The goal of the COREAM project was to monitor changes induced by Ocean Acidification (OA) in coral reef ecosystems established in artificial mesocosms, focusing on long term effects in order to take acclimation into account.
We have set up two identical artificial mesocosms that mimic environmental conditions found in a natural site: the lagoon at "La Saline" in Reunion Island, Indian Ocean. Starting with field physico- chemical records at the selected site, we have reproduced these values, including daily fluctuations in these mesocosms (Leblud et al 2014). A particularity of our mesocosms is that they match a paired design, with both the actual (pHtot around 8.05) and acidified (pHtot around 7.7) conditions obtained in two separate experimental aquaria both connected to the same mesocosm. That way, the mesocosm effect can be eliminated from the model, and only the pH (and aquarium) effects can be studied. With two identical mesocosms, we end up, thus with four experimental aquaria, two controls and two acidified ones, with a duplicate design.
We started with a short-term OA experiment (Moulin 2014). This experiment was mainly set up to test the new mesocosms, but led finally to interesting preliminary results that were published (Moulin et al 2014a). An artificial community of various corals, as calcifiers, and the sea urchin Echinometra mathaei as bioeroder and grazer and reef substrate with its cohort of micro-organisms, algae and meiofauna were studied over seven weeks at pHtot 8.1 (control) versus 7.6 (acidified). Sea urchins fed principally on algae that grow on the reef substrate. This study demonstrated that E. mathaei resists to moderate OA at short term, since neither their growth, nor their metabolism were significantly affected. It was also demonstrated that the sea urchins were able to regulate the acid- base balance of their extracellular fluid through bicarbonate compensation (Collard et al, 2013 & 2014). Experiments in parallel on a coral, Seriatopora hystrix, also indicated that this species resists to moderate acidification in term of calcification, photosynthesis of its symbiotic algae, as well as respiration, but that drastic ecophysiological changes occur with a pH lower than 7.3 (Leblud et al, in prep. A, Leblud 2015).
The mesocosms worked perfectly well during this preliminary experiment (Leblud et al 2014). So, we were ready to start a longer term experiment to investigate how a simplified reef community with calcifiers and bioeroders behaves under moderate acidfication (pHtot = 7.7, as expected around 2100.) After obtaining the required authorizations at the Reunion Island, we have collected reef substrate and its cohort of bacteria, endofauna and algae, three species of hermatypic corals representative of the coral community in the lagoon at "La Saline" (Acropora muricata, A. digitata & Pocillopora damicornis), and the most abundant species of sea urchin (Echinometra mathaei), either on site in the Marine Reserve, or in a site outside of the reserve (Saint Pierre) but on the same reef. This community was completed with a few coral colonies from the aquarium market (A. tenuis, P. damicornis and S. hystrix) because we were limited in the amount of corals we could collect in the Marine Reserve.
The long term experiment consisted in a gradual acidification of the seawater in the treatment aquaria from pHtot 8.05 down to 7.7 in six months, while the control aquaria remained at pHtot 8.05. These conditions were maintained during further 6 months. The physiology of the sea urchins and four coral species were studied all along the experiment. Microorganisms on the coral as well as in the substrate were investigated too.
Regarding the corals, acclimation of Pocilloporidae on longer term led to similar, or even higher (for Pocillopora damicornis) calcification of pHtot = 7.7. Acroporidae resisted also but a slight decrease in calcification was noted, although not significant (Leblud et al, in prep. b). Neither photosynthesis, nor respiration were affected by ocean acidification, but N and P assimilation changed at long term (between 6 months and 12 months) for two coral species: A. digitifera and S. hystrix (Leblud et al, in prep. c).
For the sea urchins, their ability to regulate the acid-base balance of their coelomic fluid and their resistance were confirmed at long term (Moulin et al 2014b). Biomechanic properties of their skeleton (Dubois 2014) were investigated too, with no significant differences between control and treatment (Moulin et al 2014b). A balance between bioaccretion and bioerosion in the simplified ecosystem was also studied (Moulin et al, submitted) and it revealed that grazing and bioerosion by E. mathaei increase (by a factor three) at low pH condition, possibly leading to a destruction of the reef substrate on the longer term. Comparison with field measurements in the literature indicate that our observations are comparable to field data, meaning that the major problem of OA on tropical coral reefs may well happen in term of interspecific relationships between calcifiers and eroders, while each species displays separately higher resistance to moderate OA on the longer term.
