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

珊瑚礁是地球上最多样化的海洋生态系统，为数亿人提供了巨大的经济价值，包括渔业、旅游业和海岸保护。然而，由于人类对地方和全球范围的加速影响，这些好处受到了珊瑚礁迅速减少的威胁。面对这种资源有限的珊瑚礁危机，需要优先采取保护行动，许多研究人员现在转向生活在典型的浅水、清水栖息地之外的珊瑚礁生态系统，作为进一步研究的关键优先事项。有新的证据表明，这些所谓的边缘珊瑚礁生活在浑浊或更深的水中，对白化、水质变化和其他影响更有弹性。增强的抗白化能力可能是由于水中的沉积物限制了紫外线的压力，或者因为珊瑚可能更容易利用浮游生物中的食物来源。因此，边缘珊瑚礁有可能成为弹性珊瑚的避难所，并可能对未来逐渐减少的清水珊瑚礁的恢复至关重要。然而，大多数关于边缘珊瑚礁的研究都集中在大堡礁（GBR）和加勒比海地区的当代（少数情况下是历史）评估上。需要来自不同地区的新数据集来捕捉现代人类影响的全部范围（特别是在珊瑚发展最多样化的地区），我们还需要跨越时间尺度（数百年至数千年）的数据，以便在边缘环境中捕捉珊瑚的生态适应和迁移。在这种背景下，最近在东南亚珊瑚三角（CT）地区发现的保存完好的化石提供了一个独特的机会，将当今的生态数据与地质记录的信息结合起来，记录现代全球生物多样性热点地区混浊水珊瑚礁的进化和生态历史。目前迫切需要更多关于CT边缘珊瑚礁的多样性、结构和功能的信息，以帮助制定管理策略，继续应对人类的影响。因此，我们研究的长期时间范围是重要的。越来越多的研究旨在描述潜在的现代珊瑚礁避难所的组成、分布和遗传结构，我们将把化石记录的数据添加到这些分析中。这样做有一个令人信服的理由，因为珊瑚礁的恢复能力很可能是由长期的过程形成的，在进化史上有很深的根源。我们将评估大堡礁边缘珊瑚礁作为生物多样性摇篮和避难所的双重作用。重点研究问题包括：1)边缘生态系统的珊瑚多样性是否随时间而变化？2)珊瑚礁群落如何在区域或全球尺度上对环境变化作出反应？3)边缘环境中珊瑚礁的功能发生了怎样的变化，对与珊瑚礁相关的生物群有什么影响？4)在生物多样性热点的进化过程中，珊瑚礁珊瑚从边缘礁石向清水礁石的迁移有多容易？ 5)如果清水栖息地变得越来越不适宜居住，对现代生物群会有什么后果？为了解决这些问题，我们将制作新的综合数据集，包括物种发生、丰度、形态特征、生态数据和环境，涵盖CT的3000万年珊瑚礁历史。有了这些资源，我们将通过应用分子系统学、地球化学和现代珊瑚礁进化模式的新工具，以及广泛而充分采样的化石记录，为长期争论的问题提供严谨的答案。最终，我们将能够揭示CT边缘珊瑚礁的模糊历史，并更好地了解CT和其他依赖珊瑚礁经济和生态价值的地区珊瑚礁的潜在未来变化轨迹。

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.