Comprendre l’association algue coralline – corail : des espèces clés aux médiateurs chimiques et microbiens

Crustose coralline algae (CCA) are commonly associated with healthy reefs and play an important role in benthic systems by guiding settlement of many habitat forming or ecologically important organisms, including corals. However, the ability of CCA to induce coral settlement is not ubiquitous among CCA species. Corals exhibit settlement preferences for certain CCA species. These preferences demonstrate the capacity of coral larvae to discriminate among CCA species and raise the question of the mechanisms involved. Despite the enormous variety of CCA species on coral reefs, little is known about the diversity of their associated chemicals and microbes and the ecological role of these compartments, notably for coral recruitment. Chapter 2 of this thesis investigated the microbial and chemical composition of six CCA species, which occupy different ecological niches on the coral reefs of Moorea (French Polynesia), and how these two compartments (i.e., microbial and chemical) relate to successful settlement success of Acropora cytherea larvae. Results showed settlement was highest on the cryptic CCA species Titanoderma prototypum and that practically no larvae settled on exposed CCA species. While all CCA species had distinct metabolic fingerprints and contained high metabolic diversity, the metabolomic diversity and richness of T. prototypum were significantly higher than those of the other CCA species. T. prototypum also hosted a significantly higher bacterial diversity than the other CCA species, and contained a higher abundance of bacteria that potentially produce antibacterial compounds. The presence of these bacteria could inhibit coral pathogens, which in turn could enhance the survival of coral settlers. Thus, coral settlement is a complex process of biochemical communications between CCA, their associated microbial surface communities and coral larvae. Despite widespread acceptance that CCA positively influence coral recruitment success, there are no experimental data on the effects of CCA species on late post-settlement survival and growth of corals. Chapter 3 tested the impact of four CCA species from two habitats (exposed and subcryptic) on the survival and growth of Pocillopora recruits. CCA had a contrasting effect on the survival of coral recruits depending on habitat and recruit size. In subcryptic habitats, CCA can reduce the survival and/or growth of coral recruits via direct competitive overgrowth, while, in exposed habitats, they can enhance coral recruitment by alleviating competition with turf algae. Importantly, this study demonstrated that not all CCA species are beneficial to the survival and growth of coral recruits and that there is considerable variability in both the outcome and process of competition between CCA and corals. Chapter 4 and 5 focused on investigating whether two environmental stressors, ocean acidification (OA) and hypoxia, respectively, impact the coral-CCA association by disrupting larval settlement behavior and recruitment of two coral species (A. cytherea and A. pulchra) on an otherwise preferred and beneficial CCA species (T. prototypum). Larvae of both coral species avoided bottom exploration and settlement in low pH environments. They avoided bottom exploration in reduced oxygen environments and settled on T. prototypum fragments only in oxygen rich environments, with settlement rates increasing exponentially with oxygen concentrations. These results indicate that low oxygen and low pH areas can negatively influence coral settlement success and that oxygen and pH act as chemical cues for coral larval orientation and settlement. This thesis aids to better understand the role of CCA, micro-organisms and chemicals in the fine-scale dynamics of coral recruitment now and under future ocean conditions. It highlights that CCA-coral interactions are complex processes that are likely mediated by chemicals and