1. Graduate School of Engineering and Science, University of the Ryukyus, 1 Senbaru, Nishihara 903-0213, Okinawa, Japan
2. Young Researchers Club, Bandar Abbas Branch, Islamic Azad University, PO Box 79159-14 1311, Bandar Abbas, Iran
Author
Correspondence author
International Journal of Marine Science, 2013, Vol. 3, No. 38 doi: 10.5376/ijms.2013.03.0038
Received: 01 May, 2013 Accepted: 03 Jun., 2013 Published: 22 Jul., 2013
This is an open access article published under the terms of the
Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Kavousi et al., 2013, Mass Mortality of Porites Corals on Northern Persian Gulf Reefs due to Sediment-Microbial Interactions, Indonesia, International Journal of Marine Science, Vol.3, No.38 306-310 (doi: 10.5376/ijms.2013.03.0038)
Little information is available on coral diseases in the Persian Gulf; however, in the recent years, reports of coral diseases increased in particular from Iranian side of the Persian Gulf. In this paper we report a White Mat Disease resulting in mass mortality of Porites colonies at Hormuz Island. This outbreak infected 96% of all Porites colonies and killed 58±30% (mean ± SD) of all Porites tissues.
1 Introduction
Being among the most diverse ecosystems on the Earth, the world’s coral reefs have been threatened by global and local stresses over the last few decades resulting in vast destruction (Burke et al., 2011; Fisher et al., 2011). Disease has been among the most important contributors to the global degradation of coral reefs (Goreau et al., 1998; Weil et al., 2006; Bruno et al., 2007; Rosenberg and Kushmaro, 2011). Little information on the prevalence or types of coral disease, however, exists for the Indian Ocean including the Persian Gulf (Riegl and Purkis, 2012).
The Persian Gulf is known as one of the most extreme environments for coral reefs with high temperature fluctuations from 12℃ in winter (Sheppard et al., 1992) to 38℃ in summer (Baker et al., 2004), high salinity (up to 39 psu), high sedimentation rate, low depth (35 m in average with majority of coral reefs in depth <10 m) and low water circulation especially in the southern part of the Gulf (see Riegl and Purkis, 2012). In spite of being among the most tolerant coral reefs to thermal stress (Burt et al., 2011), coral reefs of the Persian Gulf encounter massive coral bleaching events due to temperature anomalies (Coles and Riegl, 2012; Kavousi et al., unpublished data). Moreover, 85% of the coral reefs in the Persian Gulf are considered threatened by local stresses (Burke et al., 2011). Furthermore, coral diseases have been recently reported as another serious threat to the coral reefs of the Persian Gulf.
Although little systematic and quantitative studies have been done in the Persian Gulf (Riegl and Purkis, 2012), in recent years, reports of recognized and uncharacterized coral diseases have increased, especially from the northern Persian Gulf including Larak, Qeshm, and Hengam Islands (Samimi-Namin et al., 2010; Kavousi and Rezai, 2011). In this paper, we report a White Mat Disease resulting in mass Porites mortality from Hormuz Island of the Persian Gulf.
2 Material and Methods
During a field survey around some Iranian islands of the Persian Gulf in late August and early September 2012, following a mass coral bleaching, an outbreak of a disease was observed on the reef-building corals of the east of Hormuz Island (27°03′N, 56°30′E; Figure 1). To estimate the benthic cover of reefs, 10-meter Line Intercept transects were established (n=9) at a depth of <4 m where majority of the reefs exist. The number of infected coral colonies was obtained by counting 100 coral colonies randomly. Photoquadrat method (n=70) was used to calculate the coral tissue mortality due to the white mats. Sedimentation rate in the area was obtained by using the accumulated sediments collected with 10-day-sediment traps following the methodology mentioned in Hill and Wilkinson (2004). Three rods with 3 sedimentation traps attached to each rod (9 traps in total) were hammered to three sides of the reefs; however, the data presented here are from 6 traps because the other three traps were lost. Sedimentation rate is reported as gr/cm²/day.
