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Coral Bleaching and Mucus Release 

NOTE: The following letter and response clarify the important role of mucus in coral reef ecosystems presented in a recent paper by Wild et al., and the effects of bleaching on them. They were submitted to NATURE, which declined to publish them as "not being of sufficient interest to the scientific community". As we disagree, in cooperation with Dr. Wild and colleagues we are circulating the exchange to those concerned about the implications for reef ecology. 

Letter to Nature: 

Thomas J. Goreau, Global Coral Reef Alliance, 37 Pleasant Street, Cambridge MA 02139, 617-864-4226, goreau@bestweb.net 

James Cervino, Department of Marine Science, University of South Carolina, Columbia, SC 29073, 917-620-5287, cnidaria@earhlink.net 

Raymond Hayes, College of Medicine, Howard University, Washington DC 301-585-5892, rhayes@Howard.edu 

Sir:

Wild et al. (Nature 428:66-70; 2004) show that coral mucus functions as an energy carrier and particle trap within a tropical reef ecosystem and demonstrate its important role in nutrient recycling. However, several important points need further explanation and suggest that these measurements may be atypical. 

First, while some corals may constantly secrete mucus, few do so at a constant rate, as stated.  Copious mucus release is the first visible sign of a generalized response to environmental stress (Helgol. Meeresunters. 37: 113-137, 1984; Revista de Biología Tropical (5):173-185, 1998), including sediment and freshwater (Science 145: 383-386, 1964), aerial exposure (which was used to determine mean mucus production in the paper), cyanide exposure (Mar Poll Bul 46: 573-586, 2003), and coral bleaching (Sci. Rep. Gr. Barrier Reef Exped. 1928-1929 (1), 135-176.

1931 ; Science 145: 383-386, 1964; Coral Reefs vol. 12 pp. 1-17,

1993). 

Secondly, all the photographs, including the cover, show corals that are clearly bleaching. However, the authors do not note (either in the text or in Table 1) that the corals were bleached, nor do they mention that most of this work was conducted during the most intense coral reef bleaching event to have ever taken place on the Great Barrier Reef (GBRMPA, 2002). Corals that are thermally bleached have expelled their symbiotic zooxanthellae and have produced copious amounts of mucus, which would explain the high levels of mucus release that the authors observed. Increased mucus release occurs before corals visibly pale. This would also explain the dense mucus "floc", which is typical of severe stress, mass bleaching, or mass spawning events, which may also have been prematurely triggered by severe thermal stress.  

Thirdly, bleached corals are deficient in the chemical precursors normally released by zooxanthellae and used for coral mucus synthesis, so the biochemical composition of their mucus abnormal (Proc R Soc London Ser B 177: 237-250, 1971; Limnol  Ocean,19; (5) 810-814,1974;  Mar Biol. 79: 27-38,1984). This alters the microbial flora living on it (Proc Amlc 27:26-34). 

In summary, we believe that the quantity and quality of coral mucus release and its role as a microbial substrate is highly variable in space and time, and fluctuates with the varying stresses corals are exposed to. Therefore, further research is warranted to more fully quantify the importance of mucus cycling that Wild et al. demonstrate. 

REFERENCES

Battey, J.F., and J.S., Patton. (1984). A reevaluation of the role of glycerol in carbon translocation in zooxanthellae-coelenterate symbiosis. Mar Biol. 79: 27-38. 

Benson  A.A., L., Muscatine (1974). Wax in coral mucus: Energy transfer from corals to reef fishes. Limnology  Oceanography, vol 19; (5) 810-814.  

Cervino  J.M., R.L. Hayes, M. Honovich, T.J.,Goreau S. Jones, P.J. Rubec (2003). Changes In Zooxanthellae Density,  Morphology, and Mitotic  Index  in  Hermatypic  Corals and Anemones  Exposed to Cyanide.  Mar Poll Bul  46: 573-586. 

Glynn P.W., (1993). Coral reef bleaching-ecological perspectives. Coral Reefs vol. 12 pp. 1-17. 

Goreau T.F., (1964). Mass expulsion of zooxanthellae from Jamaican reef communities after Hurricane Flora. Science 145: 383-386. 

Great Barrier Reef Marine Park Authority,(2002). Coral Bleaching Summary,(http://www.gbrmpa.gov.au/corp_site/info_services/science/bleaching/01-02/final_report/index.html.) 

Hayes, R. L. and N. I. Goreau, (1998). “The significance of emerging diseases in the tropical coral reef ecosystem.” Revista de Biología Tropical 46(Supplement 5):173-185. 

Peters, E., (1984). “A survey of cellular reactions to environmental stress and disease in Caribbean scleractinian corals.” Helgol. Meeresunters. 37: 113-137. 