microbes and these interactions can be affected by changing environments.Les algues corallines encroûtantes (CCA) sont communément associées à des récifs sains et jouent un rôle important dans les systèmes benthiques en guidant la colonisation de nombreux organismes, comme les coraux. Cependant, la capacité des CCA à induire l’implantation des coraux ne fonctionne pas pour toutes les espèces de CCA. Les larves de coraux sélectionnent certaines espèces d’algues, ce qui pose la question des mécanismes sous-jacents. Malgré l’énorme variété d’espèces de CCA dans les récifs, on en sait peu sur leur diversité chimique et microbienne et sur le rôle écologique de ces deux composants pour le recrutement des coraux. Le chapitre 2 étudie la composition microbienne et chimique de 6 espèces de CCA sur les récifs coralliens de Moorea, et comment ces deux compartiments sont liés au succès d’implantation des larves d’Acropora cytherea. Les résultats ont révélé que le taux d’implantation était le plus élevé sur l’espèce cryptique Titanoderma prototypum. Alors que toutes les espèces de CCA avaient des empreintes métaboliques distinctes et contenaient une grande diversité métabolomique, la diversité et la richesse métabolomiques de T. prototypum étaient plus élevées que celles des autres espèces. T. prototypum hébergeait également une diversité bactérienne plus élevée, et contenait une plus grande abondance de bactéries susceptibles de produire des composés antibactériens. Ces bactéries pourraient inhiber les agents pathogènes des coraux, ce qui pourrait à son tour améliorer la survie des larves. Ainsi, le recrutement corallien est un processus complexe de communications biochimiques entre les CCA, leurs communautés de surface microbiennes associées et les larves de coraux. Malgré la large acceptation que certaines espèces de CCA influencent positivement le recrutement corallien, il n’y a pas de données expérimentales sur les effets des espèces de CCA sur la survie et la croissance post-implantation tardive des coraux. Le chapitre 3 teste l’impact de 4 espèces de CCA, de deux types d’habitats (exposés et subcryptiques), sur la survie et la croissance des recrues de Pocillopora. Les CCA ont eu un effet contrasté sur la survie des recrues coralliennes suivant l’habitat et de la taille des recrues. Dans les habitats subcryptiques, les CCA réduisaient la survie et/ou la croissance des recrues coralliennes via la compétition directe, tandis que, dans les habitats exposés, elles amélioraient le recrutement des coraux en atténuant la concurrence avec le gazon algal. Cette étude a démontré que toutes les espèces de CCA ne sont pas bénéfiques à la survie et à la croissance des recrues coralliennes et qu’il existe une variabilité considérable dans l’issue et le processus de compétition entre les CCA et les coraux. Chapitres 4 et 5 déterminent si deux facteurs de stress environnementaux, respectivement l’acidification des océans (AO) et l’hypoxie, affectent l’association corail-CCA en perturbant le comportement et l’implantation des larves des deux espèces de coraux (A. cythera et A. pulchra), ainsi que leur recrutement, sur une espèce de CCA appropriée. Les larves des deux espèces évitaient l’exploration et l’implantation dans des environnements à faible pH ou à oxygène réduit. Ces résultats indiquent que les zones à faible teneur en oxygène et pH peuvent influencer négativement le succès d’implantation des larves de coraux et que l’oxygène et le pH peuvent être des signaux chimiques pour l’orientation et l’implantation des larves de coraux. Cette thèse aide à mieux comprendre le rôle des CCA, des micro-organismes et des composés chimiques dans la dynamique à petite échelle du recrutement des coraux maintenant et dans les conditions océaniques futures. Les résultats soulignent que les interactions CCA-corail sont des processus complexes qui sont probablement médiés par des composés chimiques et microbiens et que ces interactions peuvent être affectées par des environnements changeants

