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Ecology The marine realm of possibility Dr Claude Payri is coordinating a project to determine the origins and mechanisms behind macroalgae proliferations in tropical and subtropical coastal ecosystems. We spoke with her and her collaborators about their ongoing quest to uncover the what, how and where of marine species Can you explain why the proliferation of macroalgae has previously been poorly studied? CP: Macroalgae mostly live on the hard substratum of coastal marine ecosystems, from the surface down to a depth of 150 m. Therefore, access to marine benthic populations is more difficult than access to terrestrial communities or oceanic plankton. Studying macroalgal proliferations requires specific methods and techniques of investigation that aren’t easy to routinely use. Dr Aschwin Engelen: Also, the scientific community of phycologists is currently very small worldwide and proliferating species are just one tiny subset of the total seaweed species of interest. Dr Frederique Viard: There is a lack of existing data which makes it difficult to establish baselines for further study. Furthermore, the fact that the general public and policy makers have a poor perception of the issue leads to a lack of interest in addressing it. However, this problem isn’t specific to macroalgal studies – almost all marine species (except marine mammals or corals) suffer through a lack of interest. Dr Olivier Thomas: Because this is a highly complex area of study, in terms of the number of species and interactions, it’s difficult to find an interdisciplinary team working on the same group of organisms. What drew the group to study Asparagopsis taxiformis and Asparagopsis armata? Dr Thierry Perez: It’s more a question of who – Claude Payri! She was facing the proliferation of an Asparagopsis on the outer slope of the New Caledonian coral reef and needed complementary skills to implement an interdisciplinary research project. I duly obliged. CP: People in New Caledonia pinpointed blooms of Asparagopsis and recorded the impacts on coral reefs. As the genus was known to be one of the worst invasive species, we 1 INTERNATIONAL INNOVATION needed to establish its status (native versus introduced), then characterise the proliferations to determine whether impacts on cnidarians building coral reefs could be found. Is the approach you adopted particularly unique? CP: Our approach combined various disciplines, including metabolomics, phylogeny and molecular taxonomy implemented at different biological scales. We applied this at different geographical scales: seven different local regions and globally. AE: Knowledge of the marine realm is rudimentary, especially in seaweeds; combining 16S amplicon sequencing and metagenomics on seaweed ecology, proliferation and competition is rare, particularly on the scale covered by the Seaprolif project. Could you briefly introduce the ERA-NET NETBIOME programme and describe its relationship to Seaprolif? ALL: The EU Sixth Framework Programme (FP6)-funded project is a consortium of 11 partners linking bodies related to the overseas entities from five European member states. The aim is to initiate and stimulate cooperation and coordination of research programmes for the sustainable and integrated management of biodiversity. Specifically, in a way that addresses the needs of the threatened ecosystems of the European outmost regions and overseas countries and territories. Calls for transnational research projects are one of the main goals of the ERA-NETs, as a mechanism for validating the cooperative effort between the various funding agencies. Ultimately, this has led to the funding of several research projects on biodiversity management in support of sustainable development in Europe’s tropical and subtropical outermost regions and overseas countries and territories. In November 2010, NETBIOME called for proposals for transnational and transregional research entitled ‘Towards Biodiversity Management in support of Sustainable Development in Tropical and Subtropical EU’. This resulted in 80 manifestations of interest and 35 project applications. Following evaluations, seven projects were selected for funding, one of which was Seaprolif. What inspires you in your day-to-day work? CP: As a phycologist, I am inspired by the biodiversity of the marine flora associated with coral reef, the question of species’ boundaries and biogeographical distribution. In other words – how many species, where are they and where do they come from? AE: Previous studies have suggested that microbiomes might be maintained during invasion or proliferation and form an important part of the adaptive and stress-resistant potential of the seaweed host. Therefore, investigating the microbiomes of these species is of great interest. Asparagopsis is known to produce halogenated compounds with strong antimicrobial activities, so it’s extremely interesting to investigate what kind of bacteria are associated with these