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A community change in the symbionts
of a scleractinian coral
following a natural bleaching event:
field evidence of
acclimatization
Alison Jones, Ray Berkelmans,
Madeleine van Oppen,
Jos Mieog, William Sinclair
Miall Island
Keppel Islands
Great Barrier Reef
Acropora millepora
Bleaching events
20022002 2006
The coral symbiosis
coral polyp
zooxanthellae
(algae)
‘coral bleaching’ is the
expulsion of the algal
symbiont
Symbiodinium ITS1 types
Type C2
Type D
Type C1
Type D* SSCP
The coral symbiosis
PhotosynteticallyPhotosyntetically
fixed carbonfixed carbon
lipids
lipidsCOCO22
CaCa
2+2+
Thermal tolerance
D
C2C2
C2/D
Coral mortality
Bleaching canBleaching can
eventually result ineventually result in
the death of thethe death of the
coral host andcoral host and
proliferation ofproliferation of
coral diseasecoral disease
(Douglas, 2003)(Douglas, 2003)
healthy coralhealthy coral
‘‘old’ dead coralold’ dead coral
recently deadrecently dead
or diseasedor diseased
Symbiont shuffling
Symbiont community shift
0
50
100
150
200
250
300
350
400
450
500
C2 D C1
0
5
10
15
20
25
30
35
C2 C1 D
-5
5
15
25
35
C2 C1 D
0
10
20
30
C2 C1 D
none
D
C2
C1
D*
2+
Type C2
Type D
Type C2/D
Type C1
19
21
23
25
27
29
31
33
35
37
39
Jan-01
Mar-01
May-01
Jul-01
Sep-01
Nov-01
Jan-02
Mar-02
May-02
Jul-02
Sep-02
Nov-02
Jan-03
Mar-03
May-03
Jul-03
Sep-03
Nov-03
Jan-04
Mar-04
May-04
Jul-04
Sep-04
Nov-04
Jan-05
Mar-05
May-05
Jul-05
Sep-05
Nov-05
Jan-06
TEMP
C
20062006
bleachingbleaching
eventevent
51%
5%
25%
6%
20022002
bleachingbleaching
eventevent
AIMS Halftide Rocks temperatures (meanAIMS Halftide Rocks temperatures (mean ± SD± SD °C)°C)
Chloroplast cell
membrane
Thylakoid
membrane
Thylakoid lumen
2H2O
O2 + 4H+
CYT B6f
complexPSII
H+
H+
PSI
Fd FNR
ATP
synthase
H+
ATP
ADP +ADP +
PP22NADP
+ 2H+
CO2
Calvin Cycle of carbon
fixation
Starch
synthesis
e-
LHC
DDC2C2
Physiological costs of adaptation?
Acknowledgements
This project made possible by support from
the
Australian Institute of Marine Science,
Central Queensland University
and
University of Groningen
Climate change
IPCC multi-model ensemble (Meehl, 2007)
↑ 2.0 – 4.5 °C
ReferencesBerkelmans, R. and M. J. H. van Oppen (2006). "The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change."
Proceedings of the Royal Society of London. Series B, Biological Sciences (1934-1990).
Done, T. (1992). "Phase shifts in coral reef communities and their ecological significance." Hydrobiologia 247: 121-132.
Done, T., P. Whetton, et al. (2003). Chapter 11: Global climate and coral bleaching on the Great Barrier Reef. Final report to the State of Queensland Greenhouse Task Force,
Department of Natural Resources and Mining, www.nrm.qld.gov.au/science/climate.html: 33.
Hoegh-Guldberg, O., P. J. Mumby, et al. (2007). "Coral reefs under rapid climate change and ocean acidification." Science 318(5857): 1737-1742.
IPCC, Ed. (2001). Climate change 2001: The scientific basis: Contribution of Working Group I to the third assessment report of the Intergovernmental Panel on climate change,
New York : Cambridge University Press, 2001.
Meehl, G. A., T. F. Stocker, et al. (2007). Chapter 10: Global climate projections. Climate change 2007: The Physical Science Basis, Contribution of: Working Group I to the
Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press.
Mieog, J. C., M. J. H. Van Oppen, et al. (in press). "Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR."