At the end of the experiment, microbial communities could be characterized in three coral species (Acropora muricata, Pocillopora damicornis and Seriatopora hystrix), but also in the calcareous substrates, using shotgun metagenomics. A total of 22 DNA libraries was sequenced and up to 11 106 Illumina reads (2 x 150 pb) were obtained per library. Reads were then classified in taxonomic or functional categories using the SEED classification system and libraries were then compared to each other (Laghdass et al, submitted).
The prokaryotic communities associated to the three coral species featured a similar phylogenetic profile at the phylum level. The same feature was observed in calcareous substrates but the prokaryotic communities was different compared to the one associated to coral species. For instance, sequences affiliated to Cyanobacteria represented 38–63% of the reads for corals and only 6–12% for calcareous substrates. Sequences affiliated to Proteobacteria represented 14–39% of the total for corals and 44–56% for calcareous substrates. As regard to acidification, no evidence of major effects was found for coral-associated bacterial communities or those associated to the calcareous substrates. Most of the identified changes were simply a result of confinement or could be explained by an effect of natural variability. On the contrary, a significant pH effect was detected for viral communities, mainly the Siphoviridae infecting bacteria (–45% of the reads) and the Herpesviridae infecting corals and dinoflagellates (+17% of the reads). These changes were corroborated by the observation of coral tissue necrosis in one of the acidified mesocosm. This research confirms previous observations concluding that Herpesviridae may be induced by ocean acidification.
Finally, the mesocosms studies gave us the opportunity to briefly investigate another thread to corals: sedimentation (Sheridan et al 2014). It was shown that very short term (24h) sedimentation induces immune response and changes the profile of lipids in coral tissues, indicating it constitutes a major stress that mobilizes energy for a scleractinian coral.
Overall, our results indicate that many key species of a tropical coral reef (being corals, urchins or prokaryotes) resist quite well individually to moderate OA down to pHtot = 7.7 at long term (after a gradual acclimation over 6 months). However, ecological properties of the ecosystem are altered in a much deeper way. The balance between bioaccretion and bioerosion is deeply affected. The viral communities increase with more bacteriophages and coral pathogens.
List of publications related to this project
Collard, M., K. Laitat, L. Moulin, A.I. Catarino, Ph. Grosjean & Ph. Dubois, 2013. Buffer capacity of the coelomic fluid in echinoderms. Comp. Biochem. Physiol. Part A, 166:199-206.
Collard, M., A. Dery, F. Dehairs & Ph. Dubois, 2014. Euechinoidea and cidaroidea respond differently to ocean acidification. Comp. Biochem. Physiol. A, 174:45-55.
Dubois, Ph., 2014. The skeleton of postmetamorphic echinoderms in a changing world. Biol. Bull., 226:223-236.
Leblud, J., L. Moulin, A. Batigny, Ph. Dubois & Ph. Grosjean, 2014. Technical note: Artificial coral reef mesocosms for ocean acidification investigations. Biogeosciences Discuss., 11:1-43.
Moulin, L., 2014. Impact de l'acidification des océans sur l'oursin Echinometra mathaei et son activité bioérosive des récifs coralliens : étude en mésocosmes artificiels. Thèse de doctorat ULB (septembre 2014). 214pp.
Moulin, L., Ph. Grosjean, J. Leblud, A. Batigny & Ph. Dubois, 2014a. Impact of elevated pCO2 on acid-base regulation of the sea urchin Echinometra mathaei and its relation to resistance to ocean acidification: A study in mesocosms. J. Exp. Mar. Biol. Ecol., 457:97-104.
Moulin, L., Ph. Grosjean, J. Leblud, A. Batigny, M. Collard & Ph. Dubois, 2014b. Long-term mesocosms study of the effects of ocean acidification on growth and physiology of the sea urchin Echinometra mathaei. Mar. Environ. Res., 103:103-114.
Sheridan, C., Ph. Grosjean, J. Leblud, C.V. Palmer, A. Kushmaro & I. Eeckhaut, 2014. Sedimentation rapidly induces an immune response and depletes energy stores in a hard coral. Coral Reefs, 33(4):1067-1076.
Manuscripts and Ph. D. thesis submitted or in preparation
Laghdass, M., A. Batigny, J. Leblud, L. Moulin, Ph. Grosjean, R. Wattiez & D. Gillan. The impact of ocean acidification on coral-associated microbial communities. A long-term mesocosm study on three coral species. Submitted to Coral Reefs.
