Science, Solutions and the Future: The Great Barrier Reef in a Time of Change

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SCIENCE, SOLUTIONS AND THE FUTURE: THE GREAT BARRIER REEF IN A TIME OF CHANGE FINAL SYNTHESIS STAKEHOLDER REPORT: QUEENSLAND PREMIER’S FELLOWSHIP Professor Ove Hoegh-Guldberg The Global Change Institute The University of Queensland


FOREWORD

DR GEOFF GARRETT, QUEENSLAND CHIEF SCIENTIST The Great Barrier Reef is the world’s largest coral reef ecosystem and one of the seven wonders of the natural world. It is not only incredibly valuable from an environmental perspective – it also generates substantial income for Queensland and Australia, contributing around $6 billion to our economy annually and supporting more than 60,000 Queensland jobs. To protect (and grow) this income flow, we need to make the right management decisions based on scientific understanding and objective evidence. This will help ensure our unique resource and natural wonder remains resilient in the face of immediate pressures like pollution, and future pressures such as ocean acidification and climate change. Without the right management we are effectively flying an airplane ‘blind’ – eventually a mistake, potentially a critical one, will be made that affects all those on-board. Recent evidence has shown the particular vulnerability of the Great Barrier Reef to cyclones, although we know that reefs can recover between such events given the right environment. When this recovery period between cyclones is impacted by polluted run-off, increased bleaching due to higher temperatures or increased ocean acidification, their impacts are likely to be more severe and long-lasting. Essentially, the Great Barrier Reef now faces its most severe set of threats in its history. The Premier’s Fellowship program enticed experienced researchers of national and international prominence to lead Queensland-based research teams and address the challenges facing our state. The global market for top-flight researchers is highly competitive as the importance of science in solving local and global issues is increasingly recognised. Professor Ove Hoegh-Guldberg and his collaborators have made a significant contribution to our understanding of two of the biggest threats to the Great Barrier Reef – rising seawater temperature and ocean acidification. I applaud the collaborative research effort, which tapped into both national and international expertise to produce this synthesis report of both economic and environmental relevance.

INTRODUCTION

PROFESSOR OVE HOEGH-GULDBERG, PREMIER’S FELLOW AND DIRECTOR, GLOBAL CHANGE INSTITUTE, THE UNIVERSITY OF QUEENSLAND The Great Barrier Reef (GBR) is the world’s largest continuous coral reef ecosystem, stretching over 2,000 km down the east coast of Australia. With over $6 billion being contributed to the Queensland economy each year, the GBR is also one of the greatest economic assets for the state of Queensland and Australia. Ensuring its sustainability has been the focus of most state and federal governments over the last 40 years, with international interest being ascribed following its World Heritage listing in 1981. Despite state and national appreciation of the value the GBR, it is nonetheless in serious decline. The Australian Institute of Marine Science (AIMS) reported that coral populations have declined by almost 50% since 1980. Reef-building corals are the cornerstone of coral reefs, defining much of the three-dimensional structure and hence biodiversity. At the heart of the decline is the reduced resilience of corals and their ability to bounce back from cyclones, crownof-thorns starfish outbreaks, and mass coral bleaching and mortality. Simple extrapolation of these measurements of coral cover over time suggest that the GBR will have extremely low coral abundance within 20–30 years. The reduced resilience of coral populations, in terms of bouncing back from disturbance, has its origin in the changing levels of stress associated with both local and global factors. At a local level, declining water quality has impacted coastal reef systems, resulting in complete loss of coral in many cases. For many years, declining water quality has been the principal threat to the ecosystems of the GBR. Beginning in the early 1980s, however, brief periods

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of warmer-than-normal temperatures began to drive mass coral bleaching and mortality events. These events have removed significant amounts of coral from the GBR, and the frequency and intensity of events has increased through the 1990s and 2000s. In 1998, and again in 2002, thermal stress leading to mass coral bleaching affected over 50% of reefs within the Great Barrier Reef Marine Park, removing an estimated 10% of coral populations throughout the Park. Bleaching is just one outcome of thermal stress. There is also strong evidence that unusually warm conditions can affect many other aspects of coral populations, including reducing growth and recruitment. Water temperatures are increasing steadily within the waters of the GBR and Coral Sea. The steady increase in sea temperature is occurring in lockstep with average global temperature and therefore has its roots in anthropogenic climate change. Projections of future sea temperatures reveal severe mass coral bleaching and mortality events on an annual basis by mid century. These projections have led to a reassessment of the key threats to the GBR, with climate change overtaking declining water quality as the most serious threat to the reef’s sustainability. Understanding these threats from human-driven ocean warming and acidification has consequently become an important priority for management agencies such as the Great Barrier Reef Marine Park Authority (GBRMPA).

important findings regarding the biology, oceanography and management of the GBR in a time of rapid environmental change. Together with co-sponsors the Great Barrier Reef Foundation, GBRMPA and a range of other collaborators, our research group was able to make great progress in mapping key threats and investigating potential solutions. As a result, the Fellowship has generated a number of lasting legacies. In the latter case, we have carried out some of the most extensive surveys of coral reefs ever made and established a major global database for information regarding the world’s coral reefs, including the GBR. This document is a summary of the significant research and engagement activities undertaken as part of the fiveyear Queensland Premier’s Fellowship. It details the vast number of people involved in the project and sets out the outcomes as they relate to four areas: Infrastructure Development, Research and Discovery, Research Training and Mentorship, and Communication and Engagement. It provides information on the key outputs, such as the 100+ papers that have been

published and many of the student projects that have been completed during the course of this Fellowship. There is no doubt that these outputs would not have been possible without the salary and resources contributed by the State of Queensland and Fellowship partners including the Great Barrier Reef Foundation and the Great Barrier Reef Marine Park Authority. Naturally, there are many people to thank and an extensive list is given on page 46. However, I would like to single out Dr John Schubert AO (Chair, Great Barrier Reef Foundation) and Dr Russell Reichelt (Chair, GBRMPA) and their respective organisations for providing generous support for this Queensland Premier’s Fellowship, as well as my Global Change Institute colleagues. It is my hope that this Report and the legacies of my Fellowship will provide reef managers, policy makers and decision-makers with the science and solutions to help achieve sustainable management of the Great Barrier Reef in a time of great change.

In 2009, I was fortunate enough to be awarded the Queensland Premier’s Fellowship, which I have used to investigate key aspects of global change and their impacts on the GBR. Drawing on almost 20 years of research experience, I make the case that understanding the resilience of the GBR within the context of ocean warming and acidification greatly affects our ability to manage the reef in perpetuity. As such, a large team of talented academics, PhD students and postdoctoral fellows – headed by myself – set out to discover and communicate

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FELLOWSHIP BACKGROUND “The marine scientists who advise the Foundation convinced me that climate change is the most pressing threat to our Great Barrier Reef.” Dr John Schubert AO (Chair, The Great Barrier Reef Foundation) The Queensland Government established the Premier’s Fellowships to further build ‘leadership capacity within Queensland’s research community and to position Queensland at the forefront of cutting edge research, development and innovation’. The principle objective of the Fellowship program was to entice experienced researchers of national and international prominence to lead Queensland-based research teams. In this particular instance, there were a number of additional national and international contributors, including Fellowship co-sponsors GBRMPA and the Great Barrier Reef Foundation, and numerous collaborators including the National Aeronautics and Space Administration (NASA), the National Oceanic and Atmospheric Administration (NOAA), the Australian Research Council (ARC) Centre of Excellence for Coral Reef Studies and AIMS. The research project was designed to fill scientific knowledge gaps relating to climate change and its potential long-term impacts on the Great Barrier Reef. With access to more comprehensive scientific knowledge, reef managers and decision-makers will be better placed to develop strategies and policies to support reef resilience under a changing climate. This Fellowship was thus a collaborative venture that aimed to connect state, national and international research with management teams and resources to ensure a sustainable future for Queensland through science-based solutions to climate change on the Great Barrier Reef.

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FELLOW ON A MISSION Drawn to the ocean as a child, Professor Ove Hoegh-Guldberg studied marine science at the University of Sydney and later at the University of California, Los Angeles. Fascinated by coral reefs from an early stage, Professor Hoegh-Guldberg has subsequently spent 20 years trying to understand these complex ecosystems, particularly the impact of environmental change. Together with his students and colleagues from the Coral Reef Ecosystems (CRE) Laboratory at The University of Queensland (UQ), Professor Hoegh-Guldberg has pursued a deeper understanding of the impacts of ocean warming and acidification on coral reef ecosystems. His contributions to the field of coral reef science led to him being awarded the Eureka Prize for Scientific Research in 1999, the Queensland Premier’s Fellowship in 2008, and an ARC

Laureate Fellowship in 2013. He was also elected as a Fellow of the Australian Academy of Science in 2013 and since 2005 has served as Deputy Director of the Queensland-based ARC Centre of Excellence in Coral Reef Studies (Coral CoE), which is the largest aggregation of coral reef research and training in the world. The Queensland Premier’s Fellowship has provided an important platform from which to answer some of the crucial questions facing the impact of global climate change on Australia’s Great Barrier Reef. With this support, Professor Hoegh-Guldberg has been able to pursue solutions, collaborate with a broad suite of partners, and communicate the discoveries that he and his team have been making. In addition, he has been able to conceive of and create The University of Queensland’s Global Change Institute (GCI). GCI opened its doors in January 2010 and is firmly focused on


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a ‘solutions’ agenda with respect to the challenges of global change. In this respect, the mission of the Institute focuses on much more than climate change, with research partners across ocean health, clean energy technology, sustainable water and food systems. Professor Hoegh-Guldberg’s work has taken him far and wide. As well as communicating about the impact of climate change on coral reefs, he has served in several important international roles including Chair of the Blue Ribbon Panel of the Global Partnership for Oceans and Coordinating Lead Author on the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (Chapter 30: The Ocean). Professor Hoegh-Guldberg has also continued to develop large-scale collaborations through the World Bank, United Nations and large international corporations. With research collaborations in at least 19 countries, he has been a prominent analyst of what the science is telling us about the risks of ocean warming and acidification, which are critical research themes in a rapidly changing environment. Professor Hoegh-Guldberg strongly believes that solutions can be discovered or applied to ensure a sustainable future for the Great Barrier Reef. This has been a prominent part of the research and outreach activities associated with his role as the Queensland Premier’s Fellow.

THE GREAT BARRIER REEF: THE THREATENED JEWEL WITHIN QUEENSLAND’S CROWN The GBR is a major natural resource and home to a vast number of species. It supports Australia both socially and economically, providing in excess of $6 billion in revenue and 63,000 jobs1. However, the impact of climate change has already begun to affect this exquisite, diverse and important reef system, with at least two long-term studies indicating that coral cover has decreased by 50% since 19802. Large gaps still exist in our knowledge of the status and functioning of reef organisms and systems, and effective management and policy development can only be achieved when those gaps are filled. Queensland is rightfully proud of the Great Barrier Reef, and has the capacity to be at the forefront of efforts to protect and restore this already altered yet still beautiful and highly significant ecosystem.

THE EXTREME TEAM Extreme times call for extraordinary actions and a unique aspect of this Premier’s Fellowship has been the bringing together of talented experts from many sectors of society. This was in recognition of the fact that while solutions to the issues posed to Queensland by climate change may originate in laboratory or field studies, they require further development in a setting where scientists, politicians, industrialists and philanthropists are able to blend their ideas and knowledge to derive sciencebased solutions that have real-world applicability and thus a greater chance of success. In addition to this aspect was the notion that many possible solutions likely already exist but have yet to be applied appropriately. This Fellowship aimed to capitalise on the wealth of expertise and information available in Queensland, and developed a program aimed at rapidly improving our understanding and commitment to the problems facing the world’s largest continuous coral reef ecosystem.

A SUSTAINABLE FUTURE FOR THE GREAT BARRIER REEF Climate change has already had consequences for Australia and is emerging as the key environmental, economic and social challenge of the 21st Century. The GBR faces an uncertain future and the Fellowship Program aimed to broaden our understanding of two of its biggest threats: rising seawater temperature and ocean acidification. Crucially, it also focused on increasing our capacity to respond to those threats, by focusing on five key components: oceanography, biology, eResearch tools, management and communication. This report details the Fellowship outputs, which are the efforts of a broad coalition of many highly dedicated scientists and institutions, led by the Premier’s Fellow. 1

ABARE 2006; Deloitte Access Economics 2013

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Bruno and Selig, 2007; De’ath et al. 2012

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FELLOWSHIP COLLABORATORS “There’s an old African proverb that says, “If you want to go quickly, go alone. If you want to go far, go together.” We have to go far — quickly.” Al Gore (Former Vice President of the United States) Climate change is a highly complex, multidimensional phenomenon,, requiring understanding of several disciplines and across temporal and spatial scales. With the government’s support, the Premier’s Fellow was able to bring together representatives from leading Australian and international universities, institutions and agencies, along with industry experts and philanthropists, to work together with his research team. This connectivity and partnership between the researchers, collaborators, staff and students (listed on page 46) was a critical element in the success of this Fellowship.

AUSTRALIA ADVANCES: AUSTRALIAN SPONSORS AND COLLABORATORS The University of Queensland (host institution and collaborator) is Queensland’s leading university and is in the top 100 universities worldwide. Its status as a global research leader was highlighted by the announcement that 5 UQ academics – including the Premier’s Fellow Professor Ove Hoegh-Guldberg – were among 20 new Australian Academy of Science Fellows for 2013. Scientists from several UQ units, including the School of Biological Sciences and the Advanced Water Management Centre, were involved in projects associated with the Fellowship. www.uq.edu.au The Queensland Government established the Premier’s Fellowships to further build ‘leadership capacity within Queensland’s research community and to position Queensland at the forefront of cutting edge research, development and innovation’. The principle objective of the program was to entice experienced scientists of national and international prominence to lead Queensland-based research teams. www.qld.gov.au/dsitia The Great Barrier Reef Foundation (co-sponsor) was established in 1999 with the goal of encouraging the private sector – with which the Foundation is well connected through its Board, Chairman’s Panel and the ZooX™ Ambassador Program – to fund high priority and strategic research on the GBR. The Great Barrier Reef Foundation was the principal co-sponsor, providing significant financial support to the project. The Fellow’s longstanding and productive relationship with the Great Barrier Reef Foundation flourished further as a result of projects developed during the period of the Premier’s Fellowship. www.barrierreef.org The Great Barrier Reef Marine Park Authority (co-sponsor) has formed many strategic partnerships to fulfil its obligation to protect the Great Barrier Reef Marine Park and World Heritage area. These partnerships helped GBRMPA to ensure human uses of the Park are ecologically sustainable and that issues such as climate change, deteriorating water quality and port development do not lead to a decline in the GBR’s environmental quality. www.gbrmpa.gov.au ARC Centre of Excellence for Coral Reef Studies (collaborator). The Premier’s Fellow is the Deputy Director and coordinator of the UQ node of the ARC Centre of Excellence for Coral Reef Studies, which fosters stronger collaborative links between the major partners and 24 other leading institutions in nine countries, and supports academic and student researchers in the Premier’s Fellow’s research group at UQ. www.coralcoe.org.au World Bank-Global Environment Facility Coral Reef Targeted Research (CRTC) and Capacity Building for Management Project (collaborator). The CRTR program, which the Premier’s Fellow established with partners from the World Bank and the Global Environment Facility, linked 70 laboratories and the Australasian Centre was coordinated at UQ by the Fellow between 2004–2010. www.gefcoral.org The Australia Institute of Marine Science (collaborator) is a world leader in research on tropical marine environments. Since its inception in 1972, AIMS has made research results available to Commonwealth and state governments, industry, non-government organisations, scientific peers and the Australian public to support the protection and sustainable use of the marine environment. www.aims.gov.au The Great Barrier Reef Ocean Observing System (GBROOS) Project (collaborator) is administered by AIMS on behalf of the Australian government, and a consortium of universities and agencies. The project is enabling the collection of data that is helping scientists to understand the impact of changing conditions within the Coral Sea and the GBR. Heron Island, where the Premier’s Fellow pursued many research questions, is a node within GBROOS. http://data.aims.gov.au/gbroos/

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FOCUS ON: COLLABORATION EQUALS EXCELLENCE The ARC Centre of Excellence for Coral Reef Studies represents the world’s largest assembly of coral reef scientists. A partnership between James Cook University (JCU), AIMS, The Australian National University (ANU), GBRMPA, UQ and The University of Western Australia (UWA), the Centre fosters collaborative links with a further 24 institutions in nine countries. With strong links to programs such as the Global Coral Reef Targeted Research Program, funded by the World Bank, the Census of Marine Life project and coral reef management agencies such as GBRMPA, the Centre of Excellence takes a leading role in multinational research and management initiatives. In existence since 2005 and under the guidance of Director Professor Terry Hughes (JCU) and Deputy Directors Professors Ove Hoegh-Guldberg (UQ) and Malcolm McCulloch (UWA), the Centre of Excellence entered its next phase in 2014, with funding secured until 2021. It will continue to focus on research programs to fulfil its commitment to undertake research that will lead to the sustainable use and management of coral reefs.