Ritchie, K.B., A. Jindal, R. L. Hayes, T. J. Goreau and G.W. Smith, (1994). Bacterial ecology of selected corals following the 1994 south central Pacific bleaching event. Proc AMLC 27: 26-34. 

Trench, R. K., (1971). The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. 11. Liberation of fixed 14C by zooxanthellae in vitro . Proc R Soc London Ser B 177: 237-250. 

Yonge, C.M. and A.G. Nicholls, (1931). Studies on the physiology of corals. IV The structure, distribution and physiology of the zooxanthellae. Sci. Rep. Gr. Barrier Reef Exped. 1928-1929 1, 135-176. 

RESPONSE BY DR. CHRISTIAN WILD 

Dear Madam or Sir:

We were notified by Goreau, Cervino and Hayes that they have submitted a note to Nature addressing our Nature letter “Coral mucus functions as an energy carrier and nutrient trap in the reef ecosystem” (Nature 428: 66-70, 2004). Goreau et al. raised some interesting points, however, we disagree with some of their interpretations of our work. Below, please find our reply to the comments of Goreau and colleagues. 

Sincerely, 

Christian Wild and co-authors 

Response to the comments of Goreau, Cervino and Hayes to our article “Coral mucus functions as an energy carrier and nutrient trap in the reef ecosystem (Nature 428: 66-70, 2004). Each citation from the letter by Goreau et al. (in italics) is followed by our reply to the respective comment. Citations in sequence as stated in the letter by Goreau et al. 

Goreau et al.: First, while many corals do constantly secrete mucus, few do so at a constant rate, as stated. 

We do say that corals constantly have to secrete mucus to protect themselves against fouling, desiccation and sedimentation (page 66, first paragraph, ref. 5-7), but we state clearly that this release is not constant as evidenced by our experiments with air exposure stress (see page 66, last paragraph and page 67, first sentence). 

Goreau et al.: Greatly elevated mucus release is the first visible sign of a generalized response to almost all stresses (Helgol. Meeresunters. 37: 113-137, 1984; Revista de Biología Tropical (5):173-185, 1998), including sediment and freshwater (Science 145:> 383-386, 1964), aerial exposure (which was used to determine mean mucus production in the paper), 

We did not use our container experiments with air exposure to “determine mean mucus production” as stated by Goreau et al. This is clearly stated in the text: on page 66, last paragraph, we describe the mucus production of submersed corals and on page 67, first paragraph we show the results of our container incubations with air exposure. Also, the mucus release rates that we used for our budget calculations (summarised in figure 3) are only based on the beaker incubations to stay conservative (this is also stated in the article text on page 68, last paragraph and page 69, first paragraph). Two independent beaker incubation experiments were conducted, one in 2001 and the other in 2002 (both in the Australian summer). For these experiments and the compositional mucus analyses only unbleached corals were used, for which we have photographic proofs. The results of the experiments in 2001 and 2002 are very similar and also comparable to the range of release rates observed by other authors at other times and locations (see Table 1). 

We certainly agree that mucus release fluctuates because of a range of environmental stress factors like high temperature, salinity change, pollution (Loya & Rinkevich 1980, Kato 1987), turbidity (Rublee et al. 1980, Telesnicki & Goldberg 1995) and sedimentation (Hubbard & Pocock 1972, Schuhmacher 1977). Our container experiments including air exposure as environmental stress factor for the incubated corals show higher mucus release rates than the beaker incubations (see Table 1 below; method, see ref. 26 in Nature letter). A new publication (Wild et al., submitted to MEPS: Quantitative and qualitative analyses of coral mucus release and its influence on nutrient fluxes in carbonate sands) addresses this subject in detail. 

Goreau et al.: Secondly, all the photographs, including the cover, show corals that are clearly bleached; however, the authors do not note (either in the text or in Table 1) that the corals are bleached, nor do they mention that most of this work was conducted during the most intense bleaching event to have ever taken place on the (GBRMPA, 2002). 

Our study is based on work conducted in the years 2001 and 2002 (in approximately equal amounts), of which only year 2002 was a year of extensive bleaching events in the Great Barrier Reef. During our expedition to Heron Island in January 2002, however, we could only observe minor bleaching, probably because we did our investigations at the very beginning of this bleaching period. The Great Barrier Reef Marine Park Authority reports that in January 2002 the first signs of bleaching were recorded on many locations within the Great Barrier Reef (see more details at the website http://www.gbrmpa.gov.au/corp_site/info_services/science/bleaching/01-02/final_report/index.html) and Heron Island is located at the southern end of the Great Barrier Reef where temperatures are usually lower. 