Figure 1 Map of the area including Hormuz Island where was examined in this study. SS= studied site in this study
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3 Results and Discussion
The main reefs of Hormuz Island, located at the east and 2-4 m deep, include as main reef-builders zoanthids and scleractinian corals for 59.79±15.95% (mean±SD) and 8.68±7.01% (mean ±SD) of substratum, respectively. The predominant coral genus in the area is massive Porites (more than 85% of the reef-building corals). High sedimentation rate is a permanent characteristic of this site (Figure 2 A) and a rate of 0.052±0.014 gr/cm²/day was measured. In spite of this high sedimentation, corals and zoanthids have appeared healthy during the last three years (Figure 2 B, personal observations); however, in summer 2012, the reef-building corals encountered coral bleaching (Kavousi et al., unpublished data) and outbreak of a disease that followed.
Figure2 A: Turbid waters due to high sedimentation around coral reefs at eastern Hormuz Island B: Deposition of sediments on live organisms such as corals and zoanthids as a permanent characteristic of this site
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Overgrowth of invasive organisms such as algae (Goreau et al., 1998; Barott et al., 2012) and pathogenicbacteria (Kline and Vollmer, 2011) leading to coral mortality is prevalent worldwide but mass coral mortality from sulfate reducing bacteria is a rare phenomenon that was recorded on reef-building Porites corals of Hormuz Island of the Persian Gulf in Summer 2012.
Whereas all coral colonies were affected by thermal stress (from partially bleached to fully-bleached), the Porites corals were overgrown by a white mat of bacteria (Figure 3 A and B) that infected 96% of all Porites colonies and killed 58±30% (mean ± SD) of all Porites tissues. The same phenomenon was also observed on several coral genera on the south of Hormuz and Larak Islands.
Figure 3 A: Mass mortality of Porites colonies at Hormuz Island due to bacterial mats B: White mat on a Porites colony C: White mats changed overlying black layers due to iron sulfide precipitation D: Photosynthetic sulfur and non-sulfur bacteria are probably responsible for pink and green colors
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Reports on post-bleaching coral mortality due to diseases are increasing worldwide (Bruno et al., 2007; Miller et al., 2009; Riegl et al., 2011; Bastidas et al., 2012). Although, coral reefs facing mild and sometimes severe bleaching can recover quickly (e.g. Goreau et al., 2000; West and Salm, 2003; Riegl et al., 2011), diseases can reduce resilience, coral cover, and reef resistance drastically for several years (Goreau et al., 2000; Rosenberg and Loya, 2004; Sutherland et al., 2004).
Massive Porites corals are known as the most tolerant corals to thermal stress (Goreau et al., 2000; Loya et al., 2001); however, the results of this study indicate Porites corals are still susceptible to the secondary effects of bleaching events including coral diseases. Moreover, reefs affected by coral diseases have less resistance and resilience (Goreau et al., 2000; Rosenberg and Loya, 2004) resulting in more likelihood of being overgrown by invasive organisms and competitors such as macroalgae and other reef builders; however, even under no visible stress, zoanthids are able to overgrow reef-building corals (Figure 4 A, B, C; J. Kavousi, personal observation). The reefs to the east of Hormuz Island are now dominated by zoanthids (59.79±15.95%). Whereas reef-building corals were highly affected by the recent bleaching event and its consequences, zoanthids showed no sign of bleaching or sickness. The shift from coral dominated reefs to non-scleractinian coral-dominated reefs due to climate change and its consequences were reported (reviewed by Norström et al., 2009; Bell et al., 2013). This may lead to local extinction of reef-building corals of the east of Hormuz Island under ongoing climate change.