Mieog, J. C., M. J. H. Van Oppen, et al. (2007). "Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great
Barrier Reef: implications for symbiont shuffling." Coral Reefs 26(3): 449-457.
Mieog, J. C., M. J. H. van Oppen, et al. (in press). "Enormous potential for shuffling of algal symbionts in reef corals."
Muscatine, L. (1990). The role of symbiotic algae in carbon and energy flux in reef corals. Ecosystems of the world 25: Coral reefs. Dubinsky. New York, Elsiever. 25: 75-87.
Ostrander, G. K., K. M. Armstrong, et al. (2000). "Rapid transition in the structure of a coral reef community: The effects of coral bleaching and physical disturbance."
Proceedings of the National Academy of Sciences of the United States of America 97(10): 5297-5302.
Pittock, B., Ed. (2003). Climate Change: An Australian Guide to the Science and Potential Impacts, Australian Greenhouse Office.
Smith, C. (2004). The molecular and genetic basis for variation in thermal tolerance in a common reef-building species on the inshore Great Barrier Reef. Townsville, James
Cook University. PhD Thesis.
Ulstrup, K. E. and M. J. H. van Oppen (2003). "Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier
Reef." Molecular Ecology 12(12): 3477-3484.
van Oppen, M. J. H., F. P. Palstra, et al. (2001). "Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium
strains and host-symbiont selectivity." Proceedings of the Royal Society of London. Series B, Biological Sciences (1934-1990) 268(1478): 1759-1767.
Wakeford, M., T. J. Done, et al. (2007). "Decadal trends in a coral community and evidence of changed disturbance regime." Coral Reefs On-line First.
Wilkinson, C., Ed. (2004). Status of Coral Reefs of the World 2004. Townsville, Australian Institute of Marine Science.

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International Coral Reef Society Conference 2008 - Dr Ali Jones

  • 1. A community change in the symbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization Alison Jones, Ray Berkelmans, Madeleine van Oppen, Jos Mieog, William Sinclair
  • 5. The coral symbiosis coral polyp zooxanthellae (algae) ‘coral bleaching’ is the expulsion of the algal symbiont
  • 6. Symbiodinium ITS1 types Type C2 Type D Type C1 Type D* SSCP
  • 7. The coral symbiosis PhotosynteticallyPhotosyntetically fixed carbonfixed carbon lipids lipidsCOCO22 CaCa 2+2+
  • 9. Coral mortality Bleaching canBleaching can eventually result ineventually result in the death of thethe death of the coral host andcoral host and proliferation ofproliferation of coral diseasecoral disease (Douglas, 2003)(Douglas, 2003) healthy coralhealthy coral ‘‘old’ dead coralold’ dead coral recently deadrecently dead or diseasedor diseased
  • 11. Symbiont community shift 0 50 100 150 200 250 300 350 400 450 500 C2 D C1 0 5 10 15 20 25 30 35 C2 C1 D -5 5 15 25 35 C2 C1 D 0 10 20 30 C2 C1 D none D C2 C1 D* 2+
  • 12. Type C2 Type D Type C2/D Type C1
  • 14. Chloroplast cell membrane Thylakoid membrane Thylakoid lumen 2H2O O2 + 4H+ CYT B6f complexPSII H+ H+ PSI Fd FNR ATP synthase H+ ATP ADP +ADP + PP22NADP + 2H+ CO2 Calvin Cycle of carbon fixation Starch synthesis e- LHC
  • 16. Acknowledgements This project made possible by support from the Australian Institute of Marine Science, Central Queensland University and University of Groningen
  • 17. Climate change IPCC multi-model ensemble (Meehl, 2007) ↑ 2.0 – 4.5 °C
