Re-evaluation of the emergence of reef coral diseases based on the importance of ciliate infections

Lead Research Organisation: Newcastle University
Department Name: Sch of Biology

Abstract

Global CO2 emissions are produced mainly by western economies in the temperate zones, however the impacts of climate change are mainly being seen at the climatic extremes of the poles and tropical zones. While the poles are scarcely populated, coral reefs play a vital role in directly supporting at least 500 million people worldwide, despite only representing 0.1% of the world's ocean area. The Coral Triangle in south-east Asia alone includes over 100 million people who are almost entirely dependent on coastal resources. Coral diseases have contributed significantly to global declines in coral reefs (some scientists put the figure at about 40% loss over the last 40 years), leaving few options for coastal peoples of developing countries. Many scientists have linked the emergence of coral diseases to climate change that affects the overall health and disease resistance of the host as well as promoting the activity of some pathogens. However, our understanding of coral diseases is driven mainly on the assumption that most are caused by bacteria. Following a general lack of success in identifying causal agents using traditional culture-based approaches, our group began using modern culture-independent methods based on analysing bacterial DNA in environmental samples over ten years ago. While this work has been successful in advancing understanding of the microbial ecology of several common coral diseases, there have been few breakthroughs in determining the causal agents of disease. More recently, working on a NERC-funded project to investigate temperature stress effects on coral susceptibility to disease, we have discovered that several of the most important types of coral disease are associated with mass infections by protist pathogens, as well as bacteria. The protists (ciliates similar to Paramecium) act as pathogens kill the coral by ingesting the tissues. Ongoing work will address the relative changes in ciliate and bacterial pathogen populations during the disease process, but there is no doubt that the ciliates are important agents in disease transmission and pathology and may be the primary pathogens. We have also shown that these diseases are highly temperature-dependent, which may explain the global increase in disease prevalence in the last 20-30 years. The proposed study therefore addresses the ciliate diseases specifically and will test whether they are acting as primary pathogens (causal agents) of the disease or secondary, opportunistic pathogens invading the tissues after another primary (possibly bacterial) pathogen. To do this we will apply traditional Koch's postulates, isolating the potential pathogens in culture and innoculating healthy corals in controlled incubations. We will also survey a number of locations worldwide to determine whether diseases with very similar signs are also associated with ciliates. Some of these diseases have caused serious ecological impacts, for example one (White Band Disease) has elimnated elkhorn coral as the dominant coral species in the whole Caribbean region. Since the diseases are highly temperature-dependent, we will conduct experiments to allow us to more accurately model the impacts of future climate change scenarios on coral mortality. The experiments will distinguish the effects of temperature on increased pathogen activity and changes in host coral susceptibility. We will further investigate the changes in susceptibility to determine the likely mechanisms by which corals resist ciliate infections under healthy conditions. Together, these studies will allow a mechanistic understanding of how temperature affects the disease process, so we can model the effects of future climate change, rather than just model past history. The final synthesis of the research will allow us to fundamentally re-evaluate the emergence of coral diseases in the last 20-30 years as well as predict future changes and propose potential management solutions.