Leblud, J., 2015. Ecophysiological changes of hermatypic scleractinians facing ocean acidification: Studies in original chemostats and artificial mesocosms. Thèse de doctorat, UMONS. Date de défense privée: 19 juin, défense publique: 2 juillet 2015.
Leblud, J., A. Batigny & Ph. Grosjean, in prep. a. Ecophysiology of hermatypic scleractinian Seriatopora hystrix under high pCO2 chemostats. Manuscript finalized, Leblud Ph.D. thesis.
Leblud, J., L. Moulin, A. Batigny & Ph. Grosjean, in prep. b. Four coral species do not suffer from ocean acidification: long term study in artificial reef mesocosms. Manuscript included in J. Leblud, Ph.D. thesis.
Leblud, J., L. Moulin, A. Batigny & Ph. Grosjean, in prep. c. Ecophysiological changes of four scleractinian corals experiencing long term exposure to ocean acidification: studies in original chemostats. Manuscript included in L. Leblud, Ph. D. thesis.
Moulin, L., J. Leblud, A. Batigny, Ph. Compère, J. Dille, Ph. Dubois & Ph. Grosjean. Bioerosion of tropical coral reefs by the sea urchin Echinometra mathaei may triple under ocean acidification. Submitted to ICES J. Mar. Sci.
Conferences
Moulin, L., J. Leblud, A. Batigny, Ph. Dubois & Ph. Grosjean, 2014. Effects of ocean acidification on the bioerosion by the sea urchin Echinometra mathaei in coral reefs. Gordon Research Conference on Ocean Global Change Biology, Waterville Valley, NH, USA.
Sheridan ,Ch., A. Kushmaro, J.-M. Baele, Ph. Grosjean, L. Raymundo & I. Eeckhaut, 2014. Sedimentation influences on coral microbial communities in ISME 15, Séoul, Corée.
Leblud, J., Ph. Grosjean, L. Moulin & A. Batigny, 2013. Changements écophysiologiques des scléractiniaires hermatypiques sous l'augmentation de la pCO2: étude en chemostats. CIBIM, Mons, Belgique.
Moulin, L., Ph. Dubois & Ph. Grosjean, 2013. Impact de l'acidification sur la bioérosion des coraux hermatypiques par les oursins: étude en mésocosme. CIBIM, Mons, Belgique.
Laghdass, M., J. Leblud, L. Moulin, D. Gillan, Ph. Grosjean & R. Wattiez, 2012. Effect of ocean acidification on coral-associated bacterial communities in artificial mesocosms by metaproteogenomic approach. 7ième Matinée des Chercheurs, Mons, Belgique.
Dubois, Ph., A. Catarino, M. Collard, A. Dery, K. Laitat, L. Moulin & Ph. Grosjean, 2012. Adult echinoderms from fluctuating environments: Scope for adaptation or acclimatization to ocean acidification? Third International Symposium on the Ocean in a High CO2 World, Monterey, USA.
Leblud, J., Ph. Grosjean & A. Batigny, 2012. Ecophysiological Changes of Hermatypic Scleractinians in High PCO2 Chemostat. Third International Symposium on the Ocean in a High CO2 World, Monterey.
Moulin, L., J. Leblud, A. Batigny, Ph. Dubois & Ph. Grosjean, 2012. Impact of ocean acidification on the sea urchin Echinometra Mathaei and its roles as grazer and bioeroder in coral reefs. Third International Symposium on the Ocean in a High CO2 World, Monterey, USA.
Sheridan, Ch., Ph. Grosjean & I. Eeckhaut, 2012. How dirt annoying can be – a coral immunity perspective. 19Th Benelux Congress of Zoology, Brussels, Belgium.
Moulin, L., Ph. Dubois & Ph. Grosjean, 2012. Impact of ocean acidification on growth and physiology of the sea urchin Echinometra mathaei: a study in mesocosms. 14th International Echinoderm Conference, Brussels, Belgium.
Moulin, L., Ph. Grosjean & Ph. Dubois, 2011. Impact of ocean acidification on growth and physiology of Echinometra mathaei: a mesocosm study. World conference on marine biodiversity, Aberdeen, Scotland.
Leblud, J., A. Batigny & Ph. Grosjean, 2010. Study of hermatypic scleractinian Seriatopora hystrix in high pCO2 chemostats. Euro ISRS Symposium , Wageningen, Netherland