**6. Conclusion: Towards an integrative approach**

Since mild episodes of adverse climatic and biotic conditions regularly occur, it can be assumed that coral reefs are quite resilient with respect to biodiversity losses. Today, human activities are having a steadily increasing impact on climate (global warming) and on biodiversity (overexploitation and toxic waste) and although accurate predictions cannot be made, it is assumed that massive losses of marine biodiversity associated with coral reefs will occur within the next decades. The capacity of organisms to acclimatize and that of communities to maintain their biodiversities is largely unknown, and estimates are based on isolated laboratory experiments in which tolerance limits to individual stressors are measured. The spread of microbial diseases from the shallow (0-30 m) to the mesophotic (30 – 200 m) zones has been discussed by Olson & Kellogg (2010) who prompt investigations on the algal, sponge and coral holobionts from the hitherto neglected deeper reef communities. At the holobiont level, it is important to detect early signs of stress (e.g. coral bleaching due to loss of zooxanthellae) and to identify the critical stages beyond which permanent damage results (e.g. tissue necrosis, various *band diseases* due to microbial pathogens). Intraspecific variations in the profiles of bacterial communities associated with corals may show up between distant localities (Littman et al., 2009), suggesting that environmental conditions may significantly influence the dominance profiles of a few strains, possibly reflecting on the health status of the host species. At the community and ecosystem levels, it is important to evaluate the extent of damage and whether recolonization is possible if the primary cause can be removed (e.g. by classifying an impacted area as a protected zone). Along the same lines, it should now be possible to devise molecular-based methods that can accurately estimate a shift in bacterial biodiversity from standard to pathogenic in a given sample, to estimate stress levels, or to compare metabolomic signatures between unaffected and impacted specimens. Comparable methods already exist in medical microbiology, and in cancerology in which specific markers are sought in addition to metabolomic profiling of biological fluids.

#### **6.1 The common fate of biodiversity and chemodiversity**

Biodiversity emerged as the first unicellular forms of life appeared, presumably as chemoautotrophs in hydrogeothermal environments. The original biogeochemistry was quite different to what it is today, and different mineral-water-air equilibria must have been attained several times since the emergence of life, e.g. basic Precambrian vs. acidic modern ocean (David & Alm, 2011). As biodiversity and chemodiversity increased, their influence on global biogeochemistry gradually increased (Falkowski et al., 2008). Cyanobacteria are thought to have enriched the atmosphere in oxygen to the point that through various endosymbiosis scenarios a "compromise" was reached that allowed living entities to use oxygen generated by photosynthesis for respiration while controlling its toxicity. Taming the generation of highly reactive radical oxygen species by using oxidative stresses as useful

Coral Reef Biodiversity in the Face of Climatic Changes 99

environmental disturbance. The more specific its reactivity to a specific stress, the better. The logic behind this approach is similar to extracting the chemical profile of a marine invertebrate from an impacted environment and comparing it with the profile database of a conspecific from a pristine environment, and hopefully identifying a chemical marker that would act as a signature (as in clinical analyses of body fluids and the search of specific markers of cancer). The association of biological and chemical profiling and signature marking into a standardized procedure would undoubtedly help industry deciders to evaluate the importance of environmental impacts and to take appropriate action. At an intermediate scale, in-situ monitoring of key environmental parameters in mesocosms allows modeling that is useful for decision-making in creating natural reserves. Respecting protected reef areas should be a mature political decision based on sound scientific investigations. For example, active nickel mining and ore processing in the immediate vicinity of coral reefs protected under the UNESCO's World Heritage list in New Caledonia generates difficult choices between short-term economic profit and long-term and durable

Finally, accessible information through the media and adapted and participative school programs should be encouraged in order to modify the management of reef resources to

Joseph Connell's summary of his landmark Science paper of 1978 emphasizes the necessity to maintain some kind of equilibrium between human activities and natural environments, a

"*The commonly observed high diversity of trees in tropical rain forests and corals on tropical reefs is a nonequilibrium state which, if not disturbed further, will progress toward a low-diversity equilibrium community. This may not happen if gradual changes in climate favor different species. If equilibrium is reached, a lesser degree of diversity may be sustained by niche diversification or by a compensatory mortality that favors inferior competitors. However, tropical forests and reefs are subject to severe* 

Life would then have to re-create itself in unforeseeable evolutionary scenarios, counting on the inventiveness and adaptability of the microbial world where man's inventiveness will

