Climate change and disease: Bleaching of a chemically defended seaweed

Global Change Biology

Volumn 17, Issue 9, 2011, Pages 2958-2970

  Campbell, Alexandra H ^a   Harder, Tilmann ^b   Nielsen, Shaun ^b   Kjelleberg, Staffan ^b,c   Steinberg, Peter D ^d,e  

^a Centre for Marine Bio Innovation   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d UNIVERSITY OF SYDNEY   (Australia)

^e AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

Complex interactions; Macroalgae; Surface associated microbial communities; Warming

Indexed keywords

BLEACHING; CHEMICAL DEFENSE; CLIMATE CHANGE; CONSERVATION MANAGEMENT; DISEASE PREVALENCE; ENVIRONMENTAL CHANGE; MACROALGA; MICROBIAL COMMUNITY; PATHOGEN; ROCKY SHORE; SEAWEED; WARMING;

ALGAE; BACTERIA (MICROORGANISMS); DELISEA PULCHRA;

EID: 79960976699     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/j.1365-2486.2011.02456.x     Document Type: Article

References (83)

1. Ainsworth TD, Kvennefors EC, Blackall LL, Fine M, Hoegh-Guldberg O (2007) Disease and cell death in white syndrome of Acroporid corals on the Great Barrier Reef. Marine Biology, V151, 19-29.
2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32-46.
3. Anderson MJ, Ter Braak CJF (2003) Permutational tests for multi-factorial analysis of variance. Journal of Statistical Computation & Simulation, 73, 85.
4. Bally M, Garrabou J (2007) Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change. Global Change Biology, 13, 2078-2088.
5. Bidart-Bouzat MG, Imeh-Nathaniel A (2008) Global change effects on plant chemical defenses against insect herbivores. Journal of Integrative Plant Biology, 50, 1339-1354.
6. Booth DJ, Beretta GA (2002) Changes in a fish assemblage after a coral bleaching event. Marine Ecology Progress Series, 245, 205-212.
7. Bruno JF, Selig ER, Casey KS et al. (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biology, 5, e124.
8. Bryant JP, Chapin FS III, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos, 40, 357-368.
9. Caldwell MM, Bjorn LO, Bornman JF, Flint SD, Kulandaivelu G, Teramura AH (1998) Effects of increased solar ultraviolet radiation on terrestrial ecosystems. Journal of Phytochemistry and Photobiology. B, Biology, 46, 40-52.
10. Case RJ, Longford SR, Campbell AH, Low A, Tujula NA, Steinberg PD, Kjelleberg S (2010) Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga. Environmental Microbiology, 13, 529-537.
11. Chapin FS III, Autumn K, Pugnaire F (1993) Evolution of suites of traits in response to environmental stress. The American Naturalist, 142, S78.
12. Coleman MA, Kelaher BP, Steinberg PD, Millar AJK (2008) Absence of a large brown macroalga on urbanised reefs around Sydney, Australia and evidence for historical decline. Journal of Phycology, 44, 897-901.
13. Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science, 230, 895-899.
14. Connell SD, Russell BD, Turner DJ et al. (2008) Recovering a lost baseline: missing kelp forests from a metropolitan coast. Marine Ecology Progress Series, 360, 63-72.
15. Correa JA, Flores V, Garrido J (1994) Green patch disease in Iridaea laminarioides (Rhodophyta) caused by Endophyton sp. (Chlorophyta). Diseases of Aquatic Organisms, 19, 203-213.
16. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letters, 11, 1304-1315.
17. Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theories. In: Marine Chemical Ecology (eds. Mcclintock JB, Baker BJ), pp. 325-345. CRC Press, Boca Raton.
18. de Nys R, Wright AD, Konig GM, Sticher O (1993) New halogenated furanones from the marine alga Delisea pulchra (cf. fimbriata). Tetrahedron, 49, 11213-11220.
19. Donlan RM (2002) Biofilms: microbial life on surfaces. Emerging Infectious Disease, 8, 881-890.
20. Dworjanyn SA, de Nys R, Steinberg PD (1999) Localisation and surface quantification of secondary metabolites in the red alga Delisea pulchra. Marine Biology, 133, 727-736.
21. Dworjanyn SA, de Nys R, Steinberg PD (2006a) Chemically mediated antifouling in the red alga Delisea pulchra. Marine Ecology Progress Series, 318, 153-163.
22. Dworjanyn SA, Wright JT, Paul NA, de Nys R, Steinberg PD (2006b) Cost of chemical defence in the red alga Delisea pulchra. Oikos, 113, 13-22.
23. Edwards MS, Estes JA (2006) Catastrophe, recovery and range limitation in NE Pacific kelp forests: a large-scale perspective. Marine Ecology Progress Series, 320, 79-87.
24. Engel S, Jensen PR, Fenical W (2002) Chemical ecology of marine microbial defense. Journal of Chemical Ecology, 28, 1971-1985.