Understanding the association between coralline algae and corals : from key species to chemical and microbial mediators

Les algues corallines encroûtantes (CCA) sont communément associées à des récifs sains et jouent un rôle important dans les systèmes benthiques en guidant la colonisation de nombreux organismes, comme les coraux. Cependant, la capacité des CCA à induire l’implantation des coraux ne fonctionne pas pour toutes les espèces de CCA. Les larves de coraux sélectionnent certaines espèces d’algues, ce qui pose la question des mécanismes sous-jacents. Malgré l’énorme variété d’espèces de CCA dans les récifs, on en sait peu sur leur diversité chimique et microbienne et sur le rôle écologique de ces deux composants pour le recrutement des coraux. Le chapitre 2 étudie la composition microbienne et chimique de 6 espèces de CCA sur les récifs coralliens de Moorea, et comment ces deux compartiments sont liés au succès d’implantation des larves d’Acropora cytherea. Les résultats ont révélé que le taux d’implantation était le plus élevé sur l’espèce cryptique Titanoderma prototypum. Alors que toutes les espèces de CCA avaient des empreintes métaboliques distinctes et contenaient une grande diversité métabolomique, la diversité et la richesse métabolomiques de T. prototypum étaient plus élevées que celles des autres espèces. T. prototypum hébergeait également une diversité bactérienne plus élevée, et contenait une plus grande abondance de bactéries susceptibles de produire des composés antibactériens. Ces bactéries pourraient inhiber les agents pathogènes des coraux, ce qui pourrait à son tour améliorer la survie des larves. Ainsi, le recrutement corallien est un processus complexe de communications biochimiques entre les CCA, leurs communautés de surface microbiennes associées et les larves de coraux. Malgré la large acceptation que certaines espèces de CCA influencent positivement le recrutement corallien, il n’y a pas de données expérimentales sur les effets des espèces de CCA sur la survie et la croissance post-implantation tardive des coraux. Le chapitre 3 teste l’impact de 4 espèces de CCA, de deux types d’habitats (exposés et subcryptiques), sur la survie et la croissance des recrues de Pocillopora. Les CCA ont eu un effet contrasté sur la survie des recrues coralliennes suivant l’habitat et de la taille des recrues. Dans les habitats subcryptiques, les CCA réduisaient la survie et/ou la croissance des recrues coralliennes via la compétition directe, tandis que, dans les habitats exposés, elles amélioraient le recrutement des coraux en atténuant la concurrence avec le gazon algal. Cette étude a démontré que toutes les espèces de CCA ne sont pas bénéfiques à la survie et à la croissance des recrues coralliennes et qu’il existe une variabilité considérable dans l’issue et le processus de compétition entre les CCA et les coraux. Chapitres 4 et 5 déterminent si deux facteurs de stress environnementaux, respectivement l’acidification des océans (AO) et l’hypoxie, affectent l’association corail-CCA en perturbant le comportement et l’implantation des larves des deux espèces de coraux (A. cythera et A. pulchra), ainsi que leur recrutement, sur une espèce de CCA appropriée. Les larves des deux espèces évitaient l’exploration et l’implantation dans des environnements à faible pH ou à oxygène réduit. Ces résultats indiquent que les zones à faible teneur en oxygène et pH peuvent influencer négativement le succès d’implantation des larves de coraux et que l’oxygène et le pH peuvent être des signaux chimiques pour l’orientation et l’implantation des larves de coraux. Cette thèse aide à mieux comprendre le rôle des CCA, des micro-organismes et des composés chimiques dans la dynamique à petite échelle du recrutement des coraux maintenant et dans les conditions océaniques futures. Les résultats soulignent que les interactions CCA-corail sont des processus complexes qui sont probablement médiés par des composés chimiques et microbiens et que ces interactions peuvent être affectées par des environnements changeants.Crustose coralline algae (CCA) are commonly associated with healthy reefs and play an important role in benthic systems by guiding settlement of many habitat forming or ecologically important organisms, including corals. However, the ability of CCA to induce coral settlement is not ubiquitous among CCA species. Corals exhibit settlement preferences for certain CCA species. These preferences demonstrate the capacity of coral larvae to discriminate among CCA species and raise the question of the mechanisms involved. Despite the enormous variety of CCA species on coral reefs, little is known about the diversity of their associated chemicals and microbes and the ecological role of these compartments, notably for coral recruitment. Chapter 2 of this thesis investigated the microbial and chemical composition of six CCA species, which occupy different ecological niches on the coral reefs of Moorea (French Polynesia), and how these two compartments (i.e., microbial and chemical) relate to successful settlement success of Acropora cytherea larvae. Results showed settlement was highest on the cryptic CCA species Titanoderma prototypum and that practically no larvae settled on exposed CCA species. While all CCA species had distinct metabolic fingerprints and contained high metabolic diversity, the metabolomic diversity and richness of T. prototypum were significantly higher than those of the other CCA species. T. prototypum also hosted a significantly higher bacterial diversity than the other CCA species, and contained a higher abundance of bacteria that potentially produce antibacterial compounds. The presence of these bacteria could inhibit coral pathogens, which in turn could enhance the survival of coral settlers. Thus, coral settlement is a complex process of biochemical communications between CCA, their associated microbial surface communities and coral larvae. Despite widespread acceptance that CCA positively influence coral recruitment success, there are no experimental data on the effects of CCA species on late post-settlement survival and growth of corals. Chapter 3 tested the impact of four CCA species from two habitats (exposed and subcryptic) on the survival and growth of Pocillopora recruits. CCA had a contrasting effect on the survival of coral recruits depending on habitat and recruit size. In subcryptic habitats, CCA can reduce the survival and/or growth of coral recruits via direct competitive overgrowth, while, in exposed habitats, they can enhance coral recruitment by alleviating competition with turf algae. Importantly, this study demonstrated that not all CCA species are beneficial to the survival and growth of coral recruits and that there is considerable variability in both the outcome and process of competition between CCA and corals. Chapter 4 and 5 focused on investigating whether two environmental stressors, ocean acidification (OA) and hypoxia, respectively, impact the coral-CCA association by disrupting larval settlement behavior and recruitment of two coral species (A. cytherea and A. pulchra) on an otherwise preferred and beneficial CCA species (T. prototypum). Larvae of both coral species avoided bottom exploration and settlement in low pH environments. They avoided bottom exploration in reduced oxygen environments and settled on T. prototypum fragments only in oxygen rich environments, with settlement rates increasing exponentially with oxygen concentrations. These results indicate that low oxygen and low pH areas can negatively influence coral settlement success and that oxygen and pH act as chemical cues for coral larval orientation and settlement. This thesis aids to better understand the role of CCA, micro-organisms and chemicals in the fine-scale dynamics of coral recruitment now and under future ocean conditions. It highlights that CCA-coral interactions are complex processes that are likely mediated by chemicals and microbes and these interactions can be affected by changing environments

