238 results on '"Bette L. Willis"'
Search Results
2. Deciphering Coral Disease Dynamics: Integrating Host, Microbiome, and the Changing Environment
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Rebecca Vega Thurber, Laura D. Mydlarz, Marilyn Brandt, Drew Harvell, Ernesto Weil, Laurie Raymundo, Bette L. Willis, Stan Langevin, Allison M. Tracy, Raechel Littman, Keri M. Kemp, Phoebe Dawkins, Katherine C. Prager, Melissa Garren, and Joleah Lamb
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coral ,reefs ,disease ,microbiome ,dysbiosis ,climate change ,Evolution ,QH359-425 ,Ecology ,QH540-549.5 - Abstract
Diseases of tropical reef organisms is an intensive area of study, but despite significant advances in methodology and the global knowledge base, identifying the proximate causes of disease outbreaks remains difficult. The dynamics of infectious wildlife diseases are known to be influenced by shifting interactions among the host, pathogen, and other members of the microbiome, and a collective body of work clearly demonstrates that this is also the case for the main foundation species on reefs, corals. Yet, among wildlife, outbreaks of coral diseases stand out as being driven largely by a changing environment. These outbreaks contributed not only to significant losses of coral species but also to whole ecosystem regime shifts. Here we suggest that to better decipher the disease dynamics of corals, we must integrate more holistic and modern paradigms that consider multiple and variable interactions among the three major players in epizootics: the host, its associated microbiome, and the environment. In this perspective, we discuss how expanding the pathogen component of the classic host-pathogen-environment disease triad to incorporate shifts in the microbiome leading to dysbiosis provides a better model for understanding coral disease dynamics. We outline and discuss issues arising when evaluating each component of this trio and make suggestions for bridging gaps between them. We further suggest that to best tackle these challenges, researchers must adjust standard paradigms, like the classic one pathogen-one disease model, that, to date, have been ineffectual at uncovering many of the emergent properties of coral reef disease dynamics. Lastly, we make recommendations for ways forward in the fields of marine disease ecology and the future of coral reef conservation and restoration given these observations.
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- 2020
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3. Co‐dynamics of Symbiodiniaceae and bacterial populations during the first year of symbiosis with Acropora tenuis juveniles
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Kate M. Quigley, Carlos Alvarez Roa, Greg Torda, David G. Bourne, and Bette L. Willis
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16S rRNA gene ,co‐occurrence ,coral ,coral‐associated bacteria ,ITS2 rDNA gene ,juvenile ,Microbiology ,QR1-502 - Abstract
Abstract Interactions between corals and their associated microbial communities (Symbiodiniaceae and prokaryotes) are key to understanding corals' potential for and rate of acclimatory and adaptive responses. However, the establishment of microalgal and bacterial communities is poorly understood during coral ontogeny in the wild. We examined the establishment and co‐occurrence between multiple microbial communities using 16S rRNA (bacterial) and ITS2 rDNA (Symbiodiniaceae) gene amplicon sequencing in juveniles of the common coral, Acropora tenuis, across the first year of development. Symbiodiniaceae communities in juveniles were dominated by Durusdinium trenchii and glynnii (D1 and D1a), with lower abundances of Cladocopium (C1, C1d, C50, and Cspc). Bacterial communities were more diverse and dominated by taxa within Proteobacteria, Cyanobacteria, and Planctomycetes. Both communities were characterized by significant changes in relative abundance and diversity of taxa throughout the year. D1, D1a, and C1 were significantly correlated with multiple bacterial taxa, including Alpha‐, Deltra‐, and Gammaproteobacteria, Planctomycetacia, Oxyphotobacteria, Phycisphaerae, and Rhizobiales. Specifically, D1a tended to associate with Oxyphotobacteria and D1 with Alphaproteobacteria, although these associations may represent correlational and not causal relationships. Bioenergetic modeling combined with physiological measurements of coral juveniles (surface area and Symbiodiniaceae cell densities) identified key periods of carbon limitation and nitrogen assimilation, potentially coinciding with shifts in microbial community composition. These results demonstrate that Symbiodiniaceae and bacterial communities are dynamic throughout the first year of ontology and may vary in tandem, with important fitness effects on host juveniles.