AUSTRALIA SHINES UNDER THE METRICS SPOTLIGHT Thomson Reuters is the world leader in the provision of science metrics and research performance analysis. As part of its mission on track ‘the world’s most significant scientific and scholarly literature’, its open web resource ScienceWatch published a Research Fronts report for the first time in 2013. The aim of the report was to identify the papers, authors and institutions that serve as the foundational ‘core’ of research fronts (areas of current interest and intensive investigation, with foundation papers dating from 2007-2012). The research fronts were presented as key fields to watch in 2013, particularly in terms of strategic investment. For Ecology and Environmental Science, the report ranks ocean acidification and marine ecosystems as the top research front and devotes a whole page to Australia’s leadership role: 9 of the 45 core papers in this research front were produced by Australians, with the top two authored by the Premier’s Fellow, Professor Ove Hoegh-Guldberg. The report also states that ‘it is plain that ecology and environmental sciences is a focus area for the nation and, in particular, ocean acidification, marine habitats, and specifically coral reef studies are domains in which Australia plays a global leadership role.’ It cites the existence of the ARC Centre of Excellence for Coral Reef Studies as an explanation for the nation’s research impact and shows that Australia has truly grown into a global leader in this field in recent years.

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THE WIDER WORLD: BRINGING INTERNATIONAL EXPERTISE TO QUEENSLAND

THE CORAL REEF ECOSYSTEMS LABORATORY AT UQ

The Premier’s Fellowship research program benefited from significant partnerships with two international collaborators – NASA and NOAA:

More than 20 PhD, Masters and Honours students from over a dozen countries carried out studies as part of the Queensland Premier’s Fellowship research program in the Coral Reef Ecosystems Laboratory at The University of Queensland between 2009 and 2013. They worked on a wide variety of projects, many of which were multidisciplinary and interlinked, and focused on field sites across the length and breadth of the GBR. Students also receive guidance from CRE Laboratory Director and collaborator Associate Professor Sophie Dove, senior research staff Dr Ken Anthony, Dr Simon Dunn, Dr Selina Ward and Dr Scarla Weeks, and postdoctoral researchers Dr Olga Pantos, Dr Guillermo Diaz-Pulido, Dr Mathieu Pernice, Dr Nela Rosic, Dr Davey Kline, Dr Linda Tonk and Dr Manuel Gonzalez-Rivero. PhD students Pim Bongaerts and Paulina Kaniewska remained at UQ to carry out postdoctoral research relating to the Premier’s Fellowship program. The laboratory was managed by Maya Carmi and Annemieke Van Den Heuvel together with Project Officers Lianne Cook and Hayley Ware, who oversaw the logistical, safety and operational issues relating to the Premier’s Fellowship Project. Research assistants Giovanni Bernal Carrillo and Aaron Chai were instrumental in maintaining the mesocosm system at Heron Island Research Station (HIRS). Occupational Trainee Matheus A. Mello Athayde and software engineer Clinton Roy also formed part of the Fellowship team. Details of the research activities are outlined in the Research and Discovery and Research Training and Mentorship sections of this report.

• Since its inception in 1958, NASA has maintained a robust program of scientific research alongside its exploration and technology development goals. Collaboration with members of the Ocean Biology Processing Group was hugely important to the satellite oceanography component of the fellowship. www.nasa.gov • NOAA is a leading monitoring and management agency for the United States of America (USA). Coral Reef Watch, and the Satellite Oceanography and Climatology Division (SOCD) are key departments within the organisation, and extensive linkages were made between the Premier’s Fellowship team and staff within these departments. http://coralreefwatch.noaa.gov/ Collaboration with expert researchers from other international institutions such as Stanford University, the Scripps Institution of Oceanography, Monterey Bay Aquarium Research Institute, Pennsylvania State University, the University of North Carolina, the University of Louisiana (all USA) and the Institut de Ciències del Mar (Spain) also proved invaluable to many aspects of the Fellowship. These are detailed fully in the Fellowship Outcomes section of this report.

Senior CRE Researchers involved in the Premier’s Fellowship research program: • Laboratory Director Associate Professor Sophie Dove’s research focuses are primarily coral photobiology and ocean acidification, and she coordinated the establishment of the mesocosm system at HIRS. More details of Assoc. Professor Dove’s research are given on page 9.

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• Dr Scarla Weeks established herself as a leading satellite oceanographer in her native South Africa and was part of the CRE Laboratory from 2005–2011. Dr Weeks’ research is featured in more detail on page 33. • Dr Ken Anthony is a coral reef ecologist who worked within the CRE team on projects relating to biological responses to climate change (including ocean acidification) in coastal Queensland until 2011, when he took up a position at AIMS, where he leads the Healthy and Resilient Great Barrier Reef team.

Visitors to the CRE Laboratory and participants in workshops associated with the Fellowship: Eva Abal (Great Barrier Reef Foundation) Rebecca Albright (AIMS) Matar Hamed Hlais Al Neyadi (Directorate for Energy and Climate Change of the United Arab Emirates) Mark Baird (Commonwealth Scientific and Industrial Research Organisation (CSIRO)) Simon Beckett (GE Capital) Roger Beeden (GBRMPA) Ray Berkelmans (AIMS) John Bruno (University of North Carolina) Tim Burgess (NOAA Coral Reef Watch) Maria Byrne (University of Sydney) Jeremy K. Caves (Stanford University/ANU) Billy Causey (NOAA Office of National Marine Sanctuaries) Chaolun Allen Chen (Biodiversity Research Centre at the Academia Sinica Taipei)

• Dr Selina Ward was part of the CRE Laboratory and worked on the impacts of ocean warming and acidification on coral reproduction. Dr Ward continues to carry out research in this area in her role as a lecturer in the School of Biological Sciences at UQ.

Tyler Christensen (NOAA Coral Reef Watch)

• Dr Simon Dunn has studied the molecular and cellular interactions associated with the onset, maintenance and breakdown of cnidarian-dinoflagellate symbiosis in the United Kingdom and the USA, and he continues with this research program in the CRE Laboratory.

Peter Fearns (Curtin University of Technology)

• UQ ARC Professorial Fellow Professor Jane Hunter is an internationally recognised computer scientist who is well regarded for her work on middleware, knowledge management and mining of large-scale mixed-media and data collections within the scientific, educational and cultural sectors. She coordinated all aspects of the Great Barrier ReefClimate Analysis Tool (GBR-CAT) project. Professor Hunter leads the eResearch Group within the School of Information Technology and Electrical Engineering at UQ. The CRE Laboratory hosted a number of international visitors during the period of the Premier’s Fellowship, and nearly 60 senior executives and academics from Australia and overseas participated in workshops associated with the Premier’s Fellowship. A full list of visitors can be found on the following page.

Vic Ciesielski (Royal Melbourne Institute of Technology) Cath Collier (JCU) Sean D. Connell (University of Adelaide) Arnold Dekker (CSIRO) Mark Eakin (NOAA Coral Reef Watch) Susana Enriquez Dominguez (Universidad Nacional Autónoma de México) Katharina Fabricius (AIMS) Kevin Gale (Department of Sustainability, Environment, Water, Population and Communities) Kent Headley (Monterey Bay Aquarium Research Institute) Scott Heron (NOAA Coral Reef Watch) Roberto Iglesias-Prieto (Universidad Nacional Autónoma de México) Asep Karsidi (Indonesian Deputy Coordinating Minister for People’s Welfare) Ryan Kelly (Stanford University) Randall Kosaki (NOAA Papahānaumokuākea Marine National Monument) Oren Levy (Bar Ilan University) Gang Liu (NOAA Coral Reef Watch) Janice Lough (AIMS) Sue Meek (AIMS) Kelvin Michael (University of Tasmania) Mathieu Mongin (CSIRO) Jessica Morgan (NOAA Coral Reef Conservation Program) Phil Munday (JCU) Merinda Nash (ANU) Carl Nim (NOAA Coral Reef Watch) Jamie Oliver (AIMS) Brad Opdyke (ANU) Britt Parker (NOAA Coral Reef Conservation Program) Rachel Pears (GBRMPA) Mauricio Rodriguez-Lanetty (Florida International University) Bayden D. Russell (University of Adelaide) Kenneth Schneider (Carnegie Institution) William Skirving (NOAA Coral Reef Watch) Claire Spillman (Australian Bureau of Meteorology) Craig Steinberg (AIMS) Al Strong (NOAA Coral Reef Watch) Hugh Sweatman (AIMS) Lida Teneva (Stanford University) Bronte Tilbrook (CSIRO) Matthew Valetich (ANU) Greg Vero (Orica)

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FOCUS ON: PIGMENTS, PHOTONS AND pH: ASSOCIATE PROFESSOR SOPHIE DOVE Coral Reef Ecosystems Laboratory Director and ARC Chief Investigator Associate Professor Sophie Dove holds a clutch of tertiary qualifications in mathematics, philosophy and biology. Her diverse publication record includes studies of fish otoliths, coral pigments, photobiology and Symbiodinium genetics, resulting in high-impact papers in journals such as Global Change Biology and Proceedings of the National Academy of Sciences of the United States of America. During the period of the Premier’s Fellowship, she has been able to apply her particular expertise to studying the capacity of acidified oceans to shape the future of coral reefs, being the lead researcher in the Premier’s Fellowship team that established the mesocosm system at Heron Island Research Station. In May 2013, Associate Professor Dove and the Fellowship’s mesocosm study featured in an article by a visiting journalist from the USA’s National Public Radio, which is available at: www.npr.org/blogs/thetwo-way/2013/03/07/173702462/australias-heron-islanda-canary-in-the-coal-mine-for-coral-reefs

A member of the Premier’s Fellowship team, Associate Professor Dove has been part of three successful ARC Linkage program applications since 2009 and in 2013 secured funding to further investigate the effects of climate change on Great Barrier Reef coral health.

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FELLOWSHIP OUTCOMES “Far and away the greatest threat to the ocean and to the future of mankind is ignorance.” Sylvia Earle (National Geographic Explorer-in-Residence) The Premier’s Fellowship program was structured in a way that would allow many key issues to be addressed via strategic partnerships. These were grouped within the original application into five broad areas: eResearch tools, biology, oceanography, management and communication. The research program and its outputs are outlined in the following sections of this report. For ease of understanding, these achievements have been arranged into four categories: • Infrastructure Development (incorporating eResearch and the experimental systems relevant to biology and oceanography). • Research and Discovery (incorporating biology and oceanography). • R esearch Training and Mentorship (reflecting knowledge transfer and career development within the Fellow’s research team). • Communication and Engagement (incorporating management and communication, with a further focus on publications). As one of the major aims of this Fellowship was to provide science and solutions to help manage the Great Barrier Reef into the future, each category includes break-out boxes entitled ‘Management Matters’, which highlight how the Fellowship science can help to inform reef policy and management.

MANAGEMENT MATTERS How will the science of the Premier’s Fellowship research program help decision-makers manage the reef? The short answer is: in lots of ways. For example: • The Great Barrier Reef is under increasing pressure from a range of human and environmental impacts, including climate change. Therefore the science is critical to provide evidence of the health and resilience of the GBR ecosystem in order to manage the increasing and competing uses of the GBR • Knowledge, understanding and solutions generated through science can help reef managers, policy makers and decision-makers manage the GBR in a time of great change. You can’t manage what you don’t understand • Specifically, innovative and cutting-edge research carried out at kilometre scales across the reef can provide insight and a baseline of contemporary changes in reef health, which are critical in managing reef resilience and use • This science will also provide managers with the tools and understanding necessary to manage the multitude of issues impacting the Marine Park. This in turn gives managers the confidence and credibility to manage key resources such as coral reefs

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KEY OUTCOME AREA 1: INFRASTRUCTURE DEVELOPMENT w From microscopes to satellites, SCUBA to remotely operated vehicles (ROVs), exploration of the sea has depended on the breakthroughs of early pioneers such as Jacques Cousteau. Further development of technology is rapidly assisting our ability to understand the impact of climate change on reef systems. Several state-of-the-art experimental systems and information technology (eResearch) tools have been developed or applied as part of the Premier’s Fellowship research program. From algorithms and databases to carbon-dosing flumes and deep-water robots, this new infrastructure has enabled significant advances in our understanding of the impacts of climate change on organisms and ecosystems. All relevant project milestones were met, and further discoveries and publications have already resulted due to ongoing research using this established infrastructure. The development and expansion of infrastructure is a lasting legacy of the Queensland Premier’s Fellowship, with infrastructure developed during the Fellowship now being used to underpin other research activity.

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eResearch highlights: • The GBR-CAT, a web-based tool for the integration of complex datasets, was developed to systematically store information flowing from ecological projects associated with the research and the Fellowship co-sponsor the Great Barrier Reef Foundation. This was ultimately incorporated into the next generation of the tool, eReefs. www.ereefs.org.au • Keeping track of the genetic identity of the all-important dinoflagellate symbionts associated with coral species, as well as the oceanographic environment in which they were found, is crucial. An online database was developed and is available to scientists around the world through the website. www.symbioGBR.org • Fellowship research data was contributed to the e-Atlas, an environmental research data repository and mapping tool supported through funding from the Australian Government’s National Environmental Research Program and AIMS. www.e-atlas.org.au • The Fellow attracted funding for the Catlin Global Reef Record, an initiative for which he is the Chief Scientist (2012-present). This research tool will eventually store the hundreds of thousands of images and research data sets arising from the science of the Catlin Seaview Survey. This data bank of information will be freely available to everyone and includes research data from coral reefs in 19 countries. Discussions are currently underway with several leading science agencies around plans to extend this facility to support the development of reef management policy.


FOCUS ON: SymbioGBR: SHARING CRUCIAL INFORMATION ON A PARTNERSHIP UNDER THREAT The algal endosymbionts (genus Symbiodinium) associated with scleractinian corals (and other reef invertebrates) have received a lot of research attention in the past decade, particularly as certain host-symbiont associations appear to be more affected by increasing seawater temperatures than others. Research led by Dr Linda Tonk within the Premier’s Fellow’s research group developed a web-based application that allows for easier knowledge transfer and more effective research efforts regarding the genetics of these crucial reef partnerships, which face increasing stress due to climate change. This information will be important in terms of tracking potential changes in symbiont types as conditions alter on the Great Barrier Reef. With the rapid accumulation of information on the diversity of Symbiodinium, it is becoming increasingly difficult to compare newly acquired Symbiodinium data with existing data to detect patterns of host-symbiont specificity on broader spatial scales. The lack of a general consensus on the classification of Symbiodinium species, coupled with the variety of different markers used to identify the genus Symbiodinium (ITS1, ITS2, LSU D1/D2, chloroplast 23S rDNA and psbA minicircle), further complicates direct comparison. The SymbioGBR database compiles all currently available Symbiodinium sequences and associated host information of data collected from the Great Barrier Reef into a single relational database that is accessible via a userfriendly, searchable web-based application. SymbioGBR allows users to query Symbiodinium types or sequences sourced from various genetic markers (e.g., ITS1, ITS2, LSU D1/D2 and chloroplast 23S) and invertebrate host species to explore their reported associations. In addition, as the database includes sequence information of multiple genetic markers, it allows crossreferencing between conventional (e.g., ITS2 region) and novel markers that exhibit low intragenomic variability (e.g., psbA region). Finally, the database is based on the collection details of individual specimens. Such host-symbiont associations can be assessed quantitatively and viewed in relation to their environmental and geographic context. By providing a comprehensive overview of Symbiodinium diversity and hostassociations on the Great Barrier Reef, the SymbioGBR database represents a vital resource for researchers. It provides a quick, user-friendly means to compare newly-acquired data on Symbiodinium (e.g., raw sequences or characterised Symbiodinium types) with previous data on the diversity of invertebrate host-symbiont associations on the GBR. The inclusion of psbAncr sequence information allows for validation of widely used ITS1/ITS2 markers and their ability to accurately identify relevant sequences. Most importantly, centralisation of sequence information from multiple genetic markers will aid the classification of Symbiodinium species diversity and allow researchers to easily compare patterns of host-Symbiodinium associations.