  • 18. ReferencesBerkelmans, R. and M. J. H. van Oppen (2006). "The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change." Proceedings of the Royal Society of London. Series B, Biological Sciences (1934-1990). Done, T. (1992). "Phase shifts in coral reef communities and their ecological significance." Hydrobiologia 247: 121-132. Done, T., P. Whetton, et al. (2003). Chapter 11: Global climate and coral bleaching on the Great Barrier Reef. Final report to the State of Queensland Greenhouse Task Force, Department of Natural Resources and Mining, www.nrm.qld.gov.au/science/climate.html: 33. Hoegh-Guldberg, O., P. J. Mumby, et al. (2007). "Coral reefs under rapid climate change and ocean acidification." Science 318(5857): 1737-1742. IPCC, Ed. (2001). Climate change 2001: The scientific basis: Contribution of Working Group I to the third assessment report of the Intergovernmental Panel on climate change, New York : Cambridge University Press, 2001. Meehl, G. A., T. F. Stocker, et al. (2007). Chapter 10: Global climate projections. Climate change 2007: The Physical Science Basis, Contribution of: Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press. Mieog, J. C., M. J. H. Van Oppen, et al. (in press). "Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR." Mieog, J. C., M. J. H. Van Oppen, et al. (2007). "Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling." Coral Reefs 26(3): 449-457. Mieog, J. C., M. J. H. van Oppen, et al. (in press). "Enormous potential for shuffling of algal symbionts in reef corals." Muscatine, L. (1990). The role of symbiotic algae in carbon and energy flux in reef corals. Ecosystems of the world 25: Coral reefs. Dubinsky. New York, Elsiever. 25: 75-87. Ostrander, G. K., K. M. Armstrong, et al. (2000). "Rapid transition in the structure of a coral reef community: The effects of coral bleaching and physical disturbance." Proceedings of the National Academy of Sciences of the United States of America 97(10): 5297-5302. Pittock, B., Ed. (2003). Climate Change: An Australian Guide to the Science and Potential Impacts, Australian Greenhouse Office. Smith, C. (2004). The molecular and genetic basis for variation in thermal tolerance in a common reef-building species on the inshore Great Barrier Reef. Townsville, James Cook University. PhD Thesis. Ulstrup, K. E. and M. J. H. van Oppen (2003). "Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef." Molecular Ecology 12(12): 3477-3484. van Oppen, M. J. H., F. P. Palstra, et al. (2001). "Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity." Proceedings of the Royal Society of London. Series B, Biological Sciences (1934-1990) 268(1478): 1759-1767. Wakeford, M., T. J. Done, et al. (2007). "Decadal trends in a coral community and evidence of changed disturbance regime." Coral Reefs On-line First. Wilkinson, C., Ed. (2004). Status of Coral Reefs of the World 2004. Townsville, Australian Institute of Marine Science.

Editor's Notes

  1. Study took place in the Keppel Islands region of the southern section of the GBR – inshore island surrounded by mostly hard coral fringing reefs – very high coral cover – up to 98% on some reefs – in spite of repeated bleaching and flood disturbance Leeward shores have very high cover of A millepora corymbose colonies at an abunance of 4 colonies per 1m2 Shallow reef flats are susceptible to bleaching but make good study sites for investigating Symbiodinium community change because the colonies are so close together easy to find and similar in size, age and structure. Light environment is uniform as is the depth range. The region suffered moderate to severe mass bleaching (more than 60% corals bleached) in February 2002 (Berkelmans et al. 2004) and severe bleaching in January/ February 2006 (89% corals bleached
  2. A millepora very common in the Keppels and grows very well – still not sure why this is so in the southern reaches of the GBR where accretion rates drop off dramatically south of Gladstone The reef flat at Miall has colonies that are juvenile to massive 2 m in diameter – careful to sample only colonies that were not juvenile 460 colonies in total – investigated symbiont types in them 3 monthly in the year before bleaching to see if there were seasonal changes under stable conditions?