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- 2020
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4. Heritability of the Symbiodinium community in vertically- and horizontally-transmitting broadcast spawning corals
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Kate M. Quigley, Bette L. Willis, and Line K. Bay
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Medicine ,Science - Abstract
Abstract The dinoflagellate-coral partnership influences the coral holobiont’s tolerance to thermal stress and bleaching. However, the comparative roles of host genetic versus environmental factors in determining the composition of this symbiosis are largely unknown. Here we quantify the heritability of the initial Symbiodinium communities for two broadcast-spawning corals with different symbiont transmission modes: Acropora tenuis has environmental acquisition, whereas Montipora digitata has maternal transmission. Using high throughput sequencing of the ITS-2 region to characterize communities in parents, juveniles and eggs, we describe previously undocumented Symbiodinium diversity and dynamics in both corals. After one month of uptake in the field, Symbiodinium communities associated with A. tenuis juveniles were dominated by A3, C1, D1, A-type CCMP828, and D1a in proportional abundances conserved between experiments in two years. M. digitata eggs were predominantly characterized by C15, D1, and A3. In contrast to current paradigms, host genetic influences accounted for a surprising 29% of phenotypic variation in Symbiodinium communities in the horizontally-transmitting A. tenuis, but only 62% in the vertically-transmitting M. digitata. Our results reveal hitherto unknown flexibility in the acquisition of Symbiodinium communities and substantial heritability in both species, providing material for selection to produce partnerships that are locally adapted to changing environmental conditions.
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- 2017
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5. Reduced diversity and stability of coral-associated bacterial communities and suppressed immune function precedes disease onset in corals
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F. Joseph Pollock, Joleah B. Lamb, Jeroen A. J. M. van de Water, Hillary A. Smith, Britta Schaffelke, Bette L. Willis, and David G. Bourne
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coral microbes ,disease ,immunity ,marine infrastructure ,bacteria ,white syndrome ,Science - Abstract
Disease is an emerging threat to coral reef ecosystems worldwide, highlighting the need to understand how environmental conditions interact with coral immune function and associated microbial communities to affect holobiont health. Increased coral disease incidence on reefs adjacent to permanently moored platforms on Australia's Great Barrier Reef provided a unique case study to investigate environment–host–microbe interactions in situ. Here, we evaluate coral-associated bacterial community (16S rRNA amplicon sequencing), immune function (protein-based prophenoloxidase-activating system), and water quality parameters before, during and after a disease event. Over the course of the study, 31% of tagged colonies adjacent to platforms developed signs of white syndrome (WS), while all control colonies on a platform-free reef remained visually healthy. Corals adjacent to platforms experienced significant reductions in coral immune function. Additionally, the corals at platform sites that remained visually healthy throughout the study had reduced bacterial diversity compared to healthy colonies at the platform-free site. Interestingly, prior to the observation of macroscopic disease, corals that would develop WS had reduced bacterial diversity and significantly greater community heterogeneity between colonies compared to healthy corals at the same location. These results suggest that activities associated with offshore marine infrastructure impacts coral immunocompetence and associated bacterial community, which affects the susceptibility of corals to disease.
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- 2019
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6. Elevated CO2 Has Little Influence on the Bacterial Communities Associated With the pH-Tolerant Coral, Massive Porites spp.
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Paul A. O’Brien, Hillary A. Smith, Stewart Fallon, Katharina Fabricius, Bette L. Willis, Kathleen M. Morrow, and David G. Bourne
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ocean acidification ,microbiome ,coral ,volcanic seep ,Porites ,Microbiology ,QR1-502 - Abstract
Ocean acidification (OA) as a result of increased anthropogenic CO2 input into the atmosphere carries consequences for all ocean life. Low pH can cause a shift in coral-associated microbial communities of pCO2-sensitive corals, however, it remains unknown whether the microbial community is also influenced in corals known to be more tolerant to high pCO2/low pH. This study profiles the bacterial communities associated with the tissues of the pCO2-tolerant coral, massive Porites spp., from two natural CO2 seep sites in Papua New Guinea. Amplicon sequencing of the hypervariable V3-V4 regions of the 16S rRNA gene revealed that microbial communities remained stable across CO2 seep sites (pH = 7.44–7.85) and adjacent control sites (ambient pH = 8.0–8.1). Microbial communities were more significantly influenced by reef location than pH, with the relative abundance of dominant microbial taxa differing between reefs. These results directly contrast with previous findings that increased CO2 has a strong effect on structuring microbial communities. The stable structure of microbial communities associated with the tissues of massive Porites spp. under high pCO2/low pH conditions confirms a high degree of tolerance by the whole Porites holobiont to OA, and suggest that pH tolerant corals such as Porites may dominate reef assemblages in an increasingly acidic ocean.