Data from: Evidence for water-mediated mechanisms in coral–algal interactions

Although many coral reefs have shifted from coral-to-algal dominance, the consequence of such a transition for coral–algal interactions and their underlying mechanisms remain poorly understood. At the microscale, it is unclear how diffusive boundary layers (DBLs) and surface oxygen concentrations at the coral–algal interface vary with algal competitors and competitiveness. Using field observations and microsensor measurements in a flow chamber, we show that coral (massive Porites) interfaces with thick turf algae, macroalgae, and cyanobacteria, which are successful competitors against coral in the field, are characterized by a thick DBL and hypoxia at night. In contrast, coral interfaces with crustose coralline algae, conspecifics, and thin turf algae, which are poorer competitors, have a thin DBL and low hypoxia at night. Furthermore, DBL thickness and hypoxia at the interface with turf decreased with increasing flow speed, but not when thick turf was upstream. Our results support the importance of water-mediated transport mechanisms in coral–algal interactions. Shifts towards algal dominance, particularly dense assemblages, may lead to thicker DBLs, higher hypoxia, and higher concentrations of harmful metabolites and pathogens along coral borders, which in turn may facilitate algal overgrowth of live corals. These effects may be mediated by flow speed and orientation

Importance of intertidal seagrass beds as nursery area for coral reef fish juveniles (Mayotte, Indian Ocean)

International audienceThe present study highlights the importance of intertidal seagrass beds as nursery areas for coral reef fish juveniles along four sites (Mtsoubatsou, Sohoa, Boueni, Ngouja) on the western coast of Mayotte Island. The results collected by underwater visual census from November 2012 to January 2013 showed that mean total fish density between adults and juveniles varied significantly at each site, with juveniles always being more abundant in seagrass beds than adults. Of the total fish assemblages sampled in seagrass beds, 73% were juveniles and few adults of large species were observed. Overall, our study highlights the important functional role of intertidal seagrass beds for fish assemblages, as they are the primary habitat for the juveniles of many fish species on Mayotte reefs. Seagrass beds, however, are very vulnerable ecosystems and are decreasing worldwide. Therefore it is of primary importance to protect seagrass beds within the Indo-Pacific

Effects of Asparagopsis taxiformis metabolites on the feeding behaviour of post‐larval Acanthurus triostegus

International audienc

Coral larval settlement preferences linked to crustose coralline algae with distinct chemical and microbial signatures

International audienceThe resilience of coral reefs is dependent on the ability of corals to settle after disturbances. While crustose coralline algae (CCA) are considered important substrates for coral settlement, it remains unclear whether coral larvae respond to CCA metabolites and microbial cues when selecting sites for attachment and metamorphosis. This study tested the settlement preferences of an abundant coral species (Acropora cytherea) against six different CCA species from three habitats (exposed, subcryptic and cryptic), and compared these preferences with the metabolome and microbiome characterizing the CCA. While all CCA species induced settlement, only one species (Titanoderma prototypum) significantly promoted settlement on the CCA surface, rather than on nearby dead coral or plastic surfaces. This species had a very distinct bacterial community and metabolomic fingerprint. Furthermore, coral settlement rates and the CCA microbiome and metabolome were specific to the CCA preferred habitat, suggesting that microbes and/or chemicals serve as environmental indicators for coral larvae. Several amplicon sequence variants and two lipid classes-glycoglycerolipids and betaine lipids-present in T. prototypum were identified as potential omic cues influencing coral settlement. These results support that the distinct microbiome and metabolome of T. prototypum may promote the settlement and attachment of coral larvae

Coral larval settlement preferences linked to crustose coralline algae with distinct chemical and microbial signatures

The resilience of coral reefs is dependent on the ability of corals to settle after disturbances. While crustose coralline algae (CCA) are considered important substrates for coral settlement, it remains unclear whether coral larvae respond to CCA metabolites and microbial cues when selecting sites for attachment and metamorphosis. This study tested the settlement preferences of an abundant coral species (Acropora cytherea) against six different CCA species from three habitats (exposed, subcryptic and cryptic), and compared these preferences with the metabolome and microbiome characterizing the CCA. While all CCA species induced settlement, only one species (Titanoderma prototypum) significantly promoted settlement on the CCA surface, rather than on nearby dead coral or plastic surfaces. This species had a very distinct bacterial community and metabolomic fingerprint. Furthermore, coral settlement rates and the CCA microbiome and metabolome were specific to the CCA preferred habitat, suggesting that microbes and/or chemicals serve as environmental indicators for coral larvae. Several amplicon sequence variants and two lipid classes-glycoglycerolipids and betaine lipids-present in T. prototypum were identified as potential omic cues influencing coral settlement. These results support that the distinct microbiome and metabolome of T. prototypum may promote the settlement and attachment of coral larvae