Publications

10 25 50
 
Description Coral disease epizootics were first observed in the Caribbean as a significant ecological impact in the early 1970s. Since then, coral reefs have declined by over 80% in that region. Similar epizootics have since (in the 2000s) spread to the vastly greater area of the Indo-Pacific region, threatening livelihoods and natural coastal defenses of millions of vulnerable people. In this study we have confirmed the involvement of ciliates (single-celled eukaryotes) in a number of coral diseases, including the aptly-named 'white syndrome' that causes acute tissue loss in reef corals. In particular, a histophagous (tissue-eating) ciliate, Philaster sp., has been shown to occur consistently in all samples of actively-progressing disease lesions of white syndrome from the Indo-Pacific and both White Plague (WP) and White Band Disease (WBD) in the Caribbean. Our most recent studies using selective antibiotic treatment to knock out different subsets of the microbial communities associated with WBD suggest that both the histophagous ciliate and one or more of a group of potential bacterial pathogens are causal agents of the disease. Whether tissue disruption by the ciliate enables the bacterial pathogen(s) to infiltrate the tissues, or bacterial infection reduces the coral host defenses against ciliate attack at the onset of the disease has yet to be determined.
Exploitation Route The work is being applied through a number of collaborations with public and commercial aquarium operators, as well as the Coral Aquarist Research Network (CARN), a NERC-funded Knowledge-Exchange network led by the University of Essex. As well as the commercial implications for aquarists, coral aquaculture is emerging as a means of rehabilitating and restoring reefs damaged by human impacts and diseases are a serious threat to such operations, with frequent catastrophic mortalities in culture systems. Improving husbandry and reducing losses to disease may also reduce the collection of wild corals and the environmental impacts due to the global aquarium trade. While climate change appears to increase disease prevalence and epizootic outbreaks on coral reefs, the emergence of the WBD epizootic in the Caribbean predated warming in the region due to climate change. Other factors such as novel pathogen introductions must have therefore played a role. Our work on the genetics of the ciliate pathogen may help elucidate the indroduction and spread of different strains of this important pathogen globally. In certain circumstances (such as public aquaria, commercial aquaria and in very small 'iconic' marine protected areas), we have shown that application of antibiotics is a potential treatment option for the white syndrome diseases. Knowing the pathogens involved, including the fact that multiple pathogens can and do contribute to white syndrome pathogenesis, has allowed us to develop suitable treatment options. Importantly, this latter finding indicates that traditional tests of Henle-Koch's postulates cannot be successful and our results require both a re-evaluation of previous studies that have relied on this method to identify 'the' pathogen associated with various coral diseases, but also calls for a new experimental approach amongst the academic community assessing causality in coral diseases.
Sectors Environment

URL http://www.ncl.ac.uk/biology/staff/profile/john.bythell#tab_profile
 
Description In addition to influencing the academic community, this project has interacted strongly with the public and professional aquarium industry via 1) a dedicated website providing scientific information on coral diseases, 2) interaction with a NERC Knowledge Exchange network (Coral Aquarist-Researcher Network), and 3) engagement and collaboration with industry (London Zoo, Horniman Museum Aquarium, London, SeaLife Centre and various overseas aquariums). In addition, both the PI and PDRA (now lecturer) have interacted with conservation organisations via the Zoological Society of London annual Reef Conservation UK conference and related activities. Three targeted industry-specific journal publications have been produced with industrial collaborator co-authors (see Publications) in addition to front-line academic publications.
First Year Of Impact 2011
Sector Environment,Culture, Heritage, Museums and Collections
Impact Types Societal,Economic

 
Description 'The Big UK Experiment' - a workshop and training programme for UK aquarists
Geographic Reach National 
Policy Influence Type Influenced training of practitioners or researchers
Impact Improvements in aquarist practices leading to lower mortality rates and less wild harvest of corals.
URL http://carnuk.org/
 
Description Aquarium coral diseases web site 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Web site established to aid commercial, private and public aquarium operators to identify coral diseases and provide potential treatments where appropriate.



http://aquariumcoraldiseases.weebly.com

This site has received 32,000 unique site visits (2012 to 2015)
Year(s) Of Engagement Activity 2012,2013,2014,2015
URL http://aquariumcoraldiseases.weebly.com
 
Description Aquarium coral diseases; introducing a new website for identification. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Workshop and presentation as part of NERC KE Coral Aquarist Research Network (CARN) "The Big Experiment"

Further dialogue and collaboration with aquarium industry personnel
Year(s) Of Engagement Activity 2012
 
Description First incidence of skin cancer found in fish 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? Yes
Geographic Reach International
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Planet Earth (NERC) online news story on our publication 'Evidence of Melanoma in Wild Marine Fish Populations' (PLOS One)

Well-cited publication
Year(s) Of Engagement Activity 2012,2013
 
Description Science Uncovered Event - Great North Museum 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact 1081 members of the general public attended the 'Science Uncovered' event at the Great North Museum - mirroring events going on at the Natural History Museum and elsewhere on the same night. The event was an interactive display related to impacts of climate change on coral reefs and featured a demonstration of ocean acidification, VR goggle video of coral reef survey and coral skeleton exhibits + posters.
Year(s) Of Engagement Activity 2017
URL https://www.evensi.uk/science-uncovered-great-north-museum-hancock/219601943