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- 2018
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7. Coral Restoration Effectiveness: Multiregional Snapshots of the Long-Term Responses of Coral Assemblages to Restoration
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Margaux Y. Hein, Roger Beeden, Alastair Birtles, Naomi M. Gardiner, Thomas Le Berre, Jessica Levy, Nadine Marshall, Chad M. Scott, Lisa Terry, and Bette L. Willis
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coral assemblages ,coral restoration ,effectiveness ,monitoring ,Biology (General) ,QH301-705.5 - Abstract
Coral restoration is rapidly becoming a mainstream strategic reef management response to address dramatic declines in coral cover worldwide. Restoration success can be defined as enhanced reef functions leading to improved ecosystem services, with multiple benefits at socio-ecological scales. However, there is often a mismatch between the objectives of coral restoration programs and the metrics used to assess their effectiveness. In particular, the scales of ecological benefits currently assessed are typically limited in both time and space, often being limited to short-term monitoring of the growth and survival of transplanted corals. In this paper, we explore reef-scale responses of coral assemblages to restoration practices applied in four well-established coral restoration programs. We found that hard coral cover and structural complexity were consistently greater at restored compared to unrestored (degraded) sites. However, patterns in coral diversity, coral recruitment, and coral health among restored, unrestored, and reference sites varied across locations, highlighting differences in methodologies among restoration programs. Altogether, differences in program objectives, methodologies, and the state of nearby coral communities were key drivers of variability in the responses of coral assemblages to restoration. The framework presented here provides guidance to improve qualitative and quantitative assessments of coral restoration efforts and can be applied to further understanding of the role of restoration within resilience-based reef management.
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- 2020
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8. Temperature and Water Quality-Related Patterns in Sediment-Associated Symbiodinium Communities Impact Symbiont Uptake and Fitness of Juveniles in the Genus Acropora
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Kate M. Quigley, Line K. Bay, and Bette L. Willis
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Symbiodinium ,free-living ,juvenile ,uptake ,symbiosis ,coral reefs ,Science ,General. Including nature conservation, geographical distribution ,QH1-199.5 - Abstract
The majority of corals acquire their photo-endosymbiont Symbiodinium from environmental sources anew each generation. Despite the critical role that environmental availability of Symbiodinium plays in the potential for corals to acclimate and adapt to changing environments, little is known about the diversity of free-living Symbiodinium communities and how variation in these communities influences uptake and in hospite communities in juvenile corals. Here we characterize Symbiodinium community diversity in sediment samples collected from eight reefs representing latitudinal and cross-shelf variation in water quality and temperature regimes. Sediment-associated Symbiodinium communities were then compared to in hospite communities acquired by A. tenuis and A. millepora juveniles following 11–145 days of experimental exposure to sediments from each of the reefs. Communities associated with juveniles and sediments differed substantially, with sediments harboring four times more unique OTUs than juveniles (1,125 OTUs vs. 271). Moreover, only 10.6% of these OTUs were shared between juveniles and sediments, indicating selective uptake by acroporid juveniles. The diversity and abundance of Symbiodinium types differed among sediment samples from different temperature and water quality environments. Symbiodinium communities acquired by juveniles also differed among the sediment treatments, despite juveniles having similar parentage. Moreover, Symbiodinium communities displayed different rates of infection, mortality, and photochemical efficiencies, important traits for coral fitness. This study demonstrates that the biogeography of free-living Symbiodinium types found within sediment reservoirs follows patterns along latitudinal and water quality environmental gradients on the Great Barrier Reef. We also demonstrate a bipartite strategy for Symbiodinium uptake by juvenile corals of two horizontally-transmitting acroporid species, whereby uptake is selective within the constraints of environmental availability.