Figure 4 Overgrowth of zoanthids on coral colonies including A: Favia B: Platygyra C: Porites at the east of Hormuz Island
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Sulfide oxidizing bacteria such as Beggiatoa, Thiothrix and Thioploca, etc. are suggested to be the dominant bacteria in the white mats (Jorgensen, 1977; Jorgensen and Postgate, 1982; Fenchel et al., 2012). A dark colored underlayer (Figure 3 C) that appeared at the white surface of affected tissues less than 24 hours after the first observations is probably due to iron sulfide precipitation. The pink and green colored underlayers observed on the majority of infected coral colonies (Figure 3 D) could be photosynthetic sulfur and non-sulfur bacteria; however, microbial examinations are needed.
Although sulfide oxidizing bacteria linked coral mortality was reported (Garrett and Ducklow, 1975; Mitchell and Chet, 1975), previous observations involved very localized coral mortality, often due to artificially induced stress in the laboratory or linked to sediment stress in the field (Weber et al., 2012).
Sulfide oxidizing bacteria are a visible epiphenomenon that is a result, not a cause, of mortality. Coral surface tissue smothered with fine-grained mud creates locally anoxic sites (Erftemeijer et al., 2012) that are colonized by anaerobic, heterotrophic sulfate-reducing bacteria. The Hydrogen Sulfide they produce then kills coral tissue (Weber et al., 2006; 2012). The sulfide-oxidizing bacteria live at the interface between the aerated water and the necrotic tissue, and oxidize Hydrogen Sulfide escaping from below with oxygen from above. They precipitate internal elemental sulfur granules (Jorgensen, 1977; Fenchel et al., 2012) that give them a distinctive white mat appearance (Richardson, 1998). The mat tends to trap and maintain anoxic condition (Jorgensen and Postgate, 1982) at the tissue surface (Miller and Richardson, 2012), hastening coral mortality. Thus the disease is a secondary microbial effect of sediment stress (Weber et al., 2012), not a primary pathogen that attacks coral tissue directly. The effects are worst where there is heavy sedimentation, especially coupled to organic loading (Weber et al., 2012), warm conditions, and weak water movement.
The increased number and outbreak of coral diseases reported from the Persian Gulf in the recent years may be evaluated as a sign of future frequent mass mortalities due to coral diseases which could result in reef degradation and coral extinctions. Therefore, it is necessary to monitor long-term effects of coral diseases along with doing histological and microbiological examinations in the Persian Gulf.
Acknowledgement
We thank Dr. T.J. Goreau for his professional comments to improve the manuscript. English editing was done by T. Goreau and T. McClelland.
Bell J.J., Davy S.K., Jones T., Taylor M.W., and Webster N.S., 2013, Could some coral reefs become sponge reefs as our climate changes? Global Change Biology, doi: 10.1111/gcb.12212
http://dx.doi.org/10.1111/gcb.12212
Bruno J.F., Selig E.R., Casey K.S., Page C.A., Willis B.L., Harvell C.D., Sweatman H., and Melendy A.M., 2007, Thermal stress and coral cover as drivers of coral disease outbreaks, PLoS Biology, 5: e124
http://dx.doi.org/10.1371/journal.pbio.0050124
Burke L.M., Reytar K., Spalding M., and Perry A., 2011, Reefs at risk revisited, World Resources Institute, Washington DC, USA
Coles S.L., and Riegl, B.M., 2012, Thermal tolerances of reef corals in the Gulf: A review of the potential for increasing coral survival and adaptation to climate change through assisted translocation, Marine pollution bulletin, 72: 323–332Erftemeijer P.L., Riegl B., Hoeksema B.W., Todd P.A., 2012, Environmental impacts of dredging and other sediment disturbances on corals: a review, Marine Pollution Bulletin, 64: 1737-1765