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EXPERIMENTAL SYSTEMS HIGHLIGHTS • Design and construction of the world’s first Coral-Proto Free Ocean Carbon Enrichment (CP-FOCE) system (at Heron Island Research Station) in collaboration with a large international team shows that ocean acidification has a number of key impacts on community-scale processes, including calcification. The system is described by Kline et al. (2012). • A computer controlled mesocosm system was established on Heron Island and is one of the most sophisticated experimental systems being used internationally to understand the effects of ocean warming and acidification on coral reefs on the Great Barrier Reef. Experiments undertaken as part of the Premier’s Fellowship revealed potentially devastating impacts on coral communities exposed to the conditions from the Intergovernmental Panel on Climate Change (IPCC) B1 (RCP4.5) and A1FI (RCP 8,5) scenarios. This has been communicated to decision-makers at both State and Federal levels, as well as featuring in the latest Intergovernmental Panel on Climate Change report. Further details of the system can be found in the Proceedings of the National Academy of Sciences of the United States of America. • A revolutionary high definition 360° camera was used by the Catlin Seaview Survey team to investigate coral reefs across the Great Barrier Reef in 2012; a collaborative global project carried out by a partnership between the Global Change Institute, Underwater Earth, Catlin Group Ltd and Google. The completed survey is the most extensive of the Great Barrier Reef in history, giving important insights into the health of coral dominated habitats on the GBR at regional scales. www.catlinseaviewsurvey.com • As part of the Catlin Seaview Survey, two deep-water ROVs were purchased. This infrastructure is gleaning important details of the deep-water habitats of the Great Barrier Reef and is revealing information on potential refugia at depth for corals exposed to rapid changes in condition in shallow sections of the reef. www.youtube.com/playlist?list=PL59ceiDuWHtsSfogGHZwvlsPDVh9WLVYU

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MANAGEMENT MATTERS How will the science of the Premier’s Fellowship research program help decision-makers manage the reef? • The extensive monitoring of coral reefs by the Catlin Seaview Survey team is establishing new technologies in order to build a baseline reference database in order to understand how reef health is changing • This near real-time information is being made available to coral reef managers and decisionmakers through the freeaccess database the Global Reef Record http://globalreefrecord.org/ home_scientific • The importance of the database can already be seen: recent surveys have been able to make comparisons with the existing information, and rapidly establish how cyclones and bleaching events are affecting specific reef areas


FOCUS ON: ACIDIFICATION: THE GREATEST THREAT? In a 2010 BBC documentary, Sir David Attenborough declared that he believed ocean acidification, which poses challenges to organisms from the molecular through to the ecosystem level, to be the greatest threat to our oceans. The program featured one of the major success stories of the Premier’s Fellow’s research efforts, a seawater carbonmanipulation system named the Coral-Proto Free Ocean Carbon Enrichment system. Postdoctoral fellow Dr Davey Kline worked with the Fellow and a multidisciplinary international team from The University of Queensland’s Instrumentation Laboratory, Stanford University, the Carnegie Institution for Science, Monterey Bay Aquarium Research Institute, Australian National University, the University of Adelaide, Israel Oceanographic and Limnological Research Ltd, Scripps Institution of Oceanography and UQ’s Coral Reef Ecosystems Laboratory to conceive, construct and deploy the CP-FOCE system. Part of the Heron Island Climate Change Observatory and funded by an ARC-Linkage supported by funds from the Great Barrier Reef Foundation, as well as an Infrastructure, Equipment and Facilities (LIEF) Grant, it was used to assess the effects of ocean acidification on coral reef communities at Heron Island3. Levels of atmospheric carbon dioxide (CO2) have risen dramatically since the start of the Industrial Revolution and they continue to rise in the present day. The tight coupling between the atmosphere and oceans means that oceanic

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water has absorbed over one third of this CO2, resulting in a decline in ocean pH. This phenomenon is termed ocean acidification (OA) and on coral reefs the destructive effects of OA are most strikingly seen in the calcifying organisms, including corals themselves, crustose coralline algae, foraminifera and molluscs. For coral reefs, a reduction in the calcification rate as a result of OA is likely to influence the delicate balance between growth and erosion, which may lead to loss of reef structure. Laboratory experiments and studies of natural systems with high CO2 levels have been sufficient to establish these major points. However, gaining a deeper understanding of the highly variable effects of OA and the potentially synergistic effects of other environmental variables required keeping organisms in as natural a reef setting as possible and artificially manipulating pH levels to mimic conditions that are predicted to occur in the next century. The CP-FOCE system takes its basic design from the Monterey Bay Aquarium Institute’s original FOCE system, but was modified to monitor the effects of changing pH on coral reef communities in as natural a setting as possible. In monitoring the corals over a longer time period, it was hoped the project would establish how corals and associated organisms respond to OA as a chronic stress. The CP-FOCE uses replica experimental flumes to enclose sections of the reef and dose them with CO2-enriched seawater. A network of sensors and computers monitors conditions within flumes and maintains experimental pH as an offset from environmental pH using feedback control on the injection of low pH seawater. In the four-

month experiment at HIRS, three key ecological elements of the reef flat community were considered: corals (Acropora millepora), crustose coralline algae (CCA; Porolithon onkodes) and reef sediments. Being kept in situ, rather than in a tank or mesocosm system, the organisms were not isolated from local hydrodynamics, controls on food energetics, disturbed microbial populations, lack of sediment and associated animal communities. Continued experimentation over longer time-scales will allow for better determination of the contributions of reef-driven metabolism and tidal dynamics to the trends in the carbon system parameters, but with the data obtained it was possible to see that the carbonate chemistry conditions maintained in -0.06 and -0.22 pH offset treatments were significantly different to, and closely tracked, ambient environmental conditions. Although the data are only preliminary, the study also made potentially significant discoveries regarding the mineralogy and dissolution rates of CCAs that make it necessary to reconsider the applicability of the parameter ΩMg-calcite for predicting impacts of OA on CCAs. The CP-FOCE represents an important experimental platform for the study of the complex, interactive impacts of OA on coral reef communities. Further experiments over longer time periods are needed to clarify the findings of this initial investigation and to elucidate the relative vulnerability or resilience of various reef sub-environments to OA. The same experimental approach could also be applied to gain insight into species-to-ecosystem scale biological impacts of OA in other marine environments.

Walz et al. (2008); Barry et al. (2010)

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FOCUS ON: MESOCOSMS: SEEING THE FUTURE A mesocosm is a controlled, flow-through, experimental system that allows researchers to simulate much of the complexity of a natural environment and to test notions of future environmental change. It represents the mid-way point between an in situ field situation, where replication is hard to achieve, and the artificial conditions of a laboratory experiment, where organisms may not react to stressors in a realistic way. The Premier’s Fellow and his colleague Associate Professor Sophie Dove from the Coral Reef Ecosystems Laboratory at UQ, developed and coordinated construction of one of the most advanced mesocosm systems for studying the response of coral reefs to ocean warming and acidification at the Heron Island Research Station as part of the Premier’s Fellowship (www.coralreefecosystems.org). The system was set up to explore how the various temperature and acidification scenarios proposed for the end of this century will affect the balance between reef accretion and erosion. The system is unmatched worldwide in terms of facilities that can simulate past and future ocean conditions; by allowing the manipulation of water temperature as well as carbon dioxide it therefore makes it possible to recreate the different climate scenarios predicted by the IPCC to be reached in 100 years’ time. In addition to setting conditions, the system is able to incorporate realistic hourly, daily and seasonal variability, which turns out to be extremely important in terms of interpreting the results of exposing coral reefs to future scenarios (Dove et al. 2013).

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Above: Research Assistant Aaron Chai was involved in maintaining the

Each one of the 12 mesocosms consists of a large seawater tank containing a community of fore-reef organisms such as corals, anemones, algae, crustaceans and fish, as well as their associated microbes and carbonate sediments. With several such tanks in place, the necessary replication of treatment and control conditions can be achieved; long-term experiments allow for consideration of the crucial factor of seasonal variability. The results of the first study using the mesocosm system to determine the responses of intact coral reef assemblages from rapidly warming and acidifying oceans were recently published in the Proceedings of the National Academy of Sciences of the USA and our understanding of how reef systems have, and will continue, to change under high and low scenarios of ocean warming and acidification has been substantially increased. The study showed that there has been little adaptation of corals over the past 100 years and that the IPCC B2 (450 ppm, +2oC; RCP 4.5) and A1FI (800 ppm, +4oC, RCP 8.5) scenarios will have potentially devastating impacts on coral communities. It was also found that community-level processes reacted differently to the different treatments, with community metabolism and photosynthesis being similar (despite the organisms involved changing dramatically, shifting from being a coral-dominated to a cyanobacteria-dominated system), and community calcification rates dropping to the point that reefs were dissolving by the end of the experiment under the highest greenhouse gas scenario.

Above: Composite images from the first mesocosm experiment, contrasting a healthy coral reef (left; control) with one affected by temperature and CO2 concentration expected mid-to-late century (right; treatment: 800 ppm and


A second, longer experiment is currently underway and at completion in 2014 will give a time-series of data for almost two years. The project has attracted considerable attention and has been used in a number of documentaries. Outreach around this experiment is particularly important, given what it reveals about how the current trajectories of CO2 concentration will affect the Great Barrier Reef. In this respect, the system has attracted visits from leading politicians and corporations. Fellowship postdoctoral researcher Dr Manuel Gonzalez-Rivero from Venezuela has also been using the mesocosm system to investigate the impacts of climate change and ocean acidification on a non-coral invertebrate, the sponge Cliona orientalis. Dr Gonzalez-Rivero’s study of reproductive and phenological plasticity (i.e., variation in timing of recurring natural phenomena in relation to climate change) is currently being prepared for publication. In May 2013, CO2 levels in the atmosphere passed a symbolic mark: at NOAA’s Mauna Loa Observatory in Hawaii, the average daily level of CO2 measured 400 ppm for the first time since records began in 19584. The implications of this milestone are severe, further highlighting the urgent need for research on the potential impacts of OA on the ocean. The HIRS mesocosm system represents a powerful tool for such studies and is therefore a highly important legacy of this Premier’s Fellowship.

MANAGEMENT MATTERS How will the science of the Premier’s Fellowship research program help decision-makers manage the reef? • These meaningful measurements allow for notions of future environmental change to be tested in real time and on-reef with the results being available to reef managers • This fundamental science is crucial to mitigating the impacts of environmental change and represents critical information for adaptively manage the GBR

COLOURS, CAMERAS …. ACTION! The Catlin Seaview Survey showcases an extensive and technologically advanced suite of technologies commissioned specifically for use on this project, which commenced in 2012 with funding from Catlin Group Ltd, the Queensland Premier’s Fellowship, the Global Change Institute at The University of Queensland, Google and Underwater Earth. An array of cameras, computers and robots are fundamental to the success of the project, which aims to record and reveal the oceans at a scale never before seen. Among the suite of technologies employed by the team is an underwater tablet that allows for connection to the internet and live communications from under the water, and which is linked with the project’s custom-designed camera, named ‘the SVII’. Images are posted online (www.catlinseaviewsurvey.com and www.globalreefrecord.org) so that anyone with access to a desktop, laptop, tablet or smartphone can take part in a high-resolution ‘virtual dive’. For each image captured, the location and camera direction is also recorded, which means that the photograph can be retaken at a later date from exactly the same position. In this way, changes to reef condition can be monitored over time. A number of modifications were 4.

made to the original camera, making the SVII more user-friendly and these changes have halved the time needed to complete each survey, meaning more reef can be recorded with each deployment. The Catlin Seaview Survey team also uses Remotely Operated Vehicles, which have been used to explore the mesophotic zone (between 30–100 m) of the GBR and Coral Sea. This difficult to access zone has been especially important to explore, particularly given the potential for the mesophotic zone of the Great Barrier Reef to provide refuge against the effects climate change. Each ROV carries a variety of scientific equipment that can be tailored to the

particular task of any mission. It is also fitted with a custom-made remotelycontrolled DSLR system to record high-definition wide-angle video and a geo-positioning system to capture accurate underwater locations, as well as instruments for depth, temperature, heading, tilt and altitude sensors. While SCUBA divers are generally restricted to less than 40 m depth, ROVs have relatively few dive constraints and can document vast areas of coral reefs at depths greater than normal SCUBAdiving (down to 150 m in this case). The use of these instruments has very much expanded the horizons of the Premier’s Fellow’s research program.

http://www.esrl.noaa.gov/gmd/news/7074.html

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MANAGEMENT MATTERS How will the science of the Premier’s Fellowship research program help decision-makers manage the reef? • New satellite tools are giving managers greater information about changes in environmental conditions (e.g., temperature, sediments) and hence risks to the GBR • This high level information is helping develop early warning systems and is informing management on emerging issues associated with the health of the GBR • Using new and innovative research methods the Catlin Seaview Survey can realise large-scale and affordable monitoring to provide real-time information to reef managers on the status of the GBR • This baseline information is critical to reef managers and decision-makers given that you can’t manage what you can’t measure.

A publication currently in preparation by team member and Fellowship postdoctoral scientist Dr Manuel Gonzalez-Rivero considers integrating the novel approaches with data generated by the Catlin Seaview Survey to study coral reef complexity and heterogeneity. This physical complexity, or rugosity, supports a high diversity of life and ecological processes, but measuring and accurately representing reef complexity presents challenges because existing methods are labour-intensive and scale-dependent. Dr Gonzalez-Rivero and the Catlin Seaview Survey team have hybridised existing protocols from the computer vision field of research and adapted these to use coral reef imagery from the Catlin Seaview Survey for reconstructing their tridimensional complexity at multiple spatial scales. This novel application of existing methods can be used to produce 3D reconstructions and compute rugosity measures of reefs at metre-to-kilometre scales. The satellite oceanography group, led by Dr Scarla Weeks (page 33), developed and applied a suite of tools during the Fellowship period, with the aim of generating crucial data for understanding links between oceanographic processes, water quality and biological responses at spatial and temporal scales relevant to the study of climate change impacts on ecosystem health and management. The tools included implementation of an operational algorithm for processing satellite imagery to map water clarity and optical properties of coral reef waters. This particular project resulted in a successful ARC Linkage Grant. The ARC Linkage project has since undertaken five field trips to acquire simultaneous substrate cover and in-water optical properties data. It has produced the first satellite-derived, GBR-wide map of water optical properties that includes corrections for the effect of bottom (benthic) reflectance in shallow waters. Ultimately, the algorithm will be fully integrated into NASA’s widely used, publicly-available software package SeaDAS, used for the processing, display, analysis and quality control of ocean colour data sets from current and near-future satellite ocean colour sensors (see Focus On: Ocean colour and large-scale oceanography of the GBR). The predictive capability of the satellite oceanography group was highly important to other members of the CRE Laboratory, driving the activities of team members who were focused on the impacts of thermal stress on coral reefs.

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HIGHLIGHTS Between 2009 and 2011, a near-monthly report of ocean environmental conditions was compiled by Premier’s Fellowship PhD student Ana Redondo-Rodriguez and provided to GBRMPA, the Reef and Rainforest Research Centre (RRRC) and other interested parties, as well as being made publicly available through the CRE website. This initiative has continued to be supported by UQ’s Biophysical Oceanography Group since Dr Redondo-Rodriguez completed her studies with that group. The reports, which include NASA satellite data processed and analysed by the UQ Biophysical Oceanography Group, Integrated Marine Observing System and GBROOS information sources, together with insights from NASA and NOAA, provide critical information for researchers and decision-makers across the GBR and can be found at www.gpem.uq.edu.au

Left: Representative image from an OceanSpace report, showing sea surface temperature (SST) in the Southern GBR region in February 2011. These near-monthly reports indicated anomalies and other features of importance to scientists

The satellite oceanography team, within the Premier’s Fellowship project, developed a strong working collaboration with NASA’s Ocean Biology Processing Group in developing the application of satellite ocean colour and thermal data to coral reef and coastal ecosystems, with a focus on the Moderate Resolution Imaging Spectroradiometer (MODIS). The group also developed collaborations with Dr Mark Eakin and other staff at the Centre for Satellite Applications and Research (STAR) within the Satellite Oceanography and Climatology Division (SOCD) at NOAA. A joint workshop (coordinated and led by the Premier’s Fellow) on climate impacts on coral reefs was held with NASA and NOAA in February 2010, with over 40 Australian and US researchers participating in a round-table discussion of recent research developments and the structure of the Queensland Premier’s Fellowship research program with respect to NOAA’s involvement. Left: MODIS long-term (2002–2012) monthly mean Secchi depth (m) on the central-southern Great Barrier Reef showing waters most turbid (a) during March and most transparent (b) during September. The solid black line denotes the 200 m isobath. The large white arrow represents the southward flow of the East Australian Current, with smaller white arrows showing the directions of oceanic intrusions onto the shelf. The circular arrows show the location of the Capricorn Eddy (E) that forms in the lee of the shelf bathymetry. (From

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KEY OUTCOME AREA 2: RESEARCH AND DISCOVERY

Climate change is a complex multidimensional phenomenon that requires understanding of several disciplines at a range of temporal and spatial scales. Therefore, from assessment of deep reef environments to the temperature of surface seawater, and the factors affecting single-celled microalgae to the habitat choices of manta rays, the scope of the Premier’s Fellowship research program has been necessarily vast. Some of the results have been groundbreaking. To advance our understanding of the effects of rising seawater temperature and ocean acidification on the biology and oceanography of the region, studies were conducted across the length, breadth and depth of the GBR, including at uninhabited remote cays and at the four reef-based research stations (on Heron, Lizard, One Tree and Orpheus Islands). The Coral Reef Ecosystems group, in collaboration with experts from UQ, the ARC Coral COE, AIMS, NOAA, NASA, Stanford University and several other state, federal and international institutions conducted research that resulted in over 100 peer-reviewed publications. The Premier’s Fellow was able to use many of these findings to inform a number of further key publications projecting the likely future state of the Great Barrier Reef.

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BIOLOGY HIGHLIGHTS • A major leap in our understanding of the factors determining the thermal tolerance of corals, as a result of an extensive collection and screening program of GBR corals and their symbionts. • Substantial progress in unravelling the role of deep reefs as refugia for corals. • Discovering that coralline algae, which are critical components of the coral reef structure, are highly sensitive to the combined effects of ocean acidification and warming. • Using satellite oceanography to explore the links between sea surface temperature and biological processes, and showing that, for example, the presence of upwelling and occurrence of thermal events are linked to the foraging behaviour of seabirds. • The Fellow writing and leading the authorship of the first regional chapter on the Ocean for the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (http://ipcc-wg2.gov/AR5/), as well as contributing to key cross IPCC consensus chapters on a poleward migration of marine organisms, ocean acidification, and heat stress in response to warming and acidifying oceans. These consensus chapters have been read by thousands of other scientists, ecosystem managers and policy makers worldwide.

OCEANOGRAPHY HIGHLIGHTS • Discovering that upwelling activity can be used to forecast possible thermal anomalies that may result in coral bleaching events on the GBR. • Applying satellite tools to determine environmental factors affecting a range of coral reef organisms, from microscopic algae to seabirds and manta rays. • Using satellite tools to analyse changes in sea surface temperature on the GBR and relating them to the conservation objectives of GBRMPA. • Relating climate variability on the GBR to the El Niño-Southern Oscillation (ENSO) through application of new analytical tools and variables, and finding that there is a large amount of variation in responses to ENSO between the northern and southern portions of the GBR. • Production of a near-monthly report of environmental variables for the GBR.