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- 2017
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9. Coral larvae for restoration and research: a large-scale method for rearing Acropora millepora larvae, inducing settlement, and establishing symbiosis
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F. Joseph Pollock, Sefano M. Katz, Jeroen A.J.M. van de Water, Sarah W. Davies, Margaux Hein, Gergely Torda, Mikhail V. Matz, Victor H. Beltran, Patrick Buerger, Eneour Puill-Stephan, David Abrego, David G. Bourne, and Bette L. Willis
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Coral ,Conservation ,Spawning ,Larvae ,Restoration ,Husbandry ,Medicine ,Biology (General) ,QH301-705.5 - Abstract
Here we describe an efficient and effective technique for rearing sexually-derived coral propagules from spawning through larval settlement and symbiont uptake with minimal impact on natural coral populations. We sought to maximize larval survival while minimizing expense and daily husbandry maintenance by experimentally determining optimized conditions and protocols for gamete fertilization, larval cultivation, induction of larval settlement by crustose coralline algae, and inoculation of newly settled juveniles with their dinoflagellate symbiont Symbiodinium. Larval rearing densities at or below 0.2 larvae mL−1 were found to maximize larval survival and settlement success in culture tanks while minimizing maintenance effort. Induction of larval settlement via the addition of a ground mixture of diverse crustose coralline algae (CCA) is recommended, given the challenging nature of in situ CCA identification and our finding that non settlement-inducing CCA assemblages do not inhibit larval settlement if suitable assemblages are present. Although order of magnitude differences in infectivity were found between common Great Barrier Reef Symbiodinium clades C and D, no significant differences in Symbiodinium uptake were observed between laboratory-cultured and wild-harvested symbionts in each case. The technique presented here for Acropora millepora can be adapted for research and restoration efforts in a wide range of broadcast spawning coral species.
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- 2017
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10. Modelling environmental drivers of black band disease outbreaks in populations of foliose corals in the genus Montipora
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Carla C.M. Chen, David G. Bourne, Christopher C. Drovandi, Kerrie Mengersen, Bette L. Willis, M. Julian Caley, and Yui Sato
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Black Band Disease ,Environmental covariates ,Coral Disease ,Cyanobacterial patches ,Transitional probability ,Multi-state Markov model ,Medicine ,Biology (General) ,QH301-705.5 - Abstract
Seawater temperature anomalies associated with warming climate have been linked to increases in coral disease outbreaks that have contributed to coral reef declines globally. However, little is known about how seasonal scale variations in environmental factors influence disease dynamics at the level of individual coral colonies. In this study, we applied a multi-state Markov model (MSM) to investigate the dynamics of black band disease (BBD) developing from apparently healthy corals and/or a precursor-stage, termed ‘cyanobacterial patches’ (CP), in relation to seasonal variation in light and seawater temperature at two reef sites around Pelorus Island in the central sector of the Great Barrier Reef. The model predicted that the proportion of colonies transitioning from BBD to Healthy states within three months was approximately 57%, but 5.6% of BBD cases resulted in whole colony mortality. According to our modelling, healthy coral colonies were more susceptible to BBD during summer months when light levels were at their maxima and seawater temperatures were either rising or at their maxima. In contrast, CP mostly occurred during spring, when both light and seawater temperatures were rising. This suggests that environmental drivers for healthy coral colonies transitioning into a CP state are different from those driving transitions into BBD. Our model predicts that (1) the transition from healthy to CP state is best explained by increasing light, (2) the transition between Healthy to BBD occurs more frequently from early to late summer, (3) 20% of CP infected corals developed BBD, although light and temperature appeared to have limited impact on this state transition, and (4) the number of transitions from Healthy to BBD differed significantly between the two study sites, potentially reflecting differences in localised wave action regimes.
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- 2017
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11. Temporal patterns in innate immunity parameters in reef‐building corals and linkages with local climatic conditions
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Jeroen A. J. M. van de Water, Joleah B. Lamb, Scott F. Heron, Madeleine J. H. van Oppen, and Bette L. Willis
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chromoprotein ,coral ,fluorescence ,green fluorescent protein‐like proteins ,immunity ,indicator ,Ecology ,QH540-549.5 - Abstract
Abstract Extremes in seasonal environmental conditions can significantly impact the health and physiological functioning of reef corals, underscoring the need for knowledge of seasonally specific baselines from which to monitor and forecast impending stress. Increases above summertime means in seawater temperature, sunlight intensity, turbidity, or sedimentation may reduce coral immunocompetency and increase disease and bleaching susceptibility. We analyzed temporal patterns in innate immunity parameters over nine time points throughout one year to establish baseline levels from which anomalies might be detected for representative species from three major reef‐building coral families (Acroporidae, Faviidae, and Poritidae). Temporal patterns in both phenoloxidase activity and expression of green fluorescent protein‐like proteins varied among the three families, as did overall constitutive levels. For example, Porites cylindrica had 2.8‐fold higher yearly average levels of phenoloxidase activity than Acropora millepora, which had the lowest levels. In contrast, mean fluorescence was lowest in Acropora millepora and highest in Echinopora mammiformis. Relationships between the potential physical drivers (seasonal variation in seawater temperature, rainfall, salinity) and temporal patterns in these parameters also differed among the three species. For example, phenoloxidase activity was positively correlated with seawater temperature in A. millepora, but negatively correlated in both E. mammiformis and P. cylindrica. Distinctions in constitutive levels and temporal patterns in these parameters among species suggest that corals from these three families have evolved different strategies for investing resources into innate immune parameters. Such differences highlight the need for species‐specific baselines and long‐term assessments to accurately predict coral reef trajectories in rapidly changing environments.