I am very grateful to Dr. Ian Probert for his critical reading of the manuscript and for

Ainsworth, T.D.; Vega Thurber, R. & Gates, R.D. (2009). The future of coral reefs: a microbial

Agostini, S.; Suzuki, Y.; Casareto, B.E.; Nakano, Y.; Hidaka, M. & Badrun, N. (2009). Coral

perspective. *Trends in Ecology and Evolution* Vol.25 No.4, pp. 233-240, ISSN: 0169-

symbiotic complex: Hypothesis through vitamin B12 for a new evaluation. *Galaxea,* 

condition without which very large clusters of biodiversity may be irremediably lost:

*disturbances often enough that equilibrium may never be attained.*" Joseph Connell (1978)

checking the English, and to Prof. Jean-Michel Kornprobst for useful suggestions.

*Journal of Coral Reef Studies* Vol. 11, pp. 1-11, ISSN: 1883-0838

exploitation of reef resources.

have failed.

**7. Acknowledgment** 

**8. References** 

5347

take into account sustainable and durable applications.

**6.4 Biodiversity beyond ecosystem resilience – What's next?** 

warning signals of an environmental aggression is an example of this adaptation to aerobic life. Competition between an ever-increasing number of species and ever reducing availability of resources fueled a new form of chemodiversity, that of secondary or communication metabolites. Thus, the biochemistry involved in physiological adaptation and inter-organism communication links biodiversity and chemodiversity. This simplified picture does not account for the contribution of microorganisms to both primary and secondary metabolisms of the host they live with. In aquatic environments, attempts to integrate all biotic communities participating in the same functional dynamics gave rise to the hologenome theory and to the holobiont concept. When addressing environmental issues, and especially stress responses, this new biome approach can benefit from the fast evolving molecular and genomic fields of metabolic fingerprinting and microbial metagenomics, in the quest for suitable analytical tools. Recent culture-independent approaches have revealed an unsuspected quantity of microbial diversity, not only bacterial (Sogin et al., 2006), but also eukaryotic (Dawson & Hagen 2009), the "rare biosphere", representing a potential reservoir of genes and genomes that marine life may rely on to adapt to new environmental conditions.

#### **6.2 Intellectual diversity should work for, not against natural diversity**

Man has been impacting his environment with extensive use of metals since the onset of the 19th century industrial era. Artificial chemodiversity followed, due to the development of the petroleum chemistry, synthetic polymers and new pharmaceuticals. Unfortunately, the industry has shortsightedly released into the environment thousands of novel organic molecules without proper evaluation of allergenic and carcinogenic effects on human health, both by direct exposure or through accumulation in terrestrial and aquatic food chains. Degradability and speciation of industrial and household waste have been neglected, with destruction of entire fragile ecosystems e.g. rivers and ponds. Biodiversity has also been "directed" with an increasing number of selected crop plants and farm animals and now with genetically modified versions which can arguably hybridize and displace natural conspecifics. The coming of age of bioresponsibility vs. exploration may soon become a necessity, i.e. what can be collectively termed as *intello-diversity* must be applied to the uptake of acceptable practices for the maintenance of a balanced natural equilibrium while making resources lasting and renewable.

#### **6.3 How can scientists mediate environmental conflicts and help political action**

At present, research concentrates on a handful of "convenient" model reef species and on how their metabolism reacts to experimental disturbances. This approach is of limited use outside the confines of the laboratory. To be applicable to real-life situations, i.e. mining pollution in an otherwise undisturbed environment, multi-scale studies must be undertaken. In the laboratory, stress studies must not only concentrate on the transcriptomics of stress-associated genes of the host organism, but should also include assessment of accompanying changes of the microbiodiversity which is likely to reveal a profile change from functional to pathogenic, and from autotrophic to heterotrophic (Littman et al., 2011). New molecular tools could be developed to address all types of environmental issues, ranging from specific toxicity to geoclimatic changes, including urban or industrial pollution. For example, spotting out the "sentinel" bacteria strain in an ecologically sensitive holobiont would provide a quantifiable biomarker of an

warning signals of an environmental aggression is an example of this adaptation to aerobic life. Competition between an ever-increasing number of species and ever reducing availability of resources fueled a new form of chemodiversity, that of secondary or communication metabolites. Thus, the biochemistry involved in physiological adaptation and inter-organism communication links biodiversity and chemodiversity. This simplified picture does not account for the contribution of microorganisms to both primary and secondary metabolisms of the host they live with. In aquatic environments, attempts to integrate all biotic communities participating in the same functional dynamics gave rise to the hologenome theory and to the holobiont concept. When addressing environmental issues, and especially stress responses, this new biome approach can benefit from the fast evolving molecular and genomic fields of metabolic fingerprinting and microbial metagenomics, in the quest for suitable analytical tools. Recent culture-independent approaches have revealed an unsuspected quantity of microbial diversity, not only bacterial (Sogin et al., 2006), but also eukaryotic (Dawson & Hagen 2009), the "rare biosphere", representing a potential reservoir of genes and genomes that marine life may rely on to

adapt to new environmental conditions.

making resources lasting and renewable.