Fenchel T., Blackburn H., and King G.M., 2012, Bacterial biogeochemistry: The Ecophysiology of Mineral Cycling, Academic Press, pp. 312
Fisher R., Radford B.T., Knowlton N., Brainard R.E., Michaelis F.B., and Caley M.J., 2011, Global mismatch between research effort and conservation needs of tropical coral reefs, Conservation Letters, 4: 64-72
http://dx.doi.org/10.1111/j.1755-263X.2010.00146.x
Goreau T.J., Cervino J., Goreau M., Hayes R., Hayes M., Richardson L., Smith G., DeMeyer K., Nagelkerken I., Garzon-Ferrera J., Gil D., Garrison G., Williams E.H., Bunkley-Williams L., Quirolo C., Patterson K., Porter J., and Porter K., 1998, Rapid spread of diseases in Caribbean coral reefs, Revista Biologia Tropical, 46 Supl. 5: 157-171
Hill J., and Wilkinson C., (eds.), 2004, Methods for ecological monitoring of coral reefs, Australian Institute of Marine Science, Townsville
Jorgensen B.B., and Postgate J.R., 1982, Ecology of the Bacteria of the Sulphur Cycle with Special Reference to Anoxic-Oxic Interface Environments [and Discussion], Philosophical Transactions of the Royal Society of London B, Biological Sciences, 298, 543-561
http://dx.doi.org/10.1098/rstb.1982.0096
Kline D.I., and Vollmer S.V., 2011, White Band Disease (type I) of endangered Caribbean acroporid corals is caused by pathogenic bacteria, Scientific Reports, 1: 7
http://dx.doi.org/10.1038/srep00007
Miller A.W., and Richardson L.L., 2012, Fine structure analysis of black band disease (BBD) infected coral and coral exposed to the BBD toxins microcystin and sulfide, Journal of Invertebrate Pathology, 109: 27-33
http://dx.doi.org/10.1016/j.jip.2011.09.007
Miller J., Muller E., Rogers C., Waara R., Atkinson A., Whelan K.R.T., Patterson M., and Witcher B., 2009, Coral disease following massive bleaching in 2005 causes 60% decline in coral cover on reefs in the US Virgin Islands, Coral Reefs, 28: 925-937
http://dx.doi.org/10.1007/s00338-009-0531-7
Norström A.V., Nyström M., Lokrantz J., and Folke C., 2009, Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Marine Ecology Progress Series, 376: 295-306
http://dx.doi.org/10.3354/meps07815
Riegl B.M., Purkis S.J., Al-Cibahy A.S., Abdel-Moati M.A., and Hoegh-Guldberg O., 2011, Present limits to heat-adaptability in corals and population-level responses to climate extremes, PloS one, 6: e24802
http://dx.doi.org/10.1371/journal.pone.0024802
Samimi-Namin K., Risk M.J., Hoeksema B.W., Zohari Z., and Rezai H., 2010, Coral mortality and serpulid infestations associated with red tide in the Persian Gulf, Coral Reefs, 29: 509
http://dx.doi.org/10.1007/s00338-010-0601-x
Sheppard C.R.C., Price P., and Roberts C., (eds.), 1992, Marine ecology of the Arabian Region, Academic Press, London, England
Sutherland K.P., Porter J.W., and Torres C., 2004, Disease and immunity in Caribbean and Indo-Pacific zooxanthellae corals. Marine Ecology Progress Series, 266: 273-302
http://dx.doi.org/10.3354/meps266273
Weber M., de Beer D., Lott C., Polerecky L., Kohls K., Abed R.M.M., Ferdelman T.G., and Fabricius K.E., 2012, Mechanisms of damage to corals exposed to sedimentation, PNAS, 109: E1558-E1567
http://dx.doi.org/10.1073/pnas.1100715109
Weber M., Lott C., and Fabricius K.E., 2006, Sedimentation stress in a scleractinian coral exposed to terrestrial and marine sediments with contrasting physical, organic and geochemical properties, Journal of Experimental Marine Biology and Ecology, 336:18-32
http://dx.doi.org/10.1016/j.jembe.2006.04.007
West J.M., and Salm R.V., 2003, Resistance and resilience to coral bleaching: implications for coral reef conservation and management, Conservation Biology, 17: 956-967
http://dx.doi.org/10.1046/j.1523-1739.2003.02055.x