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- 2016
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12. In situ visualization of bacterial populations in coral tissues: pitfalls and solutions
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Naohisa Wada, Frederic J. Pollock, Bette L. Willis, Tracy Ainsworth, Nobuhiro Mano, and David G. Bourne
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Coral ,Bacteria ,Fluorescence in situ hybridization ,Holobiont ,In situ visualization ,Medicine ,Biology (General) ,QH301-705.5 - Abstract
In situ visualization of microbial communities within their natural habitats provides a powerful approach to explore complex interactions between microorganisms and their macroscopic hosts. Specifically, the application of fluorescence in situ hybridization (FISH) to simultaneously identify and visualize diverse microbial taxa associated with coral hosts, including symbiotic algae (Symbiodinium), Bacteria, Archaea, Fungi and protists, could help untangle the structure and function of these diverse taxa within the coral holobiont. However, the application of FISH approaches to coral samples is constrained by non-specific binding of targeted rRNA probes to cellular structures within the coral animal tissues (including nematocysts, spirocysts, granular gland cells within the gastrodermis and cnidoglandular bands of mesenterial filaments). This issue, combined with high auto-fluorescence of both host tissues and endosymbiotic dinoflagellates (Symbiodinium), make FISH approaches for analyses of coral tissues challenging. Here we outline the major pitfalls associated with applying FISH to coral samples and describe approaches to overcome these challenges.
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- 2016
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13. Isolation of an antimicrobial compound produced by bacteria associated with reef-building corals
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Jean-Baptiste Raina, Dianne Tapiolas, Cherie A. Motti, Sylvain Foret, Torsten Seemann, Jan Tebben, Bette L. Willis, and David G. Bourne
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Coral-associated bacteria ,Disease ,Alphaproteobacteria ,Antimicrobial compounds ,Medicine ,Biology (General) ,QH301-705.5 - Abstract
Bacterial communities associated with healthy corals produce antimicrobial compounds that inhibit the colonization and growth of invasive microbes and potential pathogens. To date, however, bacteria-derived antimicrobial molecules have not been identified in reef-building corals. Here, we report the isolation of an antimicrobial compound produced by Pseudovibrio sp. P12, a common and abundant coral-associated bacterium. This strain was capable of metabolizing dimethylsulfoniopropionate (DMSP), a sulfur molecule produced in high concentrations by reef-building corals and playing a role in structuring their bacterial communities. Bioassay-guided fractionation coupled with nuclear magnetic resonance (NMR) and mass spectrometry (MS), identified the antimicrobial as tropodithietic acid (TDA), a sulfur-containing compound likely derived from DMSP catabolism. TDA was produced in large quantities by Pseudovibrio sp., and prevented the growth of two previously identified coral pathogens, Vibrio coralliilyticus and V. owensii, at very low concentrations (0.5 μg/mL) in agar diffusion assays. Genome sequencing of Pseudovibrio sp. P12 identified gene homologs likely involved in the metabolism of DMSP and production of TDA. These results provide additional evidence for the integral role of DMSP in structuring coral-associated bacterial communities and underline the potential of these DMSP-metabolizing microbes to contribute to coral disease prevention.
