coral reefs. More common are cyanobacterial cushions which can be common on the ftoor of coral reef lagoons (Charpy-Roubaud el al., 1997) (Fig. 14). Also found on coral atolls are freshwater or brackish water mats known as Kopara (DeFargeel al., 1994; Trichet& Defarge, this book). These Kopara mats form on the raised surface of the atoJJ and are thus isolated from the lagoon and the seawater on the outside of the atoll. They are often found in muddy pools and are dominated by cyanobacteria in association with other microorganisms. In deeper strata of the mats calcium precipitation appears to occur and so a comparison with stromatolites has been attempted (Charpy-Roubaud elal., this book).
Figure 14. A cyanobacterial cushion at Tikehau lagoon. Photograph taken by C.Charpy-Roubaud.
Stromatolites are large limestone boulders (up to 1 m across) (Fig. 3) which are formed by cyanobacteria and other organisms on their surface.
Weil known stromatolites occur in Baja Califomia and in Shark Bay, Western Australia. More rarely stromatolites occur in areas where corals are found such as the Bahamas (Pauliel al., 1992); but they are not now found generally on coral reefs, unless under the name of beach rock (see "Calcifying and Car-bonate-Binding Cyanobacteria", above). However, there is a certain amount 162 Bulletin de l'Institut océanographique, Monaco, n° spécial 19 (1999)
THE CY ANOBACTERIA OF CORAL REEFS
of evidence to suggest that stromatolites or stromatolitic deposits played a more important role on earlier Quatemary coral reefs (Camoin & Montag-gioni, 1994). Furthermore as pointed out in the "Introduction", stromatolites were the community which took the place of coral/stromatoporoid reefs right up to Cambrian times.
PATHOGENIC ORGANISMS
A number of pathogenic cyanobacteria probably exist on reefs. Black band disease of corals is definitely due to the cyanobacterium Phormidium coral-lyticum in association with Beggiatoa spp. (Peters, 1993; Richardson, 1996).
This disease has affected quite large amounts of reefal corals in places and as its name implies spreads across coral communities as a front with a black band Jeaving dead coral skeletons in its wake.
EXOTIC ORGANISMS Prochloron didemni
Prochloron was discovered in 1975 (see Lewin, 1977; Lewin & Chang, 1989) as a symbiont in didemnid ascidians from tropical mangrove roots and on coral reefs (Fig. 15). It is unique in being a prokaryotic oxygenic pho-totroph with chlorophyll b as well as chlorophyll a. Although early specula-tion placed it on the evoluspecula-tionary pathway to green algae recent phylogenetic determinations have placed it within the cyanobacterial clade (but distinct from two other more recently discovered organisms, which also possess sim-ilar characteristics - Prochlorothrix and Prochlorococcus; however see Larkum in press).
Since the first discovery more than 25 didemnid ascidian species have been shown to have Prochloron (Lewin & Chang, 1989). In most cases the
asso-Figure 15. Photomicroscope image of Prochloron cells together with host ascidian cells.
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ENVIRONMENT: ECOLOGY AND GLOBAL CHANGE
ciation is extracellular in the effluent cavity of ascidians from tropical man-grove roots and on coral reefs. However a number of superficial associations have been discovered. Since the early discoveries more than 25 didemnid ascidian species have been shown to have Prochloron although it is not estab-lished yet whether these are ail from the single species, Prochloron didemni (Lewin& Chang, 1989).
Acaryochloris marina
Acaryochloris marina was discovered in 1997 and is a prokaryotic oxy-genic phototroph, which contains mainly chlorophylldwith small amounts of chlorophyll a and magnesium-2,4-divinyl phaeporphyrin monomethyl ester and phycobiliproteins (Miyashita et al., 1996). This organism is presently unc1assified but preliminary data from SSU RNA indicate that it falls within the cyanobacterial clade (E. Moerschel pers. corn).
Acaryochloris occurs in Lissoclinum patella and other didemnid ascidians, which harbour Prochloron didemni. In our studies on the Great Barrier Reef, Acaryochloris occurs in Lissoclinum in very low quantities and Prochloron is the major symbiont.Itis therefore likely that Acaryochloris exists in a special niche, which is possibly in the test, but this has not been fully proven.
The discovery of Acaryochloris indicates that there may be more oxygenic prokaryotes still waiting to be discovered.
CONCLUSIONS
Cyanobacteria play a crucial role on coral reefs even though they may be inconspicuous (Figs 5& 6); if for any reason they were to be exterminated in the present world coral reefs would cease to exist as we know them.Itis the role of nitrogen fixation, which is most important in this respect. But other roles - as symbionts and as boring algae - wouId also cause a dramatic change in structure of reefs.
Ironically cyanobacteria played a pivotai role in earlier symbiotic associa-tions and indeed generated the plastids according to the widely held endo-symbiotic hypothesis but have been superseded in corals by dinoflagellate algae. The explanation of this ("Why dinoflagellates and not cyanobacteria?") raises many interesting questions and possible lines of research. The disco-very of Prochloron and Acaryochloris and the possibility that more exotic organisms will be discovered on coral reefs in the future is another indication of the long history of this ancient group. Future research will undoubtedly be concemed with this important area.
Other important areas of future research will be concemed with the role of Trichodesmium spp. in the nitrogen nutrition of coral reefs, the role of cyano-bacteria as primary producers and the role of cyanocyano-bacteria in the cemen-tation and dissolution of coral substrates by surface and boring algae. In addition, in any prediction of the future, we can expect (and hope for) a few surprises.
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