25. Eranen JK, Nilsen J, Zverev VE, Kozlov MV (2009) Mountain birch under multiple stressors; heavy metal-resistant populations co-resistant to biotic stress but maladapted to abiotic stress. Journal of Evolutionary Biology, 22, 840-851.
26. Ewald PW (1994) Evolution of Infectious Diseases. Oxford University Press, New York.
27. Figuera WF, Booth DJ (2010) Increasing ocean temperatures allow tropical fishes to survive over winter in temperate waters. Global Change Biology, 16, 506-516.
28. Frias-Lopez J, Zerkle AL, Bonheyo GT, Fouke BW (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Applied and Environmental Microbiology, 68, 2214-2228.
29. Garcia-Vallve S, Romeu A, Palau J (2000) Horizontal gene transfer in bacteria and archeal complete genomes. Genome Research, 10, 1719-1725.
30. Garrett KA, Dendy SP, Frank EE, Rouse MN, Travers SE (2006) Climate change effects on plant disease: genomes to ecosystems. Annual Review of Phytopathology, 44, 489-509.
31. Halpern BS, Walbridge S, Selkoe KA et al. (2008) A global map of human impact on marine ecosystems. Science, 319, 948-952.
32. Harvell CD, Kim K, Burkholder JM et al. (1999) Emerging marine diseases - climate links and anthropogenic factors. Science, 285, 1505-1510.
33. Harvell CD, Kim K, Quirolo C, Weir J, Smith G (2001) Coral bleaching and disease: contributors to 1998 mass mortality in Briareum asbestinum (Octocorallia, Gorgonacea). Hydrobiologia, 460, 97-104.
34. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science, 296, 2158-2162.
35. Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annual Review of Ecology and Systematics, 19, 111-145.
36. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research, 50, 839-866.
37. Huggett M, Williamson J, de Nys R, Kjelleberg S, Steinberg P (2006) Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia, 149, 604-619.
38. IPCC (2007) Climate change 2007: the physical science basis. In: Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Miller HL), Cambridge, Cambridge, UK, New York, NY, USA.
39. Jackson JBC (2001) What was natural in the coastal oceans? Proceedings of the National Academy of Sciences of the United States of America, 98, 5411-5418.
40. Karsten U, Bischof K, Wiencke C (2001) Photosynthetic performance of Arctic macroalgae after transplantation from deep to shallow waters. Oecologia, 127, 11-20.
41. Klinkert B, Narberhaus F (2009) Microbial thermosensors. Cellular and Molecular Life Sciences, 66, 2661-2676.
42. Konkel ME, Tilly K (2000) Temperature-regulated expression of bacterial virulence genes. Microbes and Infection, 2, 157-166.
43. Kumar N (2005) Furanone derivatives and methods for making same. Patent WO/2004/016588.
44. Lafferty KD, Holt RD (2003) How should environmental stress affect the population dynamics of disease? Ecology Letters, 6, 654-664.
45. Lafferty KD, Porter JW, Ford SE (2004) Are diseases increasing in the ocean? Annual Review of Ecology, Evolution and Systematics, 35, 31-54.
46. Ling S (2008) Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia, 156, 883-894.
47. Ling SD, Johnson CR, Ridgway K, Hobday AJ, Haddon M (2009) Climate-driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics. Global Change Biology, 15, 719-731.
48. Littler MM, Littler DS (1995) Impact of CLOD pathogen on Pacific coral reefs. Science, 267, 1356-1360.
49. Liu W, Marsh TL, Cheng H, Forney LJ (1997) Characterisation of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S RNA. Applied and Environmental Microbiology, 63, 4516-4522.
50. Longford SJ (2008) Ecology of epiphytic bacteria on Delisea pulchra. Unpublished PhD, University of New South Wales, Sydney
51. Longford SR, Tujula NA, Crocetti GR et al. (2007) Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquatic Microbial Ecology, 48, 217-229.
52. Manefield M, de Nys R, Kumar N (1999) Evidence that the halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology, 45, 283-291.
53. Manefield M, Rasmussen TB, Henzter M, Andersen JB, Steinberg PD, Kjelleberg S, Givskov M (2002) Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology, 148, 1119-1127.
54. Manefield M, Welch M, Givskov M, Salmond GPC, Kjelleberg S (2001) Halogenated furanones from the red alga, Delisea pulchra, inhibit carbapenem antibiotic synthesis and exoenzyme virulence factor production in the phytopathogen Erwinia carotovora. FEMS Microbiology Letters, 205, 131-138.
55. Marcais B, Breda N (2006) Role of an opportunistic pathogen in the decline of stressed oak trees. Journal of Ecology, 94, 1214-1223.