  3. Corals for obligate symbioses with dinoflagellates of the genus Symbiodinium
  4. There were multiple variants of C1 and C2 but only one variant of D (D*) Exhaustive or branch and bound searches were performed with gaps treated as a fifth base Statistical support for the phylogenies was tested using bootstrap analysis of 100 replicates BioEdit and ClustalW – PAUP for phylogenies 253 alignment positions and 13 taxa but only 2/6 variable positions were parsimony informative Also intra-colony study of 9 colonies failed to find any sig pattern in genotypes across colonies
  5. Zooxanthellae are autorophic microalgaes belonging to various taxa in the Phylum Dinoflagellata.  Zooxanthellae live symbiotically within the coral polyp tissues and assist the coral in nutrient production through its photosynthetic activities. These activities provide the coral with fixed carbon compounds for energy, enhance calcification ,and mediate elemental nutrient flux. The host coral polyp in return provides its zooxanthellae with a protected environment to live within, and a steady supply of carbon dioxide for its photosynthetic processes. The symbiotic relationship allows the slow growing corals to compete with the faster growing multicellular algaes because the tight coupling of resources and the fact that the corals can feed by day through photosynthesis and by night through predation.   The tissues of corals themselves are actually not the beautiful colors of the coral reef, but are instead clear. The corals receive their coloration from the zooxanthellae living within their tissues.  Coral reefs have survived for millions of years in relatively nutrient-poor tropical waters and in spite of extreme environmental changes {Wood, 1998 #732;Haq, 1987 #731;Thornhill, 2006 #697;Taylor, 1973 #746}. The reef-building corals that make up the structure of reefs form massive structures like the GBR that play a role in coastal protection, primary production and tourist-driven economies {Hoegh-Guldberg, 2004 #848;Wilkinson, 2004 #359}. The success of reef building corals is largely due to the recycling of nutrients from photosynthetic algae to host by autotrophic fixation of carbon {Muscatine, 1969 #605;Muscatine, 1981 #405;Muscatine, 1984 #582;Falkowski, 1984 #640;Gates, 1995 #425;Davies, 1984 #717;Trench, 1979 #842}. Photosynthetically fixed carbon forms an important energy source for reef-building corals that is used for reproduction {Muscatine, 1985 #844;Edmunds, 1986 #840}, tissue growth {Davies, 1984 #717;Muscatine, 1985 #844}, skeletal growth (calcification) {Pearse, 1971 #627}, cell repair {Fine, 2002 #845} and host respiration {Muscatine, 1990 #843}. In turn, the algae use CO2 from host respiration for photosynthesis, respiration and division {Muscatine, 1990 #843}, and gain nutrients {Trench, 1979 #842} and a habitat in the coral tissue that protects them from excess light and damaging UV and enhances incident light for photosynthesis {Salih, 2000 #686}.
  6. MECHANISM Three hypotheses have been advanced to explain the cellular mechanism of bleaching, and all are based on extreme sea temperatures as one of the causative factors. High temperature and irradiance stressors have been implicated in the disruption of enzyme systems in zooxanthellae that offer protection against oxygen toxicity. Photosynthesis pathways in zooxanthallae are impaired at temperatures above 30 degrees C, this effect could activate the disassociation of coral / algal symbiosis. This involves the detachment of cnidarian endodermal cells with their zooxanthellae and the eventual expulsion of both cell types.  interruption of CO2 fixation via the Calvin cycle (by ROS) inhibits the synthesis of proteins in photosystem II (PSII), in particular, synthesis of the D1 protein, during the repair of PSII after photodamage – resulting in further chronic photodamage {Takahashi, 2005; Takahashi, 2006}
  7. N = 460 C2 93.5% D 3.5% C/D 3% before bleaching 71% change to D and C1 N = 79 six months after bleaching Of 58 C2 colonies, 30 changed to D, 11 gained C1 and only 4 colonies remained C2 Signs of shift back between May and Ausust
  8. Miall Island is an inshore reef in the southern section of the GBR. Acropora millepora are one of the two main reef building corals at Miall Island. C2 is the most predominant zooxanthellae type with clade D found occasionally The abundance of clade D
  9. B1: 1.1 – 2.9 and highest is A1F1: 2.4 - 6.4 deg C Most likely is 2 to 4.5 deg C with most likely to be 3.0 deg C (Meehl, Ch 10, IPCC, 2007) Transient climate response TCR is 1 to 3 deg C SRES special report on emissions scenarios shading represents ± 1 SD from individual model means Figure 10.4. Multi-model means of surface warming (relative to 1980–1999) for the scenarios A2, A1B and B1, shown as continuations of the 20th-century simulation. Lines show the multi-model means, shading denotes the ±1 standard deviation range of individual model annual means. Discontinuities between different periods have no physical meaning and are caused by the fact that the number of models that have run a given scenario is different for each period and scenario, as indicated by the coloured numbers given for each period and scenario at the bottom of the panel. For the same reason, uncertainty across scenarios should not be interpreted from this figure (see Section 10.5.4.6 for uncertainty estimates).