seaweeds, their function and if they are involved in the production/ decomposition of these compounds. TP: I am driven to better understand the mechanisms behind all biotic interactions in the seas: prey-predator, host-pathogen, competition for space and resource relationships. FV: My inspiration lies in the fact that the project supports previous findings of mine regarding the high level of unknown biodiversity in the marine realm, including in supposedly well-known habitats like coastal marine habitats. It inspires me daily to still question myself on what a species or a population is, and what processes (natural or human-mediated drivers) are responsible for the patterns observed in nature. To the bottom of coastal ecosystems The ERA-NET NETBIOME programme enabled the establishment of Seaprolif – an interdisciplinary project involving six French and two Portuguese research teams. The project focuses on two red seaweed species and their circumglobal proliferation Biological diversity helps keep ecosystems in a natural balance. The permanent interactions between the components of an ecosystem are more resilient and adaptable to external stresses when diversity is higher. Additionally, the potentially damaging impacts to humans are notable. For example, the wider the variety of species, the better the scope for increasing available food services. This is particularly important given the expanding global population. Alarmingly, the proliferation of macroalgae in coastal ecosystems worldwide is perceived as a possible serious threat to the biodiversity of such ecosystems. The damaging effects of macroalgae proliferation are among their most alarming in coral reefs, where coral and algal competition can modify the balance and functioning of that particular ecosystem in danger. Expanding understanding Until recently, studies on the origins and mechanisms of these proliferations have been relatively scarce for two main reasons. First, the taxonomy of macroalgae is often highly challenging and specialists of this domain – phycologists – are rare, but these basic data are a prerequisite for further studies of their impact. Second, poor perception of the problem from a public and policy maker point of view reveals a need for scientists to adequately address this issue and provide the public with simple and clear communications. Enter researchers from France and Portugal who have established a vast network that has afforded the opportunity to collect samples from a great number of regions. This has enabled the team to highlight the diversity of macroalgae and unearth new discoveries concerning new lineages and new cryptic species. The International Union for Conservation of Nature has identified the genus Asparagopsis (Rhodophyta) as one of the 100 worst invasive species in subtropical and temperate areas, prompting the team to focus on Asparagopsis taxiformis and Asparagopsis armata. Controlling proliferation The Seaprolif project coordinated by Dr Claude Payri started in February 2012 and concluded in August 2015. Thanks to the scope of the consortium, the geographical areas studied are spread around five regions belonging to four French overseas countries and territories: New Caledonia and French Polynesia for the Pacific basin, La Réunion in the Western Indian Ocean, Guadeloupe in the French Antilles, as well as the Portuguese outermost regions Azores and Madeira in the Atlantic Ocean. In addition, surveys were conducted and observations made in the Mediterranean Sea and Atlantic Portugal coast. The team aimed to fulfil three specific objectives. First, to establish the status of the algal proliferation and monitor the interactions between Asparagopsis individuals and native species like cnidarians, mostly hard tropical corals and temperate corals (a phylum of over 10,000 marine species), across three oceans. Second, to identify Asparagopsis lineages and populations using three combined approaches: a phylogeography analysis to determine whether clades (organisms with a common ancestor) had been introduced or were native; the relevance of metabolomics fingerprinting to differentiate between taxa and clades; and the assessment of the microbial communities associated with Asparagopsis samples using next-generation sequencing technology. www.internationalinnovation.com 2 Seaprofil OBJECTIVE To shed light on the origin and mechanisms of macroalgae proliferation. KEY COLLABORATORS Dr Claude Payri; Ms Sylvie Fiat, Institute of Research for Development, UMR ENTROPIE, New Caledonia • Dr Mehdi Adjeroud, Institute of Research for Development, UMR ENTROPIE, Perpignan, France • Dr Mayalen Zubia-arreta, UFP, UMR EIO, French Polynesia • Monsieur Jean-Pascal Quod, ARVAM, La Réunion • Dr Claude Bouchon; Dr Yolande Bouchon, Université des Antilles, Guadeloupe • Dr Frédérique Viard, CNRS, Station Biologique Roscoff, France • Dr Thierry Perez, CNRS, IMBE, Marseille, France • Dr Olivier Thomas, UNS, Nice, France • Dr Aschwin Engelen, CCMAR, Faro, Portugal • Dr Joao Monteiro; Ms