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PROJECTIONS OF THE FUTURE OF THE GREAT BARRIER REEF • Completing a comprehensive global study of coral bleaching events, which concluded that coral reefs may not survive a 2°C rise in the average global temperature (Frieler et al. 2012). • Publishing a quantitative analysis of how different combinations of CO2 and fishing pressure on herbivores affect the ecological resilience of benthic reef communities (Anthony et al. 2011). • Reviewing the impacts of anthropogenic climate change on marine ecosystems, revealing that the majority are changing rapidly with an increased risk of sudden nonlinear transformations (Hoegh-Guldberg and Bruno 2010). • Publishing a paper that explores recent advances in understanding of ocean acidification, with a particular emphasis on past changes to ocean chemistry and what they can tell us about present and future changes (Calvo et al. 2010). • Collectively, the four papers outlined above have already been cited 271 times (Web of Science, January 2014), indicating the high impact of these studies.

MANAGEMENT MATTERS How will the science of the Premier’s Fellowship research program help decision-makers manage the reef? • The research and discovery unveiled by this program has advanced our understanding of the biology and oceanography of the GBR region • This research and discovery is critical to meeting the conservation objectives of the GBR and provides reef managers with an evidencebase upon which to make decisions concerning the likely future state and management of the GBR • New tools and analysis have also been applied to the GBR to strengthen our understanding, enabling proactive responses to emergent challenges

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THE CORAL REEF ECOSYSTEMS LABORATORY: FELLOWSHIP RESEARCH HUB The Coral Reef Ecosystems Laboratory at The University of Queensland is the research laboratory of Professor Ove Hoegh-Guldberg and Associate Professor Sophie Dove. Together, their group forms an important node within the ARC Centre of Excellence for Coral Reef Studies and hosts a large international team of senior scientists, postdoctoral researchers and graduate students. Research in the CRE Laboratory is focused on a number of broad, overlapping areas, which are outlined in the following pages.

OCEAN ACIDIFICATION Understanding both the physical and ecological consequences of ocean acidification for reefs was a main focus of the team during the period of the Fellowship. The scale of focus ranged from single cells to ecosystems and involved manipulative laboratory, mesocosm and field experiments, and the modelling of organism, population and community responses under a suite of IPCC emission and stabilisation scenarios. Research highlights from the CP-FOCE and mesocosm experiments are detailed on pages 14 and 15. Senior researcher Dr Ken Anthony led a study, which modelled the impacts of OA at an individual reef scale. This research, carried out in collaboration with the University of Melbourne, and Griffith and Stanford Universities investigated how different combinations of CO 2 level and rates of herbivore fishing affected the resilience of a simple benthic reef community, as defined by its capacity to maintain and recover to a coraldominated state. The results supported two important conclusions: firstly, reefs already subjected to herbivore overfishing and eutrophication are more vulnerable to rising CO 2 and, secondly, under CO 2 regimes above 450–500 ppm, management of local disturbances will become critical to keeping reefs within an Acroporadominated state. Dr Paulina Kaniewska and collaborators from James Cook University, the University of Louisiana and the Queensland Department of Employment, Economic Development and Innovation established the major cellular and physiological impacts of

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OA on Acropora millepora, an important GBR reef-building coral (see Genomics). The effects of OA on reef structure can be seen both in the reef accumulation and destruction phases. Calcium carbonate (CaCO3) accumulation in coral reef ecosystems requires rates of carbonate production to exceed rates of loss, and biological mediation on CaCO 3 losses represents an essential component of destructive forces on coral reefs. PhD student Catalina Reyes-Nivia carried out research to improve understanding of the effects of OA and rising temperature on the dissolution of reef carbonates (coral and crustose coralline algae) by microborers (the microalgae, bacteria and fungi that comprise the endolithic microbial communities of corals and CCAs). The results showed that while future projections of OA and warming will lead to increased rates of bioerosion coming from these microbial sources, the structural properties of corals may influence the magnitude of bioerosion responses, resulting in a range of implications for reef carbonate losses of warming and acidifying oceans. Postdoctoral researcher Dr Manuel Gonzalez-Rivero also focused on the impacts of climate change and OA on habitat structure, by integrating novel approaches to the study of coral reef complexity and heterogeneity. Although corals are the main focus of many studies of climate change effects on reef ecosystems, due to their many critical roles, changing environmental

conditions also have serious implications for other reef organisms. Algal turfs develop on inert benthic surfaces in marine environments, including coral reefs. Composed of many types of algae, which take up carbon dioxide directly or in the form of bicarbonate, they are akin to a rainforest in that they form a multi-canopied structure. PhD student Dorothea Bender investigated the effects of OA in combination with eutrophication on reef algal turfs, exposing them to conditions predicted by the IPCC to occur over the next 100 years. Dorothea also examined the effect of CO 2 emission scenarios on the turf algal assemblages specific to damselfish territory, with the goal of integrating the phenomenon of herbivory and gaining a more ecological perspective on which particular drivers of change on the algal community might subsequently influence this ubiquitous group of coral reef fish. Postdoctoral researcher Dr Guillermo Diaz-Pulido (and Premier’s Fellowship research program member) examined the effects of OA and warming on another group of highly important group of reef calcifiers, coralline algae. The results of this study suggested that previous experiments focused on OA alone underestimated the impact of future conditions on coralline algae, with serious ramifications for the integrity of reef ecosystems.


SMALL, BUT PACKING A MIGHTY PUNCH Symbiodinium, aka ‘zooxanthellae’, are dinoflagellate protists that live in mutualistic symbiosis with many marine invertebrates, including corals, algae, jellyfish, anemones and molluscs. Previously considered to be one species, Symbiodinium microadriaticum is now recognised as a multitude of species belonging to the dinoflagellate genus Symbiodinium. This group of species consists of nine broad genetic clades (group) containing many ecologically and genetically distinct types. With global seawater temperatures rising and so many reefs at serious risk as a result, the potential link between algal type and the thermal tolerance of their host coral species has been the subject of much research. Technologies such as pulse-amplitude modulated chlorophyll fluorometry have made it easier to assess the status of the coral-algal relationship under a variety of stressful environmental conditions. With the partnership playing such a vital role in determining reef health and survival under climate change, it remains a top priority for research.

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PHOTOBIOLOGY One of the fundamental properties of reef-building corals is their ability to capture the energy from the sun, which is made possible through their symbiosis with the dinoflagellate algae from the genus Symbiodinium. The Fellowship team was able to apply techniques such as oxygen respirometry, Pulse Amplitude Modulated (PAM) fluorometry and High Performance Liquid Chromatography (HPLC) in investigations of highly relevant topics, such as the differences between clades of Symbiodinium in terms of photobiology and the key biochemical components of the Symbiodinium photosynthetic apparatus. Much of the work of the Photobiology group links with that of other CRE groups. For example, PhD student Alicia Crawley worked with CRE members Dr Davey Kline, Dr Simon Dunn, Dr Ken Anthony and Associate Professor Sophie Dove, and showed that high CO 2 levels lead to lowered rates of photorespiration, a photo-protective mechanism associated with coral based Symbiodinium. Similarly, PhD student Rachael Middlebrook measured a number of photosynthesis parameters and was able to conclude that the bleaching susceptibility of A. millepora during a bleaching event (as defined by symbiont loss) was no greater when corals had been pre-stressed by an early summer short-term thermal anomaly. PhD student Pim Bongaerts used two techniques for assessing photo-physiology of corals (respirometry and HPLC) during a reciprocal transplant experiment that explored the physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats. The study concluded that there were photo-physiological differences between coral transplants originating from the shallow and deep habitats, Acropora millepora has served as and presented additional evidence the study organism for many of that confirmed that observed the projects carried out as part of habitat partitioning of S. hystrix the Premier’s Fellowship research and its associated Symbiodinium program. This branching coral has a is reflective of a high degree of unique scaly appearance when the adaptive divergence along the depth polyps are retracted, making it one of gradients examined. the more easily identified species of the genus Acropora. In addition, the full genome of the species has been sequenced, making it an invaluable part of the toolkit for coral researchers.

THE CRE ‘LAB RAT’

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CORAL BLEACHING

SYMBIOSIS

Coral bleaching involves the loss of the brown dinoflagellate cells and leads to the host tissue becoming transparent and the white CaCO3 skeleton becoming visible. Observations of mass coral bleaching (often covering hundreds of square kilometres of reef) were first reported in the scientific literature in the early 1980s. Although a number of stresses including increased ultraviolet (UV) radiation, toxins and acidification can trigger bleaching, the scientific consensus is that mass coral bleaching and mortality is primarily driven by anthropogenic warming of the world’s oceans. The CRE Bleaching group has been at the forefront of studies of the physiology and ecology of bleaching and mass bleaching events, with recent work particularly focused on relating the physiology of bleaching and mortality to how environmental variables might change in the future, in line with the aims of the Fellowship.

The work of the Symbiosis and Bleaching groups is tightly coupled, as understanding the molecular and cellular basis of the coral-Symbiodinium relationship is integral to understanding how stressors might affect coral-dinoflagellate symbiosis, leading to its breakdown (bleaching). Some previous studies have concluded that the breakdown begins with increased reactive oxygen species (ROS) generation, while others have reported the release of viable symbionts via a variety of host cell derived mechanisms. Senior CRE researcher Dr Simon Dunn led an investigation of an alternative model of the breakdown, where changes in coral host mitochondrial integrity were the focus. Using confocal and electron microscopy, he was able to show that coral mitochondria (often likened to ‘batteries’, in that they provide energy to the cell) were disrupted by thermal stress, and that this degradation was independent of symbiont cellular deterioration. Other symbiont-independent changes to host cell functioning were also identified, highlighting the importance of host cell response to thermal stress and symbiosis dysfunction that has important implications for understanding how coral reefs will survive in the face of climate change.

Linking with the Photobiology group, PhD student Cameron Veal investigated the role of light in the bleaching process. He tested potential methods for the mitigation of irradiance-induced coral bleaching, and for acceleration of recovery, by altering the properties of the overlying water column. Although light is vital for the photosynthesis of reef-building corals, extended periods of excess exposure to solar irradiance may exacerbate both warm and cold water bleaching. In collaboration with colleagues from Israel and Tasmania, Cameron devised a system that altered the surface water properties through sprinkling water droplets (thereby altering the reflectance, eliminating lensing effects, improving water movement and breaking up the surface). Unfortunately, the sprinkler technology did not decrease radiance and thereby influence bleaching susceptibility. On the upside, the project did identify some important and previously unknown influences of wave lensing in shallow waters.

Organisms other than corals form a symbiotic relationship with Symbiodinium spp. and several species of marine sponge are known to actively excavate into calcium carbonate coral skeletons. Cliona orientalis is both a coral excavator and contains Symbiodinium, and PhD student James Fang received co-supervision from AIMS sponge specialist Dr Christine Schoenberg to assess the impacts of eutrophication, rising sea temperatures and OA on the sponge-Symbiodinium relationship. With the effects of OA making it increasingly difficult for corals to lay down skeletal material, the increasing abundance and strong competitiveness of bio-eroding sponges poses an additional threat to the survival of coral reefs and needs to be understood. James refined methods to study and show that sponge biomass and bioerosion rates do increase under ocean warming and acidification conditions. This work has implications for the carbonate balance of coral reefs by potentially changing the balance between calcification and erosion.

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FOCUS ON: THE MICROSCOPIC POWER BEHIND THE CORAL THRONE The state of the symbiotic relationship between coral hosts and their intracellular microalgae (Symbiodinium spp.) is the determining factor of their health and growth. Many environmental factors are known to disrupt the relationship, which results in the phenomenon known as mass coral bleaching and mortality. The Premier’s Fellow has coordinated a substantial amount of research focused on understanding the nature of the symbiosis and the factors that affect it, from the cellular through to the ecosystem level. Fellowship postdoctoral researchers Dr Linda Tonk and Dr Mathieu Pernice headed two of these projects supported by a Marie Curie Fellowship. Dr Tonk investigated the role of Symbiodinium genetic variation in coral vulnerability to environmental stress, while Dr Pernice explored the cellular and molecular mechanisms involved in the breakdown of the symbiosis. Their results provide valuable insights on the mechanics and causes of coral bleaching, some of which have implications for management strategies designed to minimise climate impacts.

GENETICS OF SYMBIODINIUM ON THE GREAT BARRIER REEF The Symbiodinium genotype of GBR corals has previously been found to be diverse5 and the first stage of the project consisted of compiling a database of existing information, which was found to be largely restricted to central and midshelf GBR locations. An extensive collection effort was therefore made to target specific sites and genera to complement the existing data. In total, over 3000 samples of coral, hydroid and molluscs were collected from 26 sites and the genotypes of all associated Symbiodinium were identified using molecular methods to gain a more detailed picture of Symbiodinium diversity on the GBR. The data were used to populate SymbioGBR, a webbased database of Symbiodinium diversity, host associations, and oceanographic environment on the GBR (see page 12). A significant finding of the study is that host identity plays an important role in defining and driving Symbiodinium distribution. The type of symbiont may be of importance to the thermal tolerance of a host, but whether a certain type occurs at a particular location is mainly host driven. With environmental factors known to influence the occurrence of host-symbiont combinations at a range of scales, from local to regional, it is therefore not prudent to focus solely on symbiont genetics when making management decisions. Data from the project were deposited into the RRRC Atlas (now e-Atlas) and information was also contributed to the book The Great Barrier Reef by James Woodford.

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LaJeunesse et al. 2003, 2004


CORAL CELL SURVIVAL IN THE FACE OF THERMAL STRESS To understand the impacts of projected climate change on the coral-Symbiodinium relationship, Dr Pernice exploited a new technology designed to visualise transfer of metabolic and other products between coral hosts and their symbionts. Part of this project, Dr Pernice conducted a study to decipher one of the important cellular mechanisms that operates during coral bleaching and subsequent mortality, apoptosis. A suite of enzymes known as caspases are central to the apoptotic pathway, which is a form of programmed cell death. Dr Pernice and a team of colleagues from the CRE Laboratory and France carried out a multiparameter analysis involving quantitative Real-Time polymerase chain reaction, fluorometric Assays and Terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) labelling to gain a greater understanding of the activation of genes involved in caspase production in response to heating and, hence, the initiation, progression and completion of apoptosis. Alongside these procedures, physiological indicators of coral bleaching were also monitored, so as to provide an integrated picture of the apoptotic pathways and their functional activation in the reef-building coral Acropora millepora during thermal stress. Symbionts provide their coral hosts with carbon-rich photosynthetic compounds, receiving metabolic waste products (principally ammonia and phosphate) in return. Traditional methods have been unable to provide detailed information on the nature of the translocated substances due to constraints associated with use of radioactively labelled substrates. Marie Curie scholarship holder Dr Pernice and colleagues from the CRE Laboratory, France and Switzerland were the first to modify and optimise a state-of-the-art technology – NanoSIMS – for use with the coral-Symbiodinium partnership. In doing so, they were able to analyse the transfer of inorganic nitrogen between the environment, symbiont and host over time, demonstrating that measurement of translocation dynamics is possible. In addition, they were able to quantify levels of stable isotope at both the cellular and sub-cellular levels, and opened up the possibility of studying the involvement and fate of other metabolites, and how these processes change, when corals are exposed to environmental stressors.

MANAGEMENT MATTERS How will the science of the Premier’s Fellowship research program help decision-makers manage the reef? • By exploring key aspects of the biochemistry and physiology of host symbiont interactions, this research broadens and deepens our understanding of stress, thereby helping managers improve policy initiatives • This research also provides invaluable insight into the causes of coral bleaching, which is critical information for attempts to understand and manage the impacts of climate change on the GBR • As coral bleaching and associated death has been identified as one of the biggest threats to the future of the GBR, this science is critical for reef managers • This research has an important role in informing the planning and mitigation measures for the future impacts of climate change on the GBR • This science is also vital to the development of other science that leads to the production of management tools such as satellite algorithms for predicting bleaching mortality and recovery

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SATELLITE OCEANOGRAPHY

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Extensive partnerships with the two leading international satellite agencies – NASA and NOAA – as well as experts from various national institutions allowed the members of the satellite oceanography group within the Fellowship team to build on information already available regarding the oceanography of the GBR. This led to the development of applications of satellite ocean colour and thermal remote sensing technologies to provide a critical understanding of the links between oceanographic processes, water quality and climate change in optically shallow habitats. The group used satellite data primarily from NASA’s Moderate Resolution Imaging Spectroradiometer (MODIS), and applied these to the GBR for two main purposes: understanding the dynamics of sea temperature, and using ocean colour to define processes relating to primary productivity and water clarity within the water column (see Focus On: Ocean colour and large-scale oceanography of the GBR).