**6.2 Intellectual diversity should work for, not against natural diversity** 

Man has been impacting his environment with extensive use of metals since the onset of the 19th century industrial era. Artificial chemodiversity followed, due to the development of the petroleum chemistry, synthetic polymers and new pharmaceuticals. Unfortunately, the industry has shortsightedly released into the environment thousands of novel organic molecules without proper evaluation of allergenic and carcinogenic effects on human health, both by direct exposure or through accumulation in terrestrial and aquatic food chains. Degradability and speciation of industrial and household waste have been neglected, with destruction of entire fragile ecosystems e.g. rivers and ponds. Biodiversity has also been "directed" with an increasing number of selected crop plants and farm animals and now with genetically modified versions which can arguably hybridize and displace natural conspecifics. The coming of age of bioresponsibility vs. exploration may soon become a necessity, i.e. what can be collectively termed as *intello-diversity* must be applied to the uptake of acceptable practices for the maintenance of a balanced natural equilibrium while

**6.3 How can scientists mediate environmental conflicts and help political action**  At present, research concentrates on a handful of "convenient" model reef species and on how their metabolism reacts to experimental disturbances. This approach is of limited use outside the confines of the laboratory. To be applicable to real-life situations, i.e. mining pollution in an otherwise undisturbed environment, multi-scale studies must be undertaken. In the laboratory, stress studies must not only concentrate on the transcriptomics of stress-associated genes of the host organism, but should also include assessment of accompanying changes of the microbiodiversity which is likely to reveal a profile change from functional to pathogenic, and from autotrophic to heterotrophic (Littman et al., 2011). New molecular tools could be developed to address all types of environmental issues, ranging from specific toxicity to geoclimatic changes, including urban or industrial pollution. For example, spotting out the "sentinel" bacteria strain in an ecologically sensitive holobiont would provide a quantifiable biomarker of an environmental disturbance. The more specific its reactivity to a specific stress, the better. The logic behind this approach is similar to extracting the chemical profile of a marine invertebrate from an impacted environment and comparing it with the profile database of a conspecific from a pristine environment, and hopefully identifying a chemical marker that would act as a signature (as in clinical analyses of body fluids and the search of specific markers of cancer). The association of biological and chemical profiling and signature marking into a standardized procedure would undoubtedly help industry deciders to evaluate the importance of environmental impacts and to take appropriate action. At an intermediate scale, in-situ monitoring of key environmental parameters in mesocosms allows modeling that is useful for decision-making in creating natural reserves. Respecting protected reef areas should be a mature political decision based on sound scientific investigations. For example, active nickel mining and ore processing in the immediate vicinity of coral reefs protected under the UNESCO's World Heritage list in New Caledonia generates difficult choices between short-term economic profit and long-term and durable exploitation of reef resources.

Finally, accessible information through the media and adapted and participative school programs should be encouraged in order to modify the management of reef resources to take into account sustainable and durable applications.

### **6.4 Biodiversity beyond ecosystem resilience – What's next?**

Joseph Connell's summary of his landmark Science paper of 1978 emphasizes the necessity to maintain some kind of equilibrium between human activities and natural environments, a condition without which very large clusters of biodiversity may be irremediably lost:

"*The commonly observed high diversity of trees in tropical rain forests and corals on tropical reefs is a nonequilibrium state which, if not disturbed further, will progress toward a low-diversity equilibrium community. This may not happen if gradual changes in climate favor different species. If equilibrium is reached, a lesser degree of diversity may be sustained by niche diversification or by a compensatory mortality that favors inferior competitors. However, tropical forests and reefs are subject to severe disturbances often enough that equilibrium may never be attained.*" Joseph Connell (1978)

Life would then have to re-create itself in unforeseeable evolutionary scenarios, counting on the inventiveness and adaptability of the microbial world where man's inventiveness will have failed.