Paola Paretti, IMAR, Horta, Azores PhD students: Dr Laury Dijoux, IRD, UMR ENTROPIE, New Caledonia (co-supervised by Payri and Viard) • Stéphane Greff, IMBE, Marseille, France (cosupervised by Perez and Thomas) PARTNERS Institut de Recherche pour le Développement, New Caledonia • Centre National de Recherche Scientifique, Roscoff, France • Centre National de Recherche Scientifique, IMBE, Marseille, France • Université Nice Sophia Antipolis, France • Agence Pour la Recherche et la Valorisation Marine (ARVAM), La Réunion • Université des Antilles, UMR BOREA, Guadeloupe • Center of Marine Sciences (CCMAR), Portugal • Instituto do Mar (IMAR), Azores FUNDING EU Sixth Framework Programme (FP6) • French National Research Agency (ANR) • Agence de Développement de la Calédonie (ADECAL) • Fundação para a Ciência e a Tecnologia (FCT) • Région Réunion •Région Guadeloupe • Pôle Mer Méditerranée CONTACT Dr Claude Payri Project Coordinator Institute of Research for Development UMR ENTROPIE 101, Promenade Roger Laroque BP A5 98848 Noumea New Caledonia T +687 26 07 50 E [email protected] http://bit.ly/agencenationalerecherche @UMREntropie DR CLAUDE PAYRI works as research Director at the Institute of Research for Development (IRD) in Noumea, New Caledonia. Her research is focused on the biodiversity of marine flora associated to coral reef ecosystems, particularly integrative taxonomy and biogeography at the Indo-pacific scale. Within the Seaprolif project she contributes to the sampling and investigates the taxonomy, phylogeny and ecology aspects of Asparagopsis. 3 INTERNATIONAL INNOVATION The third and final objective was to test the proliferation of Asparagopsis – both in situ and in aquaria – and the ecological harm it may inflict upon cnidarians. More specifically, the researchers examined the natural toxicity of algal species on the health of coral. Ultimately, in achieving these three objectives, the team was able to fill knowledge gaps to provide a better understanding of the mechanisms behind algal proliferation – essential when determining effective means of controlling and managing the abundance of Asparagopsis. New clades, new species Over the course of the project, the team made several important discoveries. A new cryptic species was found in the ‘species’ A. armata, demonstrating that there are actually two different species under this name. Importantly, the researchers ascertained that while this could not be recognised morphologically, it could be seen using molecular, DNAbased tools. The researchers also unearthed several key findings regarding the native or introduced status of each species in each location. “We discovered a new lineage of A. taxiformis that was restricted to the South Pacific, including New Caledonia and French Polynesia,” explains Payri. The introduced origin of other A. taxiformis lineages was confirmed in both the Mediterranean and Atlantic. Further findings included the discovery of a new clade in A. taxiformis which, so far, has been found to be endemic from a single region surrounding New Caledonia, New Zealand and one part of Australia. Interestingly, the team has determined that this clade is unlikely to have been transported by human activities and probably evolved in the South Pacific. Asparagopsis Although Asparagopsis is widely known for its antimicrobial properties, it turns out to harbour a rich associated bacterial community that shows distinguished differentiation among higher taxonomic levels of the host, but that is also strongly dependent on the environment in which the Asparagopsis host occurs. Metabolomics analyses highlighted a high and untapped chemical diversity. The researchers isolated and properly characterised two new brominated compounds with original antibacterial, antifungal, and cytotoxic activities. The comparative analyses of a proxy of the algae bioactivity showed that temperate individuals are overall more toxic than tropical ones. However, all ecological assessment, performed both in natural conditions and in aquaria, did not allow the team to demonstrate a negative effect on native corals. Spread the news The team is now embarking on a mission to disseminate its findings to the scientific community and general public. The goal is to foster further research and inform policies designed to protect tropical and subtropical coastal ecosystems around the world, eg. as part of the French coral reef initiative – IFRECOR – action plan. Ironically, one of the papers they have published acknowledges how little is known about marine biodiversity for, although the group’s endeavours have gone some way to filling in knowledge gaps, spaces remain. Meanwhile, citizens have been encouraged to report any incidences of Asparagopsis species proliferation they have noticed, especially divers and marine parks managers. In these ways, the Seaprolif team hopes to cement the foundations for better understanding and monitoring of marine biodiversity and its interconnectivity in relation to climate change consequences.