At Heron Island we recorded in 2002 that some of the corals were partially bleached like it is seen on the Nature cover. The figure on the cover page is the same at in Fig. 1a, but enlarged and enhanced in brightness. The water cover in Fig. 1c, from our point of view, does not permit an assessment whether any of the depicted corals were bleached, thus, there is just one photograph of corals displayed in the whole letter. It is therefore disproportionate to write, “all the photographs show corals that are clearly bleached”. We submitted the photograph to Nature because of the good quality and also because the mucus strings are very clearly visible. However, we have a range of other photographs showing unbleached corals with similar mucus strings attached. These photographs were taken at the same time and can be provided upon request. We observed mucus strings on unbleached corals frequently also at other locations than the GBR. One of those pictures was made in the Northern Red Sea and can be seen on the Science Magazine website at the following link: http://sciencenow.sciencemag.org/cgi/content/full/2004/305/1 

Goreau et al.: Corals that are thermally bleaching expel their symbiotic zooxanthellae and produce copious amounts of mucus, which would explain the high levels of mucus production that the authors observed. This would also explain the dense mucus "floc", which is typical of severe stress, mass bleaching, or mass spawning events (which may have been prematurely triggered by severe thermal stress) 

Bleaching may enhance mucus production; however, bleaching is not necessary to induce massive mucus release from corals as can easily be demonstrated by exposing healthy corals to air. Our container experiments quantified the latter process. Massive mucus release as a consequence of air exposure is also observed in years without any coral bleaching and was also reported from other reef environments in Australia, Madagaskar, the Red Sea and Hawaii (Krupp 1984, Romaine et al. 1997). Subsequent formation of floating mucus aggregations was also described for reef flats in Hawaii (Krupp 1984), thus this phenomenon is neither site-specific, nor necessarily connected to coral bleaching or atypical as stated by Goreau and colleagues. 

Goreau et al.: Thirdly, bleached corals are deficient in the chemical precursors normally released by zooxanthellae and used for coral mucus synthesis, so the biochemical composition of their mucus changes.  

The detailed mucus composition results are based on mucus samples from unbleached corals and collected in 2001 and 2002. Any possible bleaching effects do therefore not affect the samples. However, we agree that stress and bleaching may change the composition of coral mucus. 

Goreau et al.: In summary, we believe that the quantity and quality of mucus as a microbial substrate is highly variable in space and time, and fluctuates with the varying stresses corals are exposed to. Therefore, further research is warranted to more fully quantify the importance of mucus cycling that Wild et al. demonstrate. 

Our work focusing on one genus of corals (Acropora) only cannot claim to be sufficient to quantify mucus release and mucus composition in corals or the variability of mucus quantity and quality. The aim of our study was to demonstrate the recycling of coral mucus in the reef ecosystem and to show that the mucus, which is a dominant fraction of particulate organic matter in coral reefs (Johannes 1967, Marshall 1968), is a carrier of nutrients and efficient particle trap. Bleaching events may enhance this recycling loop; however, the mechanisms described in our letter to Nature (mucus dissolution, particle trapping, sedimentation, sedimentary filtration and degradation) are independent of such stress events. 

Table 1. Mucus release as carbon in comparison to other studies (modified after Wild et al., submitted to MEPS). The container experiment included exposure to air resulting in elevated mucus release rates. Numbers in brackets are standard deviations. 

REFERENCES 

 ADDIN ENBbu 码Hubbard JAE, Pocock YP (1972) Sediment-rejection by recent scleractinian corals: a key to palaeo-environmental reconstruction. Geol Rundschau 61:598-626

Johannes R (1967) Ecology of organic aggregates in the vicinity of a coral reef. Limnol Oceanogr 12:189-195

Kato M (1987) Mucus-sheet formation and discoloration in the reef-building coral, Porites cylindrica : Effects of altered salinity and temperature. Galaxea 6:1-16

Krupp DA (1984) Mucus production by corals exposed during an extreme low tide. Pac Sci 38:1-11

Loya Y, Rinkevich B (1980) Effects of oil pollution on coral reef communities. Mar Ecol Prog Ser 3:167-180

Marshall M (1968) Observations on organic aggregates in the vicinity of coral reefs. Mar Biol 2:50-55

Romaine S, Tambutte E, Allemand D, Gattuso JP (1997) Photosynthesis, respiration and calcification of a zooxanthellate scleractinian coral under submerged and exposed conditions. Mar. Biol. 129:175-182

Rublee P, Lasker H, Gottfried M, Roman M (1980) Production and bacterial colonization of mucus from the soft coral Briarium asbestinum. Bull Mar Sci 30:888-893

Schuhmacher H (1977) Ability of fungiid corals to overcome sedimentation. In: Proceedings of the Third International Coral Reef Symposium, Miami, Florida, p 503-509

Telesnicki G, Goldberg W (1995) Effects of turbidity on the photosynthesis and respiration of 2 South Florida reef coral species. Bull Mar Sci 57:527-539