Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data

Lesser, Michael P.; Bythell, John C.; Gates, Ruth D.; Johnstone, Ron; Høegh-Guldberg, Ove

doi:10.1016/j.jembe.2007.02.015

Cited by 261 publications

(224 citation statements)

References 57 publications

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“…Such mortality events were not reported previously. Our results also are in accordance with the findings of studies on microorganisms as a factor related to these events, because biomass loss is a sign of physiological stress that makes colonies more susceptible to opportunistic, residential, and/or pathogenic microorganisms (11,19,21), which has been observed in corals (43). But under the observed trend of increasing extreme temperature events, increased contributions of lethal temperature and increased virulence of microorganisms to the events should be expected in the near future.…”

Section: Resultssupporting

confidence: 91%

Global warming-enhanced stratification and mass mortality events in the Mediterranean

Coma

Ribes²,

Serrano³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

346

272

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Summer conditions in the Mediterranean Sea are characterized by high temperatures and low food availability. This leads to ''summer dormancy'' in many benthic suspension feeders due to energetic constraints. Analysis of the most recent 33-year temperature time series demonstrated enhanced stratification due to global warming, which produced a Ϸ40% lengthening of summer conditions. Many biological processes are expected to be affected by this trend, culminating in such events as mass mortality of invertebrates. Climatic anomalies concomitant with the occurrence of these events represent prolonged exposure to warmer summer conditions coupled with reduced food resources. Simulation of the effects of these conditions on a model organism demonstrated a biomass loss of >35%. Losses of this magnitude result in mortality similar to that noted in field observations during mass mortality events. These results indicate that temperature anomalies are the underlying cause of the events, with energetic constraints serving as the main triggering mechanism.climatic anomalies ͉ summer lengthening ͉ energetic constraints ͉ benthic suspension feeders ͉ extreme events I n a rapidly warming world, marine and terrestrial biodiversity and ecosystems are responding through shifts in distribution and changes in abundance, phenology, structure, and functioning (1-3). Furthermore, global environmental change is expected to lead to a higher frequency and shorter return time of extreme events (4). An example of this is the occurrence of mass mortality events, which are affecting an increasing number of marine species and ecosystems worldwide (5, 6). These events have been well documented in coral reef ecosystems, where they have produced dramatic phase shifts in community structure (7-9). In recent years, the coralligenous community, one of the most diverse in the Mediterranean Sea (Ϸ1,666 species; ref. 10), where suspension feeders are dominant, has been strongly affected by several mass mortality events [supporting information (SI) Table S1]. Engineer species, including gorgonians and sponges, have been the most affected taxa down to depths of 45 m (11-13). The impact of these events on populations is similar to that observed in the 1980s and 1990s in the Caribbean Sea (14, 15). But despite the wide extent of these effects on Caribbean populations, identification of the causes has not always been possible; however, some were associated with temperature increases (15), and others were associated with diseases (14). Understanding mass mortality events is becoming increasingly important, given the escalating presence of anthropogenic stressors that affect marine ecosystems (5, 6, 16).The causes of mass mortality events in the Mediterranean remain unknown, and our ability to predict the effects of these events depends on characterizing them and elucidating trends exhibited by potentially causative factors. Current hypotheses about the causes of these events in the Mediterranean focus on their relationship with the occurrence of distinctive cl...

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Section: Resultssupporting

confidence: 91%

Global warming-enhanced stratification and mass mortality events in the Mediterranean

Coma

Ribes²,

Serrano³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

346

272

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“…These and other studies have suggested that WPD represents a group of different diseases with similar signs in different species (Dustan, 1977;Rosenberg et al, 2007;Sunagawa et al, 2009). Furthermore, it has been suggested that some coral diseases have a polymicrobial origin involving an imbalance in the structure and diversity of microorganism communities symbiotically associated with their host (Harvell et al, 2007;Lesser et al, 2007). An example is the black band disease, which is associated to a bacterial consortium of cyanobacteria and other less abundant groups of sulfur-oxidizing and sulfur-reducing bacteria (Sekar et al, 2006;Barneah et al, 2007;Sato et al, 2010).…”

mentioning

confidence: 83%

“…In the last three decades, local and global deterioration of environmental conditions have dramatically compromised the health of corals, which consequently affected the entire coral reef ecosystem. (Harvell et al, 1999(Harvell et al, , 2007Wilkinson, 1999;Green and Bruckner, 2000;Gardner et al, 2003;Pandolfi et al, 2003;Lesser et al, 2007). Recent reports indicate that 58-70% of coral reefs worldwide are threatened by human activities, while more than 30% of the biota associated with Caribbean coral reefs have disappeared within the last 30 years Weil et al, 2006;Jackson, 2008).…”