56. Maximilien R, de Nys R, Holmstrom C et al. (1998) Chemical mediation of bacterial surface colonisation by secondary metabolites from the red alga Delisea pulchra. Aquatic Microbial Ecology, 15, 233-246.
57. Moxon ER, Rainey PB, Nowak MA, Lenski RE (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Current Biology, 4, 24-33.
58. 2 alters response to thermal stress in sea urchin larvae. Marine Biology, 156, 439-446.
59. Pantos O, Cooney RP, Le Tissier MDA, Barer MR, O'Donnell AG, Bythell JC (2003) The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis. Environmental Microbiology, 5, 370-382.
60. Paul NA, de Nys R, Steinberg PD (2006) Chemical defense against bacteria in the red alga Asparagopsis armata: linking structure with function. Marine Ecology Progress Series, 306, 87-101.
61. Poloczanska ES, Babcock RC, Butler A et al. (2007) Climate change and Australian marine life. In: Oceanography and Marine Biology: An Annual Review (eds. Gibson RN, Atkinson RJA, Gordon JDM), CRC Press, Taylor & Francis.
62. Reinheimer G (1992) Aquatic Microbiology. Wiley, New York.
63. Ridgeway KR (2007) Long-term trend and decadal variability of the southward penetration of the East Australian Current. Geophysical Research Letters, 34, L13613.
64. Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annual Review of Microbiology, 31, 107-133.
65. Schoeneweiss DF (1975) Predisposition, stress and plant disease. Annual Review of Phytopathology, 13, 193-211.
66. Scrosati R, de Wreede RE (1998) The impact of frond crowding on frond bleaching in the clonal intertidal alga Mazella cornucopiae (Rhodophyta, Gigartinaceae) from British Columbia, Canada. Journal of Phycology, 34, 228-232.
67. Selifonova O, Valle F, Schellenberger V (2001) Rapid evolution of novel traits in microorganisms. Applied and Environmental Microbiology, 67, 3654-3649.
68. Short FT, Neckles HA (1999) The effects of global climate change on seagrasses. Aquatic Botany, 63, 169-196.
69. Staehr PA, Wernberg T (2009) Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. Journal of Phycology, 45, 91-99.
70. Steenwerth KL, Jackson LE, Calderón FJ, Stromberg MR, Scow KM (2002) Soil microbial community composition and land use history in cultivated and grassland ecosystems of coastal California. Soil Biology and Biochemistry, 34, 1599-1611.
71. Steinberg PD, de Nys R, Kjelleberg S (2001) Chemical mediation of surface colonisation. In: Marine Chemical Ecology (eds. McClintock JB, Baker BJ), pp. 355-378. CRC Press, Boca Raton.
72. Steinberg PD, de Nys R, Kjelleberg S (2002) Chemical cues for surface colonization. Journal of Chemical Ecology, 28, 1935-1951.
73. Thompson IP, Bailey MJ, Fenlon JS et al. (1993) Quantitative and qualitative seasonal changes in the microbial community from the phyllosphere of sugar beet (Beta vulgaris). Plant and Soil, 150, 177-191.
74. Toohey BD, Kendrick GA (2007) Survival of juvenile Ecklonia radiata sporophytes after canopy loss. Journal of Experimental Marine Biology and Ecology, 349, 170-182.
75. Underwood AJ (1997) Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance. Cambridge University Press, Cambridge.
76. Valentine JP, Johnson CR (2004) Establishment of the introduced kelp Unidaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania, Australia. Marine and Freshwater Research, 55, 223-230.
77. Vergeer LHT, Den Hartog C (1994) Omnipresence of Labyrinthulaceae in seagrasses. Aquatic Botany, 48, 1-20.
78. Walker JM, Spencer JF, Ragout De Spencer AL (2004) Environmental Microbiology: Methods and Protocols. Humana Press, Totowa, NJ.
79. Williamson JE, Carson DG, de Nys R, Steinberg PD (2004) Demographic consequences of an ontogenetic shift by a sea urchin in response to host plant chemistry. Ecology, 85, 1355-1371.
80. Womersley HBS (1996) The Marine Benthic Flora of Southern Australia. Australian Biological Resources Study, Adelaide.
81. Wright JT, de Nys R, Steinberg PD (2000) Geographic variation in halogenated furanones from the red alga Delisea pulchra and associated herbivores and epiphytes. Marine Ecology Progress Series, 207, 227-241.
82. Zangerl AR, Bazzaz FA (1992) Theory and pattern in plant defense allocation. In: Plant Resistance to Herbivores and Pathogens: Ecology, Evolution and Genetics (eds. Fritz RS, Simms EL), pp. 363-391. University of Chicago Press, Chicago and London.
83. Zangerl AR, Berenbaum MR (1997) Cost of chemically defending seeds: Furanocoumarins and Pastinaca sativa. American Naturalist, 150, 491-504.