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Premier’s Fellowship PhD student Ana Redondo-Rodriguez used sea surface temperature to explore climate variability across the GBR region and discovered that the connection between El Niño and mass coral bleaching and mortality varies with latitude. While the principal driver of extreme events on the GBR was previously thought to be El Niño periods riding on top of a warming ocean, the group showed that classical ENSO events have a strong signature in the atmospheric circulation in the northern GBR but no significant relationship with SSTs and that the opposite applies for the southern GBR. Conversely, El Niño/La Niña Modoki were found to be significantly related to summer SSTs on the northern GBR, but not on the southern GBR. In a separate study, the group explored indices in order to quantify upwelling on the central GBR, so that environmental and biological relationships associated with

upwelling in this area can be explored. They showed that ‘upwelling days’ (the number of days of upwelling) and diurnal variation in subsurface temperature (maximum–minimum, 20 m depth) are satisfactory metrics to describe the duration and intensity of upwelling events, respectively. The results show, somewhat paradoxically, that although upwelling involves cold water being brought near to the surface, it is linked to positive thermal anomalies on the GBR, both locally and regionally. Summers (Dec–Feb) with strongest upwelling occurred during the GBRwide bleaching events of 1997–1998 and 2001–2002. Upwelling in the GBR is enhanced during doldrums conditions that were a feature of these summers. During these conditions, the poleward-flowing East Australian Current flows faster, lifting the thermocline closer to the surface, spilling more sub-thermocline waters onto the shelf. Doldrums conditions also result in intense local heating, stratification of the water column and, when severe, coral bleaching. Upwelling intrusions are spatially restricted (central GBR), generally remain subsurface and are often intermittent, allowing GBR-wide bleaching to occur despite conditions resulting in enhanced upwelling. Intense upwelling events precede anomalous seasonal temperature maxima by up to two months and bleaching by one to three weeks, leading to the prospect of using upwelling activity as a seasonal forecasting index of unusually warm summers and widespread mass coral bleaching.


GENOMICS Genomics provides a detailed view of physiological diversity and function, as well as mechanistic insight into how organisms respond to environmental stress. Algal heat shock proteins (HSPs) play an important role in heat acclimation and environmental plasticity, and may be involved in the prevention of cellular damage during periods of environmental stress. Postdoctoral researcher Dr Nela Rosic explored HSP regulation in the coral Acropora millepora in response to heat stress by looking for alterations in the transcription profiles of algal HSPs. Differential gene expression profiles observed for members of two major HSP families – Hsp70 and Hsp90 – suggest diverse roles for these molecular chaperones during the heat stress response of A. millepora, and provide insight to the capability of symbiotic dinoflagellates and their host to tolerate future changes to the environment. Gene expression in corals in relation to stress was also explored by postdoctoral researcher Dr Paulina Kaniewska, who compared changes

REPRODUCTION AND RECRUITMENT Premier’s Fellowship Research Fellow Dr Selina Ward has been studying reproduction of GBR corals for over two decades and Premier’s Fellowship PhD student Chris Doropoulos was able to highlight the fact that OA can have an effect on a variety of coral lifehistory stages. Chris’ study, undertaken in collaboration with scientists from UQ and Griffith University, identified a connection between OA and coral reproduction, with OA found to reduce coral recruitment by disrupting coral larval-algal interactions. Temperature is also known to affect the reproductive processes of some reef organisms and postdoctoral researcher Dr Manuel Gonzalez-Rivero examined the reproductive phenology of the abundant bioeroding sponge Cliona orientalis in the southern Great Barrier

in the physiological characteristics and gene expression of A. millepora in relation to changes in carbonate water chemistry. When exposed to increased levels of carbon dioxide, the density of Symbiodinium within the coral tissues was seen to decrease, resulting in a concomitant drop in photosynthesis. A reduction in the respiration rate suggested reduced function of host tissue. Using a microarray – a powerful analytical tool that can measure expression of a large number of

genes simultaneously – Dr Kaniewska established that there was a significant change in host genes under different acidification scenarios, suggesting that acidification of the surrounding water also results in cellular physiological changes, including metabolic and cell transport processes, which may have negative effects on coral health. Further investigation of these influences is currently underway.

Reef. Bioeroding sponges have a destructive effect on the carbonate structure of coral reef habitats and, as such, are hugely important component of reef ecosystems, yet basic aspects of their population biology, including reproduction, remains understudied. Dr Gonzalez-Rivero was able to show that

seawater temperature strongly drives sponge investment in reproduction, with his results suggesting that temperature anomalies due to climate change can have a profound impact on the reproductive effort and phenology of C. orientalis.

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ECOSYSTEM RESPONSES The responses of natural ecosystems such as coral reefs to rapid changes to the environment are inherently complex and interconnected, and ultimately impact on the ecological goods and services that are provided to associated coastal human populations. The Ecosystem Responses group has used a variety of tools within the CRE laboratory to study a number of ecosystem responses at a range of scales, from empirical measurements on the reef crest to remote sensing from space. Understanding ecosystem responses is critically important to conservation goals as well as for planning adaptation responses to threats such as climate change. As one of their four Centres of Excellence, the CRE Laboratory was deeply involved with the World Bank-Global Environment Facility Coral Reef Targeted Research and Capacity Building for Management Program (www.gefcoral.org), the first phase of which ran from 2004–2010, with the Premier’s Fellow in the role of Coordinator of the Australasian Centre of Excellence and Chair of the Bleaching Working Group. The Program was focused on trying to understand changes within coastal ecosystems and their impact on human dependence, including in Australia. The aim of the CRTR program was to address knowledge and technology gaps, promote learning and capacity building, and link scientific knowledge to management and policy within the realm of coral reef ecosystems across all regions of the world. The aspirations of this project were highly consistent with the ambitions of the Premier’s Fellowship, and hence provided yet another platform for the Premier’s Fellow and his team to establish a range of linkages and collaborations that directly addressed key questions within the Fellowship research program.

FOCUS ON: OCEAN COLOUR AND LARGE-SCALE OCEANOGRAPHY OF THE GBR Around the time that reports of mass coral bleaching began to appear in the scientific literature, a highly significant technical advancement revolutionised our capacity to visualise the colours of the ocean, which are a product of particles suspended in the water column absorbing, reflecting or scattering incident light. NASA’s Coastal Zone Color Scanner was launched in 1978 on board the Nimbus 7 satellite and since then several other sensors have been launched, generating time-series of ocean colour data that have been used to gain insight to the processes behind a wide range of environmental phenomena, including coral bleaching. Data from three of these sensors – SeaWIFS (which operated until 2010), MODIS and MERIS – have been used by the satellite oceanography group to develop colour oceanography for the GBR and so better understand a wide range of processes, from the movements of manta rays relative to the productive regions of the Coral Sea to the influence of benthic properties on the remotely sensed reflectance of ecosystems. In order to define and model physical and biological processes at the relevant scales in space and time, and therefore understand how global change translates into changes on the Great Barrier Reef, satellite technology was applied to allow observation of patterns in biological and ecosystem responses down to the level of individual coral reefs. Achieving this resolution of observation is critical to informing responses to those changes and this important outcome of the Fellowship was made possible through collaboration with experts from leading satellite agencies: NASA Ocean Biology Processing Group, NOAA, AIMS and the Curtin University Remote Sensing and Satellite Research Group.

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FOCUS ON: DEEP REEF, SAFE HAVEN? Reef communities represent a dynamic equilibrium between processes that re-establish coral reefs (‘recovery’) and those that lead to the deterioration of reef communities (‘disturbance’). With many shallow-water coral reefs (<30 m) in decline due to local and global anthropogenic stresses, there has recently been renewed interest in the ‘deep reef refugia’ hypothesis (DRRH) 6, which stipulates that deep reef areas (1) are protected or dampened from disturbances that affect shallow reef areas and (2) can provide a viable reproductive source for shallow reef areas following disturbance. As reefs face continued and unprecedented anthropogenic disturbance, the hypothesis constitutes one of the few hopeful aspects of coral reef biology. Fellowship program then-PhD student Pim Bongaerts reviewed the assumptions of the DRRH using the Caribbean as an example, and also explored the molecular ecology of GBR mesophotic coral ecosystems (MCEs). These deep, light-dependent coral communities are found at depths in excess of 30 m (usually confined to a maximum depth of 100–150 m) and they have received little attention compared to their shallow-water counterparts due to their relative inaccessibility. However, recent technological advances (e.g., ROVs, autonomous underwater vehicles, technical diving) have sparked a renewed interest in these enigmatic ecosystems, particularly as they seem to be largely protected from several major reef stressors, such as storm events and elevated seawater temperatures. By exploring the molecular ecology of MCEs, Dr Bongaerts has furthered our understanding of the ability of these deep reef areas to act as refugia and, importantly, to re-seed shallow reefs post disturbance. In the case of the Caribbean, he found that while there is evidence to support the notion that deep reefs can escape the direct effects of storm-induced waves and thermal bleaching events, they are not immune 6 7

to disturbance. The upper mesophotic zone (30–60 m) seems to hold the greatest potential to aid in reef recovery following disturbance due to species overlap with the shallow reef and the ability to at least partially escape certain disturbances. Dr Bongaerts’ study of GBR MCEs focused on the genetic connectivity between shallow and deep coral populations and the genetic diversity of Symbiodinium associated with mesophotic corals. Dr Bongaerts and colleagues carried out an initial assessment of Symbiodinium diversity using denaturing gradient gel electrophoresis (DGGE) fingerprinting of the internal transcribed spacer region 2 (ITS2) of the ribosomal DNA. Symbiodinium diversity was compared to previously published information on related coral taxa from shallower GBR locations to provide a first indication of whether mesophotic corals associate with a distinct deep-water Symbiodinium community and whether known patterns of host-symbiont specificity are maintained across broad bathymetric ranges. There was little indication of a differentiated deepwater Symbiodinium community, with the majority of corals associating with pandemic Symbiodinium types also commonly found in shallow water. Novel host-symbiont associations were only observed in species with a horizontal symbiont acquisition mode (gaining them from the external environment), whereas species with a vertical symbiont acquisition mode (directly inherited) harboured previously described host-specific lineages of Symbiodinium (with the exception of the novel symbiont C131). These observations indicate that mesophotic reefs can harbour coral-Symbiodinium combinations similar to those in shallow water, which appears hopeful with regards to the ability of deep reefs to act as a source for recruits in shallow water. Nonetheless, the coral host and associated Symbiodinium may still be differentiated on the population level7.

population structure will be important to gain a better understanding of how different life history strategies affect levels of connectivity between shallow and deep habitats. Only then will the extent to which deep reefs may act as a refuge in the face of global reef decline become apparent.

MANAGEMENT MATTERS How will the science of the Premier’s Fellowship research program help decision-makers manage the reef? • The mesophotic zone of the reef is almost completely unstudied yet contains an equal, if not greater, biodiversity than the more shallow sections of the reef • This research used innovative technology to show that the upper mesophotic zone (30–60 m) seems to hold the greatest potential to aid in reef recovery following disturbance • This discovery and science can now be factored into future management plans for the GBR regarding reef recovery and resilience

As we move forward with research on MCEs and their potential role as refugia, integrative molecular approaches looking at both Symbiodinium and host

Glynn 1996; Riegl and Piller 2003; Armstrong et al. 2006 Barshis et al. 2010, Bongaerts et al. 2010, Finney et al. 2010

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BEYOND THE CORAL REEF ECOSYSTEMS LABORATORY The Premier’s Fellow has contributed to the research projects of scientists from a number of national and international institutions, including that of a team led by Dr Todd LaJeunesse (Pennsylvania State University, USA) who investigated factors influencing the relative ecological dominance and genetic diversification of Symbiodinium. He collaborated with Professor John Bruno (University of North Carolina, USA) on a highly influential review of the impact of climate change on marine ecosystems and with Spanish biologists Professor Carles Pelejero and Dr Eva Calvo (ICREA and Institut de Ciències del Mar, Spain) on a review of recent advances in our understanding of ocean acidification with a particular emphasis on past changes to ocean chemistry, and what they can tell us about present and future changes. The Fellow also held a number of positions where he was able to advise on and influence research on a range of issues facing the marine environment, including climate change. These positions included: • Coordinating Lead Author for the regional ocean’s chapter in the Fifth Assessment Report of the Intergovernmental Panel on Climate Change • Co-author within the Fifth Assessment Report of the intergovernmental panel on climate change for cross chapter consensus topics on ocean acidification, upwelling, heat stress and the relocation of marine organisms to higher latitudes • Chair, Blue Ribbon Panel, Global Partnership for Oceans, World Bank • Member of the Scientific Advisory Board of the Biodiversity Research Centre of the Academia Sinica (Taipei, Taiwan) • Member of Scientific Advisory Board of the Zentrum für Marine Tropenökologie (Bremen, Germany) • Member of the Review Board of the Red Sea Research Centre (King Abdullah University of Science and Technology (KAUST), Saudi Arabia) • Visiting Professor, Stanford University (USA) • Scientific Advisor to the Centre for Ocean Solutions, Stanford University • Member, Royal Society of London Marine Advisory Network (MAN) • Chair, Global Environmental Facility-World Bank-Intergovernmental Commission (IOC) working group on climate change and coral health www.gefcoral.org • Member, International Scientific Advisory Committee, Great Barrier Reef Foundation.

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KEY OUTCOME AREA 3: RESEARCH TRAINING AND MENTORSHIP

The Coral Reef Ecosystems research team benefited from the wealth of multidisciplinary expertise brought by the laboratory members and from the knowledge gained during the period of the Fellowship. As it moves into its next phase the CRE group is well placed to build on the developments made during the past five years. After successfully supervising PhD, Masters and Honours students, and working in collaboration with each other and outside agencies, several senior members of the CRE Laboratory have gone on to take up positions elsewhere, setting up research groups of their own and continuing to foster the next generation of reef scientists. This flow of knowledge and skills from the Premier’s Fellow’s research team into other laboratories in Australia and around the world is another important legacy of the Fellowship.

HIGHLIGHTS • Between 2009 and 2013, 20 Doctoral students, and four Masters and Honours students in the CRE Laboratory successfully completed their studies. A further five Fellowship-linked graduate students will complete their studies in the near future. • Eight former Fellowship PhD students have gone on to take up postdoctoral positions at institutions within Australia and overseas. • Senior Fellowship team members have taken up positions where they will continue to make positive contributions to the conservation and management of the GBR: Dr Ken Anthony is currently based in Townsville, leading AIMS’ Responding to Climate Change Team and Dr Scarla Weeks was appointed as a senior lecturer in the School of Geography, Planning and Environmental Management at UQ in 2011. Dr Selina Ward is now a lecturer in the School of Biological Sciences at UQ and Dr Guillermo DiazPulido is a senior lecturer in Griffith University’s School of Environment and a Research Member of the Australian Rivers Institute. • The Fellow and former Fellowship postdoctoral researcher Dr Davey Kline (now employed at Scripps Institution of Oceanography) are involved in the analysis of data collected for the Catlin Seaview Survey and the Global Reef Record.

Many of the research projects carried out by CRE Laboratory members were necessarily connected, leading to collaboration within the group as well as with outside agencies and institutions. This connectedness was beneficial to students, who were able to draw on expertise in other sub-groups of the laboratory and make use of a number of innovative technologies such as the operational algorithm for processing satellite imagery and the mesocosm system. The mesocosm provides one of the best examples of connectivity between CRE research areas, individual projects and lab members: Under the guidance of project leader Associate Professor Sophie Dove and two postdoctoral positions, four PhD students, two Honours students, two interns, two technicians, one occupational trainee and two laboratory managers (co-opted from general duties) were trained in a wide variety of techniques and used the mesocosm system to study coral reef communities, corals, sponges, sea cucumbers and sediments. Some of these acidification-focused projects also contributed to the outputs of the Symbiosis, Photobiology, Genomics and Ecosystem Responses research areas.

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FOCUS ON: UNDERSTANDING THE OCEANS FROM SPACE: DR SCARLA WEEKS Dr Scarla Weeks was employed as a Senior Research Fellow on the Premier’s Fellowship team until 2011. Her particular expertise in applying satellite data to the marine environment at ecosystem scales led her to contribute data and expertise to a large number of Fellowship research projects, including those of the Coral Reef Ecosystems Laboratory and Fellowship collaborators NOAA and NASA, with whom she has a longstanding and ongoing research relationship. Originally hailing from South Africa, Dr Weeks completed her PhD in Satellite Oceanography at the University of Cape Town, pioneering the use of operational marine remote sensing in southern Africa. She joined the CRE Laboratory in 2005, where she continued to work with key collaborators, including the NASA Ocean Biology Processing Group, with whom she began to develop satellite applications for coral reef ecosystems. Her interests and applications broadened further to include the link between climate change, oceanography and the biological response. An ARC Linkage Grant awarded in 2010 allowed Dr Weeks – in partnership with NASA – to develop an operational algorithm for processing satellite imagery to map water clarity and light availability in coral reef waters, and led to the production of a time series of ocean colour product maps for the GBR. From 2009–2011, the group of CRE researchers led by Dr Weeks (OceanSpace) produced a freely-available monthly report of environmental conditions on the GBR, with satellitederived data and forecasts regarding phenomena such as SST anomalies and bleaching. In 2011, Dr Weeks was appointed as a Senior Lecturer in the School of Geography, Planning and Environmental Management at The University of Queensland. As leader of the Biophysical Oceanography Group in GPEM, Dr Weeks continues to collaborate with experts she has now worked with for over two decades, during her time in South Africa and as part of the Premier’s Fellow’s team. Her current collaborative investigations include an integrated examination of the drivers of movements of large filter-feeding organisms of high ecotourism value, monitoring the health of Torres Strait coral reefs, and a study of critical seabird foraging locations and trophic relationships for the Great Barrier The Great Barrier Reef Ocean Observing System, which is managed by Reef. AIMS on behalf of a consortium of partners, including UQ, is part of IMOS. GBROOS is an observing system that looks to document the impact of Dr Weeks is a member of key state the Coral Sea on the Great Barrier Reef and in particular to provide the and national bodies such as the observational data to understand long-term change and the impact this will IMOS National Working Group have on the Great Barrier Reef. on Bio-optical Instrumentation and Observing, which has the broad mandate of tackling issues of national relevance related to biooptical measurements and interpretation, and is funded under the National Collaborative Research Infrastructure Strategy (NCRIS). She is also deeply involved in the international ocean colour community, having been elected to represent Australia on the committee of the International Ocean Colour Coordinating Group (IOCCG), made up of an international Committee of Experts comprising representatives from both the provider (Space Agencies) and user communities (scientists, managers). The objectives of the IOCCG are to develop consensus and synthesis at the world scale in the subject area of satellite ocean colour radiometry. Dr Weeks served as a committee member from 2009–2012.