Section: Introductionmentioning

confidence: 99%

Shifts in bacterial communities of two caribbean reef-building coral species affected by white plague disease

et al. 2011

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Coral reefs are deteriorating at an alarming rate mainly as a consequence of the emergence of coral diseases. The white plague disease (WPD) is the most prevalent coral disease in the southwestern Caribbean, affecting dozens of coral species. However, the identification of a single causal agent has proved problematic. This suggests more complex etiological scenarios involving alterations in the dynamic interaction between environmental factors, the coral immune system and the symbiotic microbial communities. Here we compare the microbiome of healthy and WPD-affected corals from the two reef-building species Diploria strigosa and Siderastrea siderea collected at the Tayrona National Park in the Caribbean of Colombia. Microbiomes were analyzed by combining culture-dependent methods and pyrosequencing of 16S ribosomal DNA (rDNA) V5-V6 hypervariable regions. A total of 20 410 classifiable 16S rDNA sequences reads were obtained including all samples. No significant differences in operational taxonomic unit diversity were found between healthy and affected tissues; however, a significant increase of Alphaproteobacteria and a concomitant decrease in the Beta-and Gammaproteobacteria was observed in WPD-affected corals of both species. Significant shifts were also observed in the orders Rhizobiales, Caulobacteriales, Burkholderiales, Rhodobacterales, Aleteromonadales and Xanthomonadales, although they were not consistent between the two coral species. These shifts in the microbiome structure of WPD-affected corals suggest a loss of community-mediated growth control mechanisms on bacterial populations specific for each holobiont system. The ISME Journal (2012) 6, 502-512; doi:10.1038/ismej.2011.123; published online 29 September 2011Subject Category: microbial population and community ecology Keywords: bacterial community; white plague disease; coral diseases; pyrosequencing; Diploria strigosa; Siderastrea siderea IntroductionCoral reefs posses an immense biodiversity comparable only to that of the tropical rain forest (Mulhall, 2009). The structural, physiological and ecological bases of reefs are the scleractinian corals. They are in symbiotic relationship with a variety of bacteria and archaea as well as with microalgae (zooxanthellae), which are mainly responsible for the corals' high contribution to primary productivity of coral reefs . Modifications in the structure and relative density of symbiotic microbial communities might have a critical role in the coral adaptation to rapid environmental changes (Reshef et al., 2006). In the last three decades, local and global deterioration of environmental conditions have dramatically compromised the health of corals, which consequently affected the entire coral reef ecosystem. (Harvell et al., 1999(Harvell et al., , 2007Wilkinson, 1999;Green and Bruckner, 2000;Gardner et al., 2003;Pandolfi et al., 2003;Lesser et al., 2007). Recent reports indicate that 58-70% of coral reefs worldwide are threatened by human activities, while more than 30% of the biota associated with Caribb...

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“…Instead, we observed an increase in diversity in samples from diseased tissues (Table 2), whereas there was no overwhelming dominance by a single bacterial species, which appears to be an unexpected result for a primary infection. It has been argued that opposed to the idea of a primary infection, coral diseases may also result from unchecked growth of otherwise harmless bacteria in compromised hosts and/or due to changes in the environment, for example, increased temperatures (Harvell et al, 1999(Harvell et al, , 2007Lesser et al, 2007). The identification of bacteria in healthy corals that were similar to known pathogens or bacteria that were previously isolated from diseased, stressed or injured marine invertebrates may point toward a role of latent, usually non-pathogenic commensals.…”

Section: Comparison Of Healthy and Diseased Coral Tissue Samplesmentioning

confidence: 99%

Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata

et al. 2009

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Increasing evidence confirms the crucial role bacteria and archaea play within the coral holobiont, that is, the coral host and its associated microbial community. The bacterial component constitutes a community of high diversity, which appears to change in structure in response to disease events. In this study, we highlight the limitation of 16S rRNA gene (16S rDNA) clone library sequencing as the sole method to comprehensively describe coral-associated communities. This limitation was addressed by combining a high-density 16S rRNA gene microarray with, clone library sequencing as a novel approach to study bacterial communities in healthy versus diseased corals. We determined an increase in diversity as well as a significant shift in community structure in Montastraea faveolata colonies displaying phenotypic signs of White Plague Disease type II (WPD-II). An accumulation of species that belong to families that include known coral pathogens (Alteromonadaceae, Vibrionaceae), bacteria previously isolated from diseased, stressed or injured marine invertebrates (for example, Rhodobacteraceae), and other species (for example, Campylobacteraceae) was observed. Some of these species were also present in healthy tissue samples, but the putative primary pathogen, Aurantimonas corallicida, was not detected in any sample by either method. Although an ecological succession of bacteria during disease progression after causation by a primary agent represents a possible explanation for our observations, we also discuss the possibility that a disease of yet to be determined etiology may have affected M. faveolata colonies and resulted in (or be a result of) an increase in opportunistic pathogens.

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Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data

Cited by 261 publications

References 57 publications

Global warming-enhanced stratification and mass mortality events in the Mediterranean

Global warming-enhanced stratification and mass mortality events in the Mediterranean

Shifts in bacterial communities of two caribbean reef-building coral species affected by white plague disease

Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata

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