Reef refugia out of the shadows: dynamics of marginal coral reef ecosystems over the past 30 million years in the Coral Triangle

Coral reefs are the most diverse marine ecosystems on Earth and provide enormous economic value for hundreds of millions of people including fisheries, tourism, and coastal protection. However, these benefits are threatened by the rapid decline of coral reefs resulting from accelerating human impacts on local to global scales. Confronting this reef crisis with limited resources requires prioritisation of protection actions, and many researchers are now turning to reef ecosystems living outside of typical shallow, clear-water habitats as critical priorities for additional research. There is new evidence that these so-called marginal reefs living in turbid or deeper water can be more resilient to bleaching, changes in water quality, and other impacts. Increased bleaching resilience might result from sediments in the water that limit UV stress, or because the corals may be more readily able to take advantage of food sources in the plankton. Thus, marginal reefs potentially serve as refugia for resilient corals, and could be critical for the future recovery of declining clear-water reefs. However, most studies of marginal reefs have focused on contemporary (and in a few cases historical) assessments from sites on the Great Barrier Reef (GBR) and the Caribbean. New datasets from different regions are needed to capture the full range of modern human impacts (especially in areas of the most diverse coral development), and we also need data that spans the timescales (centuries to millennia) necessary to capture coral ecological adaptation and migration within marginal settings. In this context, recent discoveries of exceptionally preserved fossils from the Coral Triangle (CT) region of Southeast Asia provide a unique opportunity to integrate present-day ecological data with information from the geological record to document the evolutionary and ecological history of turbid water reefs in the modern-day global biodiversity hotspot. There is an urgent need for more information on the diversity, structure, and functioning of marginal reefs in the CT in order to help develop management strategies they continue to respond to human impacts.

The long-term temporal scope of our study is thus significant. A growing body of research aims to describe the composition, distribution, and genetic structure of potential present-day reef refugia and we will add data from the fossil record into these analyses. There is a compelling case to do this because reef resilience is likely to be shaped by long-term processes with deep roots in evolutionary history. We will assess the dual role of marginal reefs in the CT as both cradles and refugia of diversity. Key research questions include: 1) has coral diversity of marginal ecosystems changed through time? 2) how have reef communities responded to environmental changes on regional or global scales? 3) how has reef functioning in marginal settings changed and what have been the consequences for reef-associated biota? 4) how easy has it been for reef-corals to move from marginal to clear-water reefs during the evolution of the biodiversity hotspot, and 5) what could be the consequences for the modern biota if clear water habitats become increasingly inhospitable?

To address these questions we will produce new comprehensive datasets of species occurrences, abundances, morphological traits, ecological data, and environments that cover 30 million years of reef history of the CT. With this resource, we will provide rigorous answers to long-debated issues by applying new tools for molecular systematics, geochemistry, and evolutionary patterns to modern reefs and an extensive and well-sampled fossil record. Ultimately, we will be able to reveal the murky history of marginal reefs in the CT and better understand the potential future trajectories of change for coral reefs in the CT and in other regions that depend on coral reefs for their economic and ecological value.

Coral reefs in the CT are the most diverse reefs on Earth yet they remain poorly studied. Of the 2463 articles published by the journal Coral Reefs since 1982 only 8% concern reefs from the CT, compared with 46% from Australia. For marginal reefs there are even fewer studies from the CT. Here we will fill this gap with new data on coral occurrences and abundances, morphological and functional traits of corals, molecular markers and phylogenetic information for target groups, together with environmental data based on geochemical proxies and direct measurements on modern reefs. There is an increasing interest in coral response to environmental stress in marginal habitats. New data collected in this study will be relevant to this emerging field.

We identify three main groups of stakeholders that will directly benefit from the outcomes of this project as follow:

Scientific community: the results our study will benefit not only reef researchers but also a broad community of taxonomists, ecologists, evolutionary biologists, palaeontologists and palaeoclimate workers studying biotic responses to climate change. We will reach the scientific community by publishing in high-profile international journals and by participating in international professional meetings. Our datasets will be available on open data repositories such as NHM data portal and we will load data into community platforms including the Paleobiology Database, coraltraits.org, and the Community of Earth Systems Model. Analytical methods and scripts will also be made available to follow best practices of Open Science.

Conservation agencies: our research results will benefit governmental and non-governmental organisations linked to the conservation and management of coral reefs, such as the International Union for Conservation of Nature, World Wide Fund for Nature, The Nature Conservancy, The United Nations Educational, Scientific and Cultural Organization and other UK-based organisations such as the Marine Conservation Society, and the Joint Nature Conservation Committee. We will partner with the marine and coastal programme of the Zoological Society of London to organise a one-day workshop at NHM that will include stakeholders from the research community and conservation agencies. The aim of this event is to present the main results of this project and discuss further application of the information compiled, for example to address the protection of marginal reefs and coral species vulnerability status. At regional scale, we will organise an additional half-day workshop in Sabah with representatives of artisanal fisheries, diving centres, the ecotourism sector, and members of the Semporna Park in order to raise awareness about the importance of marginal reefs. We will deliver short communications to popular scientific magazines of conservation agencies and NHM publications, or elsewhere as invited.

Public outreach: the NHM is a leading institution for public engagement in the UK that offers multiple opportunities to reach broad audiences. In 2015 and 2016, over 100,000 visitors have experienced coral reefs as part of the recent NHM exhibition "Coral Reefs: Secret Cities of the Sea" and the innovative virtual reality experience "David Attenborough's Great Barrier Reef Dive". We will organise several sessions of "visiteering", a new museum programme that aims to engage new audiences through hands-on collections in the Specimen Preparation Area (SPA) that is part of the exhibitions area. We will contribute to the planned temporary exhibitions "Life in the dark" (2018) and "Nature's architects" (2019) with coral specimens and habitat information on marginal reefs that thrive under low-light conditions. We will participate a range of public events, including Science Late Nights events. We will have a blog to communicate expedition news and provide topical information and publications by the project. We will have a public display at the National Museum Cardiff.