OCEAN OBSERVING IN QUEENSLAND

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FOCUS ON: GETTING TO THE BOTTOM OF REEF MATTERS: PIM BONGAERTS Dr Pim Bongaerts started as a student in the Premier’s Fellowship team, but has stayed in the laboratory and over the years has established himself as a leading international expert in the field of mesophotic coral systems. Dr Bongaerts completed his doctoral studies under the supervision of Professor Ove Hoegh-Guldberg, Dr Cynthia Riginos and Dr Tyrone Ridgway in 2011. He remained at UQ to carry out postdoctoral research on MCEs (which start at at 30-40 m and extend down to >150 m in the Fellow’s laboratory. Since 2012, and representing the Global Change Institute, he has been cataloguing the deep reefs of the GBR, and elsewhere, as the Deep Reef Scientific Leader of the Catlin Seaview Survey team. Hailing from the Netherlands, Dr Bongaerts arrived in Queensland in 2006 to carry out an internship as part of his MSc research and stayed on after being awarded a highly competitive PhD scholarship at The University of Queensland. Focusing on the adaptations of corals living in both shallow and deep reef habitats, he employed a range of molecular techniques to explore the genetic structuring of corals and their associated Symbiodinium over depth. He has obtained research funding from organisations such as the Great Barrier Reef Foundation (being the recipient of their 2010 Bommies Award), the Explorers Club, PADI Foundation and Australian Geographic. Dr Bongaerts’ research is reaching a wide audience: Several of his 15 publications are already highly cited by other scientists and his use of timelapse photography was featured by BBC Nature (http://www.bbc.co.uk/ nature/16843053). His work has also been reported by NBC, CNN, Fox News, Australian Geographic, New Scientist, and – hopefully inspiring the next generation of reef researchers – Totally Wild. A paper providing some of the first evidence that coral populations can be strongly genetically structured across adjacent reef habitats and highlighting the role of depth gradients on reefs in the diversification of coral species was awarded the Virginia Chadwick Award for Best Student Paper in 2010. Dr Bongaerts is also the webmaster, skilful database expert and coeditor of www.mesophotic.org, a collaborative effort of NOAA and The University of Queensland that serves as a central source of information on mesophotic coral ecosystems.

CORAL REEF ECOSYSTEMS LABORATORY GRADUATE STUDENTS Siham Affatta; Campbell Allen; Dorothea Bender; Pim Bongaerts; Marites Canto; Robert Canto; Margaux Carmichael; Alicia Crawley; Ajax Diaz-Ruiz; Christopher Douroplous; Udo Engelhardt; David Harris; Meegan Henderson; James Kar-Hei Fang; Paulina Kaniewska; Narinratana Kongiandtre; Charlotte Kvennefors; Angela Lawton; Robert Mason; Rachael Middlebrook; Juan-Carlos Ortiz; Chantelle Reid; George Roff; Ana Redondo-Rodrigues; Catalina Reyes-Nivia; Zoe Reynolds; Andrew Taylor; Cameron Veal; Mirta Zupan

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KEY OUTCOME AREA 4:

COMMUNICATION, ENGAGEMENT AND POLICY IMPACT Queensland is home to a large cluster of world-class coral reef science research and management experts. By leading an alliance of science, government, industry and philanthropic partners, the Premier’s Fellow sought to facilitate proactive management responses and effective policy development to combat the effects of climate change on the Great Barrier Reef. Therefore, a major element of the Premier’s Fellowship has been taking the message of climate change to Australia and beyond, engaging with as broad an audience as possible, from the decision-makers who make the decisions of today to the Year 11s who will become the scientists of tomorrow. This stage of the Fellowship is arguably the most important in that it involves the translation of fundamental science into outcomes and responses that are relevant to the reef’s management and, ultimately, the reef’s future. To this end, the Fellow continued to build on existing collaborative relationships with the key state reef management agency GBRMPA and forged new alliances for the provision, coordination and synthesis of information with institutions such as AIMS and NOAA. Through lectures, workshops, policy analysis, tailored knowledge transfer and capacity-building activities, the Fellow was able to help develop management-relevant outputs and policies that should result in real benefits to the GBR and Queensland. He presented seminars around the world, and social media outlets such as Twitter, YouTube and Google+ helped to propel information about the Premier’s Fellowship to a global audience of many millions, strengthening Queensland’s reputation as a research leader.

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MANAGEMENT AND COMMUNICATION HIGHLIGHTS • Being appointed as the Coordinating Lead Author of Chapter 30 (The Ocean) of the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, due for full release in August 2014. • Chairing the Blue Ribbon Panel, a group of 21 ‘ocean leaders’ nominated by the global ocean community and including CEOs of some of the largest seafood companies in the world, government ministers and scientists, as well as prominent marine conservationists. The Panel was convened by the World Bank and tasked with providing recommendations designed to help the Global Partnership for Oceans, or any institution investing in oceans, achieve positive impact and sustainable outcomes (www.globalpartnershipforoceans.org/blue-ribbon-panel). • Building on the already-strong partnership with the Great Barrier Reef Foundation by being a member of its Scientific Advisory Committee and Chair of the Attributes of a Resilient Reef, which brings together 15 scientists from UQ, JCU, Griffith University, AIMS, CSIRO and GBRMPA. The Working Group was set up and funded by the Foundation to compile a set of criteria (attributes) describing the unique values of the GBR and to identify which values are vulnerable to the impacts of climate change (Great Barrier Reef Foundation 2010). The Fellow has also been appointed Chair of the Technical Advisory Group to the Great Barrier Reef Foundation. • Establishing and coordinating a two-part workshop on ocean acidification held in partnership with the Great Barrier Reef Foundation. • Interacting with industry leaders and their employees through the Great Barrier Reef Foundation’s ZooX Ambassador program. • Co-chairing (with NOAA Coral Reef Watch coordinator Dr Mark Eakin) a four-day workshop entitled Satellite Monitoring of Reef Vulnerability in a Changing Climate, which brought together scientists representing GBRMPA, AIMS, the Australian Bureau of Meterology, several Australian universities and other international partners including NASA. • Maintaining a blog aimed at facilitating discussion on climate issues and disseminating research findings (www.climateshifts.org). • Delivering an invited address at the National Youth Science Forum, which is dedicated to inspiring young Australians to a future in science.

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FOCUS ON: CATLIN SEAVIEW SURVEY: STATE OF OUR CORAL REEFS We live in a media-dominated society where anyone with access to the internet can talk face-to-face with a friend or relation in a far-off country or view a house on a street thousands of kilometres away, all from the comfort of their own home. Now, there is another online presence available that is revolutionising the way we see our world: the Catlin Seaview Survey (CSS). Over several years, many areas of coral reef rarely visited or measured by science will be surveyed and the results made freely available to scientists and the public alike. Communication is a key part of the project, which uses state-of-theart technology to gather and analyse images and samples, and outlets such as Google+ and Twitter to maintain an immediate online presence. Videos are available to view on a dedicated Google YouTube channel that has nearly 2000 subscribers, and the Catlin Seaview Survey has over 8000 Facebook friends. In total, over three million people are connected to the project via a variety of media outlets. Launched in September 2012, the Catlin Seaview Survey is one of few scientific efforts to make such a massive and immediate connection with so many people. Media impressions have been recently measured at over 85 billion.

8

Time Magazine, July 31 2013

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The project, sponsored by global insurers Catlin Group Ltd, is a collaborative effort between the Global Change Institute, not-for-profit organisation Underwater Earth and partner Google. The Premier’s Fellow is the Chief Scientist for the Catlin Seaview Survey project and a further five GCI staff members are part of the project support team. Several GCI researchers are part of the scientific team including: Dr Pim Bongaerts, who leads the deep reef survey component, and Dr Manuel GonzalezRivero and Dr Ben Neal who jointly lead the shallow water survey team. The GCI team has developed a great collaboration with communication experts Richard Vevers (Director of the CSS) and Lorna Parry. Other GCI and CRE Laboratory researchers have been part of expedition teams that have carried out surveys on the Great Barrier Reef and in over 19 countries worldwide. There are two main project components. For the shallow reef survey, images are captured and analysed using sophisticated camera and software technologies to catalogue vast tracts of reef around the globe. The deep reef survey is particularly concerned with assessing the impacts of climate change on the health and biodiversity of the leaststudied coral reef zone, that from 30– 100 m (see Focus On: Deep sea, safe haven?). A related project is currently developing online courses and citizen science activities to build upon the legacy of this remarkable project.

Reef surveys have been conducted at over 30 sites in the Great Barrier Reef/ Coral Sea region (imagery consisting of a total of 175 km of reef), more than 13 countries in the Caribbean (imagery consisting of a total of 375 km of reef) and at other sites such as the Galapagos Islands. With funding secure until 2015, the focus has shifted to Southeast Asia and the Coral Triangle in 2014, but with the database already bursting with images, a further aspect of the project was launched in September 2013: the Catlin Global Reef Record (http:// globalreefrecord.org; see Focus On: Social media: A new world vision for coral reef research). The Global Reef Record is a research tool aimed at collating and communicating the coral reef science of the Catlin Seaview Survey and combining that information with data from other leading sources of marine scientific research. A recent Time Magazine article on the project sums it up as ‘big data for a very big scientific challenge’ 8. Coral reefs are deteriorating at a rate of 1–2% per year, and both the Catlin Seaview Survey and the Catlin Global Reef Record are applying innovative technology and thinking to address this pressing global issue, making vast amounts of crucial data quickly and freely available to researchers, policy makers and all those involved in conserving our precious coral reef environments. It’s reef science as we haven’t seen it before; it’s a gamechanging research endeavour.


FOCUS ON: ENGAGING EMPLOYEES The Premier’s Fellow has been involved with two innovative schemes run by the Great Barrier Reef Foundation that aim to link business and reef conservation. The Great Barrier Reef Foundation Chairman’s Panel builds support for both the Foundation and the Great Barrier Reef with the Chief Executives and Chairs of many large Australian companies. This involvement with the Great Barrier Reef Foundation, chaired by Dr John Schubert AO (Chairman), represents an enormous opportunity to bring the key issues associated with the Great Barrier Reef to Australia’s business leadership. www.barrierreef. org/who-we-are/chairmans-panel The Fellow participated in the ZooX Ambassador Program as a Special Presenter in September 2012, showcasing the mesocosm system and lecturing on the effects of climate change on the reef. The Program provided benefit to participating employees (who were recognised as sustainability champions) and businesses (through the potential positive commercial and environmental outcomes of the ambassador-designed projects), the Foundation (through investment) and the Reef itself (through the outcomes of research made possible with funding generated by the Program). The program provides an opportunity for the Great Barrier Reef’s corporate partners to identify and develop sustainability champtions for the reef. Now in its seventh year, the program has had in excess of 170 Reef Champions from 11 companies participate in the ZooX Ambassador program. Further information on the Program can be found at www.barrierreef.org/who-we-are/zoox-ambassador-program

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PUBLICATIONS: OUTPUT AND RECOGNITION

THE SPOKEN WORD

Maintaining a high publication rate in peer-reviewed scientific literature was set out as an important overarching aim of the Fellowship. This expectation was exceeded, with the annual number of citations for the Fellow’s papers growing from just under 1200 in 2008 to nearly 2000 in 2012, and other publicationrelated achievements including the following:

The following represents a small selection of the nearly 50 plenary addresses, invited presentations and lectures given by the Premier’s Fellow between 2009 and 2013:

• 129 of the Fellow’s career total of 377 publications (as of November 2013; sources: Google Scholar, Thomson Reuters ResearchID; includes non-journal literature, book chapters, conference proceedings and abstracts, and major reviewed research reports) have been produced since the beginning of his tenure as the Premier’s Fellow in 2009. This equates to 34% of his total publishing output during his career. 87 papers were in peer-reviewed journals, and two of these, published in 2010 and 2012, feature on the Thomson Reuters Essential Science Indicators Most Highly Cited Papers List, having together already been cited over 150 times (within the first few years).

• Climate change in the ocean – the big picture? ARC Centre of Excellence symposium Coral Reefs in the 21st Century, Townsville, 2013.

• The citation rate of his publications results in the Fellow having an h-index of 61 as of November 2013 [Google Scholar, or 51 on Thomson Reuters]. The h-index is recognised internationally as an index of scientific research impact, incorporating measures of both the productivity and impact of the published work of a scientist. • The Fellow is currently the most cited Australian author (and 3rd internationally out of 53,136) authors on the subject of climate change (2009, Thomson Reuters ISI Web of Science). • In 2012, the Fellow was selected by Thomson Reuters Australia to receive a Citation Award in recognition of his outstanding contribution to research in the field of ecology. He is in the top 10 most cited authors in this field. A wide range of other publications have resulted from Fellowship activities and collaborations, in keeping with the aim to translate science being generated by the Fellowship research program into meaningful outcomes for public communication, industry advice, management and policy development. A selection of these written publications includes: • R esilient Coral Reefs Successfully Adapting to Climate Change – A Research Portfolio, Great Barrier Reef Foundation. ISBN: 978-0-646-54785-5 • A co-authored book published by Springer/CSIRO Publishing entitled The Great Barrier Reef (edited by P. Hutchings, M. Kingsford & O. HoeghGuldberg) won a Whitley Award commendation in 2009. These awards are made annually by the Royal Zoological Society of New South Wales and are presented for outstanding publications that contain new information about the fauna of the Australasian region. • Hoegh-Guldberg et al. (2009) The Coral Triangle and Climate Change: Ecosystems, People and Societies at Risk. WWF Australia. • Hoegh-Guldberg et al. (2011) Vulnerability of coral reefs in the tropical Pacific to climate change in Vulnerability of tropical Pacific fisheries and aquaculture to climate change, edited by J.D. Bell, J.E. Johnson and A.J. Hobday. Secretariat of the Pacific community. • An article read by over 14,000 people was listed as one of the top ten of 2011 by academic journalism website The Conversation (http:// theconversation.com/the-conversations-top-ten-articles-in-2011-4929).

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• Saving the Planet one Ocean at a Time, BrisScience, Brisbane City Hall, 2013. • T homson Reuters Citation & Innovation Awards, Canberra. One of two award winners invited to address the Press Club, Canberra, 2012. • C oral reefs in the rapidly changing climate: going, going, gone? Nobel Conference, Gustavus Adolphos College, Minnesota, 2012. • C oral reefs and global climate change: Where do the solutions lie? Keynote address, International Coral Reef Symposium, Cairns, 2012. • Ocean planet: Understanding, living and meeting the challenges of a changing world, Peter Doherty Lecture, Indooroopilly State High School, 2011 (also filmed and made into an episode of ABC Catalyst). • L arge-scale change in marine ecosystems, Invited speaker, World Forum on the Environment and Enterprise, Oxford University, 2011. • Our Changing Oceans: Evidence, implications and ramifications, Stanford University, 2010. • C oral Reefs and Rapid Climate Change: Impacts, Risks and Implications for Tropical Societies, International Scientific Congress on Climate Change, University of Copenhagen, 2009.


MASS MEDIA AND A GLOBAL FELLOWSHIP Fellowship-related activities and findings have been presented to millions of people representing many sectors of society in a huge variety of ways, in keeping with the way traditional information sources have transformed in recent times. From blogs, to public lectures in Brisbane, plenary addresses in Spain, virtual dives, and workshops in Switzerland, news of the Fellowship has been taken around Australia and the world – and back again – many times over the past five years. In 2010 alone, the national and international news coverage for the Premier’s Fellowship included 17 features on the ABC (radio, print, television) and 56 features by other Australian news outlets (including the Australian, Sydney Morning Herald and Brisbane Times). There were 16 features in the USA in that year and another 100 print, radio and online articles appeared in the media of a further 27 countries. This breadth of coverage and audience figures took on a new dimension in 2012, with the launch of the Catlin Seaview Survey and then, in 2013, the Blue Ribbon Panel Report. The launch of Underwater Street View with Google and the Catlin Seaview Survey gained over 80 billion media impressions. Concerted publicity drives meant that these two initiatives garnered huge media attention (see Focus On: Social media: A new world vision for coral reef research).

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CATLIN SEAVIEW SURVEY IN THE CARIBBEAN: A SNAPSHOT 13 countries surveyed: • Anguilla • Aruba • The Bahamas • Belize • Bermuda • Bonaire • Curaçao • Guadeloupe • Mexico • St Eustatius • St Martin and St Maarten • St Vincent and the Grenadines

Premier’s Fellowship team presented scientific seminars about the project to these organisations: • International Coral Reef Initiative • Wildlife Conservation Society • Bermuda Institute of Ocean Sciences • Instituto de Zoología y Ecología Tropical (Venezuela) • Department of Fisheries and Resource Management (Anguilla) • School of Field Studies (Turks and Caicos Islands) • Healthy Reefs for Healthy People Initiative

• Turks and Caicos Islands

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• Comisión Nacional de Áreas Naturales Protegidas (Mexico)


FOCUS ON: SOCIAL MEDIA: A NEW WORLD VISION FOR CORAL REEF RESEARCH Two projects with which the Premier’s Fellow had heavy involvement were launched in September and October 2013, and both demonstrated the power of social media for science communication. The Fellow chaired the Blue Ribbon Panel, which was convened by The World Bank to advise the Global Partnership for Ocean and was comprised of 21 experts from 16 countries. The Panel’s report Indispensable Ocean: Aligning ocean health and human well-being was released on 16 October 2013. Within days, the media release of the report entitled ‘Business urged to do more to save oceans: World Bank study’ had garnered over 212 million media impressions (using a media industry standard that combines viewership, circulation and online visitor numbers) via Reuters outlets such Yahoo! and CNBC. Through a concerted effort of media releases, proactive pitches and interviews, it took just three weeks following its launch in Bermuda for the Catlin Global Reef Record to achieve an exceptional media presence. In total over 240 million impressions have been recorded. This includes representation by top-tier business/mainstream outlets such as CNN (broadcast and online), CBSNews. com, Associated Press TV, Time Magazine, Huffington Post, The Daily Mail and many others, and featured articles in top science, technology and climate outlets such as Science, Popular Science and Weather.com. Importantly for the main funding partner, Catlin Group Ltd, it also gained important core audience insurance trade coverage. The stories have highlighted the global, scientific significance of the Catlin Global Reef Record, and raised the profile of the Catlin Seaview Survey and the Premier’s Fellowship. In addition to the above projects, the Fellow started the popular blog www. climateshifts.org in 2007 and maintained it throughout the period of the Fellowship. The blog deals with topics relating to science, climate change, politics, coral reefs and the environment. By 2012, the blog had been visited by over 90,000 unique visitors and registered around 20,000 hits each month.

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CONCLUSION “The sea, the great unifier, is man’s only hope. Now, as never before, the old phrase has a literal meaning: We are all in the same boat.” Jacques-Yves Cousteau (Marine Conservationist)

FELLOWSHIP LEGACIES Being awarded a Queensland Premier’s Fellowship allowed the Fellow to focus on research and research training, establish a highprofile Institute dedicated to global change research, and contribute to the understanding as well as policy development in this area at state, federal and international levels. The support provided by the program also enabled him to attract major research opportunities to Queensland and the University. As a result, he was able to build projects such as the Catlin Seaview Survey and ARC Linkages with the United States, right here in Brisbane. These opportunities brought in over $15 million to Queensland (much of which supported up-and-coming Queensland research scholars and postgraduate students). This activity and capacity allowed the Fellow to pursue key questions facing the Great Barrier Reef and coral reefs in general, and to develop and establish the Global Change Institute at The University of Queensland. Already, this new Institution has attracted over $60 million in research funding in areas of direct importance to Queensland (e.g., food security, climate change, clean energy solutions), and as the ARC Centre of Excellence for Coral Reef Studies moved into a new seven-year phase at the beginning of 2014, these two organisations are cementing

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Queensland’s reputation as the global centre for coral reef ecosystem research. With the Great Barrier Reef still facing an uncertain future due to a multitude of threats, this research – and other legacies of the Premier’s Fellowship – will continue to be of paramount importance in the coming years and decades. The legacies of this Premier’s Fellowship are numerous and diverse, from infrastructure to partnerships and collaborations, ongoing grants and projects, publications, documentaries and data. The Premier’s Fellowship has provided Queensland and Queenslanders with important information and technology for understanding how ocean warming and acidification are likely to propagate through coastal ecosystems such as the Great Barrier Reef. This understanding is important in providing accurate information on the types of changes, and the options available in terms of management responses. In addition to providing critically important knowledge and understanding, the Fellowship has also generated a number of unique tools with important capacity for efforts aimed at preserving the Great Barrier Reef and its benefits in perpetuity. The project also established a series of collaborations that will go well beyond the project itself. For example, the

Fellowship team developed a number of satellite tools that led to collaborations with international partners such as NOAA, bringing one of the largest ARC Linkage projects ever awarded to Queensland. The research activities, tools and knowledge leadership that has been delivered through this Fellowship are lasting legacies of the project, as are the many scientific papers, trained students, postdoctoral fellows, international and national partnerships, and organisations which were attracted and enriched by the Fellowship program.


THE MONETARY LEGACY During the period of this Premier’s Fellowship, over $15 million in additional funding was secured from a range of UQ, ARC and other funding sources, and many of these projects are ongoing.

Project Title

Dates

Funding Amount

Parties Involved

Funding Type

ARC Centre of Excellence for Coral Reef Studies

2014-21

$4M (of $12M total awarded to the Premier’s Fellow)

UQ, JCU, ANU

ARC Centre of Excellence

Coral reef metabolism in a rapidly changing climate

2013-18

$3M

GCI

ARC Laureate Fellowship

Catlin Global Reef Record

2013-15

$700,000

Catlin Group Ltd, GCI, Underwater Earth, World Resources Institute, International Union for Conservation of Nature, NOAA and Scripps Institution of Oceanography

Catlin Seaview Survey II (Caribbean and Coral Triangle)

2013-14

$3.326M

Catlin Group Ltd, Google, GCI and Underwater Earth

Next generation satellite tools for understanding change in coral reef ecosystems due to multiple global and local stressors

2012-17

$2.65M

NOAA, AIMS and GBRMPA

Catlin Seaview Survey I (GBR)

2012

$980,000

Catlin Group Ltd, Google, GCI, Underwater Earth

Australian Water & Environment Research Alliance

2012-13

$200,000

UQ and Griffith University

Coral Triangle Alliance

2012-13

$50,000

UQ, JCU, ANU and AIMS

Australian Sea Level Rise University Project (ASLRP)

2012-15

$1.4M

UQ, University of Wollongong and CSIRO

ARC Super Science Fellowship

ARC Centre of Excellence for Coral Reef Studies

2006-13

$4M (of $12M total awarded to the Premier’s Fellow)

UQ, JCU, ANU

ARC Centre of Excellence

Multiscale analysis of the vulnerability of coral reefs to ocean acidification

2009-11

$279,000

UQ, NOAA, Stanford, GBRMPA

ARC Linkage

The Heron Island Climate Change Observatory: An in-situ ocean acidification and carbonate chemistry monitoring platform

2009-10

$190,000

ANU, AIMS, MBARI, GBRMPA

ARC Linkage Infrastructure, Equipment and Facilities

ARC Linkage

Total > $15M

In addition, in a bid to secure future funding for the project, the Premier’s Fellow participated in three retreats organised for top insurance business CEOs by the Catlin Group Ltd in Singapore, Bermuda, and the Turks and Caicos Islands, taking CEOs of major insurance companies into the field and giving lectures on climate change and the Catlin Seaview Survey.

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POST-PREMIER’S FELLOWSHIP: THE NEAR FUTURE

2013–2018

The early part of 2014 saw the Fellow directly involved with several projects that had their inception during the Fellowship period. For example, at the World Ocean Summit in California in February 2014, where key speakers included US Secretary of State John Kerry and HSH Prince Albert II of Monaco, the Fellow presented on topics including the Catlin Seaview Survey. He submitted and went through the IPCC consensus plenary for the final version of Chapter 30 (The Ocean) in Yokohama, Japan in March, ahead of the launch of the Fifth Assessment Report in August at an event in Stockholm, which the Fellow will attend and which will attract the attention of the world’s media. Also in March, a Great Barrier Reef Foundation co-funded workshop on ocean acidification adaptation was held at GCI, with national and international experts participating. In April, the Fellow continued his interaction with KAUST by participating in a Reef Futures Genomics International Consortium (ReFuGe 2020) meeting on coral genomes. The Fellow also gave the opening plenary to 800 politicians and advisors at the Global Ocean Action Summit in The Hague on April 22 (www.globaloceansactionsummit.com).

In 2012 the Australian Research Council awarded the Premier’s Fellow a fiveyear Australian Laureate Fellowship, recognising him as a ‘researcher of international repute who will play a significant, sustained leadership and mentoring role in building Australia’s international competitive research capacity’. The Premier’s Fellowship significantly assisted the Fellow’s career and led to him satisfying the criteria for selection as an Australian Laureate Fellow with a focus on coral reef metabolism in a rapidly changing climate. As he transitions into this new role, the Fellow continues to hold a number of other positions, including:

Other activities and projects linked to the Premier’s Fellowship are continuing into the future, including leading the development and attraction of funding to build the Global Change Institute at The University of Queensland. The collaborative Capturing Coral Reef Ecosystems Services (CCRES) program continued, the second phase of which commenced in January 2014 with the aim of deploying data and results from the first phase into the East Asia-Pacific region. More information on this project is available at www.gci.uq.edu.au/projects/capturingcoral-reef-related-ecosystem-services. In April 2014, the Fellow began teaching on a University of Queensland free online course (1-2 year University level) entitled Tropical Coastal Ecosystems as part of the edX partnership led by Harvard University and MIT. The innovative course introduces the major tropical coastal ecosystems (principally coral reefs, mangroves, sea grass meadows) and explores the problems and solutions that these critical systems face, drawing on research carried out as part of the Premier’s Fellowship. The lecturers involved include CRE collaborator Associate Professor Sophie Dove, and contributors include former CRE PhD student and current postdoctoral researcher Dr Dorothea Bender. Further information on the course is available at http://bit.ly/JEnRkV.

MANAGEMENT MATTERS How the science of the Premier’s Fellowship research program will help decision-makers manage the reef: • This research and discovery will provide reef managers, policy makers and decision-makers with the science and evidence required to make informed, evidence-based management decisions regarding the future sustainability of the Great Barrier Reef – in a time of great change

• Director, Global Change Institute, The University of Queensland. • Deputy Director, ARC Centre for Excellence for Reef Studies. • Chair, Global Partnership for Oceans, Blue Ribbon Panel. • Member of the Scientific Advisory Board of the Biodiversity Research Centre of the Academia Sinica (Taipei, Taiwan). • Member of the Scientific Advisory Board of the Zentrum für Marine Tropenökologie (Bremen, Germany). • Scientific Advisor to the Centre for Ocean Solutions, Stanford University (USA). • Chair of the Technical Advisory Group for the Great Barrier Reef Foundation. • Member, Royal Society of London Marine Advisory Network (MAN). • Member, International Scientific Advisory Committee, Great Barrier Reef Foundation. • Member of the Reef Future Genomics International Consortium. These roles helped the Fellow to build the research and collaborative capacity that made the Premier’s Fellowship a success, and will provide a basis for further advancements in the effort to sustain the Great Barrier Reef during his five-year tenure as an Australian Research Council Laureate Fellow.

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CLOSING STATEMENT FROM THE PREMIER’S FELLOW

The aim of this Fellowship was to build upon my almost 20 years of research experience on the Great Barrier Reef, and to carry out collaborative and innovative research to better understand the resilience of the GBR within the context of ocean warming and acidification. The science and solutions outlined in this Report are a result of five years of research partnerships and engagement with many and varied stakeholders. It is my hope that this research, the tools it generated, and other legacies of this Fellowship will help inform the management and decision-making for the long-term sustainability and resilience of the Great Barrier Reef.

THANKS UQ: Peter Høj Paul Greenfield Max Lu Hugh Possingham Cynthia Riginos Gene Tyson

GCI Board:

State Government: Campbell Newman Andrew Powell Anna Bligh Geoff Garrett

GCI: David Harris Kate Hannah Anna Moloney Melanie King Nicola Da Silva Peter Fogarty Shay O’Farrell Suzanne Pillans Jo Davy

Great Barrier Reef Foundation: John Schubert Claire Hanratty Judith Stewart Eva Abal Theresa Fyffe Shay O’Hara-Smith Emily Saeck Members of Chairman’s Panel GBRMPA: Russel Reichelt David Wachenfeld Roger Beeden Paul Marshall AIMS: Peter Doherty CRE: Sophie Dove Hayley Ware Annamieke Van Den Heuvel Maya Carmi Researchers and students listed on page 34.

Robert Hill Graeme Wood Robyn Williams Margaret Brown Ian Buchanan

NASA: Gene Feldmann NOAA: Mark Eakin William Skirving Gang Lu Al Strong Catlin Group Ltd: Stephen Catlin John Carroll Chip Cunliffe Underwater Earth: Richard Vevers Lorna Parry Christophe Bailhache Ben Glasson Ellen Ray

Catlin Seaview Survey: Sara Naylor Pahia Cooper Susie Green Pim Bongaerts Manuel Gonzalez-Rivero Anjani Ganase Linda Tonk Kyra Hay David Whillas Paul Muir Ana-Teresa Herrera Reveles Michelle Hall Dominic Bryant Norbert Engelbert Jaap Barendrecht CSS research team Institutions involved with FOCE project: The University of Queensland’s instrumentation laboratory, Stanford University, the Carnegie Institution, Monterey Bay Aquarium Research Institute, Australian National University, the University of Adelaide, Israel Oceanographic and Limnological Research Ltd, Scripps Institution of Oceanography Peter Brewer Meg Caldwell Robert Dunbar All visitors to the Premier’s Fellow’s laboratory and participants in workshops associated with the Fellowship.

Panedia: Aaron Spence

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CLOSING STATEMENT PROFESSOR PETER HØJ, VICE-CHANCELLOR AND PRESIDENT, THE UNIVERSITY OF QUEENSLAND

The award of the prestigious 2009-2014 Premier’s Fellowship to Professor Ove Hoegh-Guldberg has yielded a multitude of benefits, making possible many research outcomes that have been outlined in preceding pages. Another important outcome is the return on investment to the people of Queensland who, through the State Government, effectively backed Ove to remain in Queensland, and continue and expand his game-changing work. This has meant that Queensland, home to the world’s largest continuous coral reef system and richly biodiverse terrestrial regions, is also home to one of the world’s most cited climate change scientists, a globally-esteemed marine biologist. This may seem like a natural fit, but it cannot be taken for granted in today’s intensely competitive global market for top academic talent. I therefore thank the people of Queensland for enabling us to keep Ove! The Premier’s Fellowship has helped Ove and UQ attract substantial income to Queensland, including at least $11.1 million in Australian Research Council funding. Among this is $3.19 million for a five-year ARC Laureate Fellowship for Ove, and seven-year funding of $4.4 million for an ARC Centre of Excellence. The Fellowship has also helped buttress Ove’s research as he has led UQ’s Global Change Institute, which was started by a $15 million philanthropic gift in 2010 and has since garnered more than $60 million for research in areas directly relevant to Queensland, such as food security and renewable energy. The certainty of Fellowship funding has also given Ove flexibility to work with global groups such as Catlin (contributing $5.1 million to UQ research) and the World Bank (which is contributing to a new $10.4 million UQ project). All of this bolsters Queensland’s stature as the home of a top 100 global university, which in turn helps the state compete for international students (part of the nation’s fourth-biggest export industry), for top Australian students, and for fine university staff – who collectively make Queensland a more attractive destination for businesses and investors in the knowledge economy. This report does not attempt to make a final tally of the gains from the 2009-2014 Premier’s Fellowship, because they will continue to multiply for many years if not decades. However even the snapshot shown here illustrates the importance of continuing state investment in top researchers, who will remain in or be drawn to Queensland when they have the guarantee of supportive infrastructure and colleagues, along with a culture that celebrates innovation. I commend the Queensland Government for demonstrating that it appreciates the value of research, even in difficult fiscal circumstances. Most of all, I congratulate Ove and his colleagues, students, partners and collaborators. They have created a body of work to enable leaders of communities, industry and government to make well-informed decisions and leave a more positive legacy for future generations.

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REFERENCE LIST & KEY PUBLICATIONS Anthony, KRN, Maynard, JA, Diaz-Pulido, G, Mumby, PJ, Marshall, PA, Cao, L and Hoegh-Guldberg, O (2011) Ocean acidification and warming will lower coral reef resilience. Global Change Biology 17: 1798-1808. Bender, D, Diaz-Pulido, G and Dove, S (accepted). The impact of CO2 emission scenarios and nutrient enrichment on a common coral reef macroalga is modified by temporal effects. Journal of Phycology DOI: 10.1111/jpy.12153 Berkelmans, R, Weeks, SJ and Steinberg, CR (2010) Upwelling linked to warm summers and bleaching on the Great Barrier Reef. Limnology and Oceanography 55(6): 2634-2644. Bongaerts, P, Riginos, C, Ridgway, T, Sampayo, EM and others (2010a) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLOS ONE 5:e10871. Bongaerts, P, Ridgway, T, Sampayo, EM, Hoegh-Guldberg, O (2010b) Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309−327. Bongaerts, P, Riginos, C, Hay, KB, Van Oppen, MJH, Hoegh-Guldberg, O, Dove, S (2011) Adaptive divergence in a scleractinian coral: physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats. BMC Evolutionary Biology 11: 303-303. Bongaerts, P, Bridge, TCL, Kline, DI, Muir, PR, Wallace, CC, Beaman, RJ, Hoegh Guldberg, O (2011) Mesophotic coral ecosystems on the walls of Coral Sea atolls. Coral Reefs 30: 335-335. Bongaerts, P, Sampayo, EM, Bridge, TCL, Ridgway, T, Vermeulen, F, Englebert, N, Webster, JM, Hoegh-Guldberg. O (2011) Symbiodinium diversity in mesophotic coral communities on the Great Barrier Reef: a first assessment. Marine Ecology Progress Series 439: 117-126. Bongaerts, P, Muir, P, Englebert, N, Bridge, TCL, Hoegh-Guldberg, O (2013) Cyclone damage at mesophotic depths on Myrmidon Reef (GBR) Coral Reefs 32(4) 935-935. Crawley, A, Kline, DI, Dunn, SR, Anthony, KRN and Dove, S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora Formosa. Global Change Biology 16(2): 851-863. Diaz-Pulido, G, Anthony, KRN, Kline, DI, Dove, S and Hoegh-Guldberg, O (2010 Interactions between ocean acidification and warming on the morality and dissolution of coralline algae. Journal of Phycology 48(1): 32-39. Doropoulous, C, Ward, S, Diaz-Pulido, G, Hoegh-Guldberg, O and Mumby, PJ (2012 Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions. Ecology Letters 15: 338-346. Dove, SG, Kline, DI, Pantos, O, Angly, FE, Tyson, GW, Hoegh-Guldberg, O (2013) Future reef decalcification under business-as-usual CO2 emission scenario. Proceedings of the National Academy of Sciences of the USA 110(38): 15342-15347. Dunn, SR, Pernice, M, Green, K, Hoegh-Guldberg, O and Dove, SG (2012) Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians: Are the batteries of the reef going to run out? PLOS ONE 7(7): e39024.

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Fang, JKH, Schoenberg, CHL, Kline, DI, Hoegh-Guldberg, O and Dove, S (2013) Methods to quantify components of the excavating sponge Cliona orientalis Thiele 1900. Marine Ecology - An Evolutionary Perspective 34(2): 193-206. Fang, JKH, Mello-Athayde, MA, Schönberg, CHL, Kline, DI, Hoegh-Guldberg, O, Dove, S (2013) Sponge biomass and bioerosion rates increase under ocean warming and acidification. Global Change Biology, 19(12): 3581-3591. Fang, JKH, Schönberg, CHL, Mello-Athayde, MA, Hoegh-Guldberg, O and Dove, S (2014) Effects of ocean warming and acidification on the energy budget of an excavating sponge. Global Change Biology, 20:1043-1054. Fielding, KS, Head, BW, Laffan, W, Western, M and Hoegh-Guldberg, O (2012) Australian politicians’ beliefs about climate change: political partisanship and political ideaology. Environmental Politics 21(5), 712-733. Frieler, K, Meinshausen, M, Golly, A, Mengel, M, Lebek, K, Donner, S and Hoegh Guldberg, O (2012) Limiting global warming to 2˚C is unlikely to save most coral reefs. Nature Climate Change 3(2), 165-170. Great Barrier Reef Foundation (2010) Resilient Coral Reefs Successfully Adapting to Climate Change – A Research Portfolio, Great Barrier Reef Foundation, ISBN: 978-0-646-54785-5 Published 2010. The Great Barrier Reef Foundation Attributes Working Group paper. Great Barrier Reef Foundation (2010) Research Portfolio - Project Summary, Great Barrier Reef Foundation, ISBN: 978-0-646-54785-5 Published 2010. The Great Barrier Reef Foundation Attributes Working Group paper. Hegerl, GC, Hoegh-Guldberg, O, Casassa, G, Hoerling, M, Kovats, S, Parmesan, C, Pierce, D and Stott, P (2010) Good practice guidance paper on detection and attribution related to anthropogenic climate change. IPCC, WMO Switzerland. Hoegh-Guldberg, O and Bruno, JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328: 1523-1528. Hoegh-Guldberg, O, Aqorau, T, Arnason, R, Chansiri, T, Del Rio, N, Demone, H, Earle, S Feeley, MH, Gutierrez, D, Hilborn, R, Ishil, N, Lischewski, C, Lubchenco, J, Anh Nguyen, K, Obura, D, Payet, R, Neroni Slade, HE, Tanzer, J, Williams, JH, Wright, DJ, Xu, J (2013) Indispensable ocean: Aligning ocean health and well-being. Guidance from the Blue Ribbon Panel to the Global Partnership for Oceans. World Bank, Washington DC. 44pp. Kaniewska, P, Campbell, PR, Kline, DI, Rodriguez-Lanetty, M, Miller, DJ, Dove, S and Hoegh-Guldberg, O (2012) Major cellular and physiological impacts of ocean acidification on a reef building coral. PLOS ONE 7(4):e34659. Kline, DI, Teneva, L, Schneider, K, Miard, T, Chai, A, Marker, M, Headley, K, Opdyke, B, Nash, M, Valetich, M, Caves, JK, Russell, BD, Connell, SD, Kirkwood, BJ, Brewer, P, Peltzer, E, Silverman, J, Caldeira, K, Dunbar, RB, Koseff, JR, Monismith, SG, Mitchell, BG, Dove, S and Hoegh-Guldberg, O (2012) A shortterm in situ CO 2 enrichment experiment on Heron Island (GBR). Nature Scientific Reports 2: 413 doi: 10.1038/srep00413. LaJeunesse, TC, Pettay, DT, Sampayo, EM, Phongsuwan, N, Brown, B, Obura, DO, Hoegh-Guldberg, O and Fitt, WK (2010) Long-standing environmental conditions, geographic isolation and host–symbionts specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. Journal of Biogeography 37: 785-800. Middlebrook, R, Anthony, KRN, Hoegh-Guldberg, O and Dove, S (2012) Thermal priming affects symbiont photosynthesis but does not alter bleaching susceptibility in Acropora millepora. Journal of Experimental Marine Biology and Ecology 432: 64-72.

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Morton, SR, Hoegh-Guldberg O, Lindenmayer, DB, Olson, MH, Hughes, L, McCulloch, MT, McIntyre, S, Nix, HA, Prober, SM, Saunders, DA, Andersen, AN, Burgman, MA, Lefroy, EC, Lonsdale, WM, Lowe, I, McMichael, AJ, Parslow, JS, Steffen, W, Williams, JE and Woinarski, JCZ (2009) The big ecological questions inhibiting effective environmental management in Australia. Austral Ecology, 34, 1-9. Pelejero, C, Calvo, E and Hoegh-Guldberg, O (2010) Paleo-perspectives on ocean acidification. Trends in Ecology and Evolution 25: 332-344. Pernice, M, Van Den Heuvel, A, Koop, C, Domart-Coulon, I, Meibom, A, Hoegh Guldberg, O and Dove, S (2011) A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME Journal 6(7): 1314-1324. Rau, G, McLeod, E and Hoegh-Guldberg, O (2012) The need for new ocean conservation strategies in a high CO2 world. Nature Climate Change 2(10), 720-724. Redondo-Rodriguez, A, Weeks, SJ, Berkelmans, R, Hoegh-Guldberg, O and Lough, JM (2012) Climate variability of the Great Barrier Reef in relation to the tropical Pacific and El Ni単o-Southern Oscillation, Marine and Freshwater Research 63(1): 34-47. Reyes-Nivia, C, Diaz-Pulido, G, Kline, D, Hoegh-Guldberg, O and Dove, S (2013) Ocean acidification and warming scenarios increase microbioerosion of coral skeletons. Global Change Biology 19(6): 1919-1929. Rosic, NN, Pernice, M, Dove, S, Dunn, S and Hoegh-Guldberg, O (2011) Gene expression profiles of cytostolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching. Cell Stress and Chaperones 16(1): 69-80. Tonk, L*, Bongaerts P*, Sampayo EM, Hoegh-Guldberg O (2013) SymbioGBR: a web-based database of Symbiodinium associated with cnidarian hosts on the Great Barrier Reef. BMC Ecology 13:7. (*equal contributors). Tonk, L, Sampayo, EM, Weeks, S, Magno-Canto, M and Hoegh-Guldberg, O (2013) Host-specific interactions with environmental factors shape the distribution of Symbiodinium across the Great Barrier Reef. PLOS ONE 8(7) 1-14. Veal, CJ, Carmi, M, Dishon, G, Sharon, Y, Michael, K, Hoegh-Guldberg, O, Tchernov, D and Fine, M (2010) Shallow water wave lensing in Coral Reefs: A physical and biological case study. Journal of Experimental Biology 213, 4304-4312. Vitt, P, Havens, K and Hoegh-Guldberg, O (2009) Assisted migration: part of an integrated conservation strategy. Trends in Ecology and Evolution 24, 473-447. Weeks, SJ, Bakun, A, Steinberg, CR, Brinkman, R and Hoegh-Guldberg, O (2010) The Capricorn Eddy: a prominent driver of the ecology and future of the southern Great Barrier Reef Coral Reefs 29(4) 975-985. Weeks, SJ, Werdell, PJ, Schaffelke, B, Canto, M, Lee, ZP, Wilding, JG and Feldman, GC (2012) Satellite-derived photic depth on the Great Barrier Reef: Spatiotemporal patterns of water clarity. Remote Sensing 4(12): 3781-3795.

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FOOTNOTE REFERENCES ABARE (2006) Australian commodity statistics 2006, Canberra, 367pp. Armstrong, RA, Singh, H, Torres, J, Nemeth, RS, Can, A, Roman, C, Eustice, R, Riggs, L, Garcia-Molinar, G (2006) Characterizing the deep insular shelf coral reef habitat of the Hind Bank Marine Conservation District (US Virgin Islands) using the Seabed autonomous underwater vehicle. Continental Shelf Research 26:194-205. Barry, J, Hall-Spencer, J and Tyrrell, T (2010) in Guide to best practices for ocean acidification research and data reporting (eds. Riebesell, U, Fabry, VJ, Hansson, L and Gattuso, JP) Publications Office of the European Union, 123–136. Barshis, DJ, Stillman, JH, Gates, RD, Toonen, RJ, Smith, LW, Birkeland, C (2010) Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Molecular Ecology 19:1705-1720. Bongaerts, P, Riginos, C, Ridgway, T, Sampayo, EM, van Oppen, MJH, Englebert, N, Vermeulen, F, and Hoegh-Guldberg, O (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLOS ONE 5:e10871. Bruno, JF and Selig, ER (2007) Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLOS ONE 2:e711. De’ath, G, Fabricius, KE, Sweatman, H and Puotinen, M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences of the USA, 109(44):17995-17999. Deloitte Access Economics (2013) Economic contribution of the Great Barrier Reef. Great Barrier Reef Marine Park Authority, Townsville. Finney, JC, Pettay, D, Sampayo, E, Warner, M, Oxenford, H, LaJeunesse, T (2010) The relative significance of host-habitat, depth, and geopgraphy on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microbial Ecology 60:250-263. Glynn, PW (1996) Coral reef bleaching: facts, hypotheses and implications. Global Change Biology 2:495-509. LaJeunesse, TC, Loh, WKW, van Woesik, R, Hoegh-Guldberg, O, Schmidt, GW, Fitt, WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnology & Oceanography 48:2046-2054. LaJeunesse, TC, Bhagooli, R, Hidaka, M, DeVantier, L, Done, T, Schmidt, GW, Fitt, WK, Hoegh-Guldberg, O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Marine Ecology Progress Series 284:147-161. Riegl, B and Piller, WE (2003) Possible refugia for reefs in time of environmental stress. International Journal of Earth Sciences 92:520-531. Walz, PM, Kirkwood, WJ, Peltzer, ET, Hester, KC and Brewer, PG (2008) Creating controlled CP2 perturbation experiments on the seafloor – Development of FOCE techniques. Oceans 2008 – Mts/Ieee Kobe Techno-Ocean, Vols. 1–2:750–753. Weeks, S, Werdell, PJ, Schaffelke, B, Canto, M, Lee, Z, Wilding, JG & Feldman, GC 2012. Satellite-derived photic depth on the Great Barrier Reef: Spatiotemporal patterns of water clarity. Remote Sensing 4:3781-3795.

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IMAGE CREDITS Page Credit Cover

Catlin Seaview Survey

1

Ove Hoegh-Guldberg

2

Davey Kline

3

Linda Tonk

4

Biodiversity Heritage Library

6

Ove Hoegh-Guldberg

7

Ove Hoegh-Guldberg

12

Linda Tonk

13

Ove Hoegh-Guldberg

15

Ove Hoegh-Guldberg

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(a and b) Sophie Dove

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Catlin Seaview Survey

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(a) UQ OceanSpace Group (b) Weeks et al. 2012

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Ove Hoegh-Guldberg

22

Olga Pantos

23

Selina Ward

24

Ove Hoegh-Guldberg

25

Olga Pantos

26

Mathieu Pernice

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(a) Ove Hoegh-Guldberg (b) Pim Bongaerts

30

Ove Hoegh-Guldberg

34

Catlin Seaview Survey

37

Catlin Seaview Survey

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Great Barrier Reef Foundation

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Fe Lumsdaine, Lumsdaine Photography

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Catlin Seaview Survey

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Biodiversity Heritage Library

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Ove Hoegh-Guldberg

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GLOSSARY Algorithm: a step-by-step procedure for calculations, applied for tasks such as data processing. Apoptosis: a form of programmed cell death that is mediated by an intracellular program and involves controlled, predictable steps, in contrast to necrosis, which is caused by external factors such as infection or injury. Biodiversity: the variety of plant and animal life in the world or in a particular habitat, a high level of which is usually considered to be important and desirable. Climate change: any change in climate over time, whether due to natural variability or as a result of human activity. Coral bleaching: the loss of coral colour, either due to the expulsion of intracellular Symbiodinium cells or the loss of pigments from the symbionts, which both lead to the host tissue becoming transparent. Coral reef calcification: the deposition of a matrix of calcium carbonate (aragonite) by corals and other reef organisms, including coralline algae. Community metabolism: the sum total of the chemical processes occurring in a group of living organisms whereby some substances are broken down to yield energy for vital processes and other substances necessary for life are synthesised. Crown of thorns starfish: The crown-of-thorns starfish, Acanthaster planci, is a large, multiple-armed starfish (or seastar) that usually preys upon hard, or stony, coral polyps (Scleractinia). The crown-of-thorns receives its name from venomous thornlike spines that cover its upper surface, or the crown of thorns. It is one of the largest sea stars in the world. Cyanobacteria: bacteria that obtain their energy through photosynthesis. DNA sequencing: determination of the precise order of nucleotides (adenine, guanine, thymine, cytosine) along a strand of DNA. El Niño: the warm oceanic phase of the El Niño-Southern Oscillation, which refers to variations in the temperature of the surface of the tropical eastern Pacific Ocean and in air surface pressure in the tropical western Pacific, and results in the periodic development of a band of warm ocean water off the Pacific coast of South America. Endoliths: generally slow-growing microbial organisms, including fungi, algae and bacteria, that live within the calcium carbonate skeletons of live and dead corals. Eutrophication: the process by which a body of water becomes over-enriched with nutrients, either naturally or by pollution, and which leads to deficiency in dissolved oxygen (hypoxia). Foraminifera: a group of primarily marine organisms that typically produce an external test (shell) made of calcium carbonate, making them useful for studies of past and present climate conditions and change. Fore-reef: the sloping area of a reef that is closest to the open ocean and usually has the highest abundance and diversity of corals in a particular reef system. Genetic marker: a piece of genetic material (usually a gene or DNA sequence) with a known location on a chromosome that can be used in a range of laboratory analyses to delineate cells, individuals, populations or species. Greenhouse gases (GHGs): gases in the Earth’s atmosphere that absorb and emit radiation within the thermal infrared range and are thus fundamental to the greenhouse effect, which greatly impacts the Earth’s temperature.

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GLOSSARY Host-symbionts An organism hosting a smaller living organism. The smaller organism derives a benefit (such as extracting nutrients etc) whereas the host may or may not derive any benefit. Intergovernmental Panel for Climate Change (IPCC): a scientific body under the auspices of the United Nations that reviews and assesses the most recent scientific, technical and socio-economic information produced worldwide relevant to the understanding of climate change. Mesocosm An experimental tool that brings a small part of the natural world under controlled conditions. NanoSIMS: a method for ultra high-resolution chemical imaging using mass spectrometry, which can be used, for example, to examine cellular structures. Ocean acidification: the continuing process whereby the pH of the oceans is decreasing, as a result of increasing carbon dioxide concentration in the atmosphere and its uptake by the oceans. Photosynthesis: the process used by plants and other organisms to convert light energy (usually from the sun) into chemical energy in the form of organic compounds. Primary production: the synthesis of organic compounds, such as glucose, from atmospheric or aqueous carbon dioxide, primarily through photosynthesis. Pulse amplitude modulated (PAM) fluorometry: a widely applied technique for measuring the photosynthetic performance of Symbiodinium spp. and thereby obtaining a quantitative measure of photoinactivation, which occurs during coral bleaching. Reactive oxygen species (ROS): chemically reactive molecules containing oxygen that are a normal byproduct of metabolism but which may, during times of environmental stress, increase dramatically in abundance and damage cell structures. Remote sensing: the use of aerial sensor technologies to acquire information about an object or phenomenon without making physical contact, instead making use of propagated signals that may be passive (e.g., sunlight) or active (e.g., emitted from a satellite). Resilience: the ability to withstand or return to the original form following stress or disturbance. Scleractinian corals Also known as stony or hard corals, these are marine corals with a hard skeleton. They secrete calcium carbonate to form a skeleton and are one of the primary reef builders in coral systems. Symbiosis: the prolonged, intimate association of two or more species, which may – as is the case for corals and Symbiodinium – be mutualistic, meaning both species benefit. Upwelling: an oceanographic phenomenon that involves wind-driven motion of dense, cooler and usually nutrient-rich ocean water up through the water column, where it replaces the generally nutrient-depleted, warmer surface water.

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MAJOR SPONSORS

GLOBAL CHANGE INSTITUTE The University of Queensland St Lucia QLD 4072 Australia T +61 7 3443 3100 E gci@uq.edu.au W www.gci.uq.edu.au

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