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- 2016
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14. Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis
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Kate M. Quigley, Bette L. Willis, and Line K. Bay
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symbiodinium ,settlement ,juvenile ,survivorship ,maternal effects ,coral reef ,Science - Abstract
Coral endosymbionts in the dinoflagellate genus Symbiodinium are known to impact host physiology and have led to the evolution of reef-building, but less is known about how symbiotic communities in early life-history stages and their interactions with host parental identity shape the structure of coral communities on reefs. Differentiating the roles of environmental and biological factors driving variation in population demographic processes, particularly larval settlement, early juvenile survival and the onset of symbiosis is key to understanding how coral communities are structured and to predicting how they are likely to respond to climate change. We show that maternal effects (that here include genetic and/or effects related to the maternal environment) can explain nearly 24% of variation in larval settlement success and 5–17% of variation in juvenile survival in an experimental study of the reef-building scleractinian coral, Acropora tenuis. After 25 days on the reef, Symbiodinium communities associated with juvenile corals differed significantly between high mortality and low mortality families based on estimates of taxonomic richness, composition and relative abundance of taxa. Our results highlight that maternal and familial effects significantly explain variation in juvenile survival and symbiont communities in a broadcast-spawning coral, with Symbiodinium type A3 possibly a critical symbiotic partner during this early life stage.
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- 2016
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15. Correction: Seasonal Rainfall and Runoff Promote Coral Disease on an Inshore Reef.
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Jessica Haapkylä, Richard K. F. Unsworth, Mike Flavell, David G. Bourne, Britta Schaffelke, and Bette L. Willis
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Medicine ,Science - Published
- 2011
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16. Correction: The Roles and Interactions of Symbiont, Host and Environment in Defining Coral Fitness.
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Jos C. Mieog, Jeanine L. Olsen, Ray Berkelmans, Silvia A. Bleuler-Martinez, Bette L. Willis, and Madeleine J. H. van Oppen
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Medicine ,Science - Published
- 2009
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17. Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution
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Hannah E. Epstein, Tanya Brown, Ayomikun O. Akinrinade, Ryan McMinds, F. Joseph Pollock, Dylan Sonett, Styles Smith, David G. Bourne, Carolina S. Carpenter, Rob Knight, Bette L. Willis, Mónica Medina, Joleah B. Lamb, Rebecca Vega Thurber, and Jesse R. Zaneveld
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Evolutionary tradeoffs between life-history strategies are central to animal evolution. However, because microbes can influence aspects of host physiology, behavior, and resistance to stress or disease, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a highly biodiverse and data-rich host system to test this idea, made more relevant by increases in coral disease outbreaks as a result of anthropogenic changes to climate and reef ecosystems. Identifying factors that determine coral disease susceptibility has therefore become a focus for reef conservation efforts. Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by combining a cross-species coral microbiome survey (the “Global Coral Microbiome Project”) with long-term disease prevalence data at multiple sites. Interpreting these data in their phylogenetic context, we show that microbial dominance and composition predict disease susceptibility. We trace this dominance-disease association to a single putatively beneficial bacterial symbiont,Endozoicomonas, whose relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera. Conversely,Endozoicomonasabundances in coral tissue strongly correlated with high growth rates. These results demonstrate that the evolution of microbial symbiosis in corals correlates with both disease prevalence and growth rate. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbiosis influences animal life-history tradeoffs, and in efforts to use microbes to increase coral growth or disease resistancein-situ.Significance StatementThe evolution of tropical corals, like that of many organisms, involves tradeoffs in life-history strategy. We sought to test whether microbes influence coral life-history traits. Comparative data from a census of modern coral microbes, combined with long term disease surveys in three regions, provide evidence for a correlation between microbiome structure, growth rate, and disease susceptibility during coral evolution. These trends were driven primarily by changes in the relative abundance ofEndozoicomonasin coral tissue microbiomes, suggesting the novel hypothesis thatEndozoicomonasmay allow corals to grow more quickly at the cost of greater vulnerability to disease. Thus, symbiosis with microbes may be an important aspect of animal life-history strategy.
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- 2023
18. Energy depletion and opportunistic microbial colonisation in white syndrome lesions from corals across the Indo-Pacific
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Hillary A. Smith, David G. Bourne, Amanda Shore, Jessica A. Conlan, David S. Francis, F. Joseph Pollock, Bette L. Willis, Naohisa Wada, Julia Yun-Hsuan Hung, and Greta S. Aeby
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0106 biological sciences ,0301 basic medicine ,Zoology ,lcsh:Medicine ,Pocillopora damicornis ,010603 evolutionary biology ,01 natural sciences ,Article ,Lesion ,03 medical and health sciences ,RNA, Ribosomal, 16S ,medicine ,Metabolomics ,Animals ,Rhodobacteraceae ,lcsh:Science ,Relative species abundance ,Cell Proliferation ,Ecological epidemiology ,Abiotic component ,Multidisciplinary ,biology ,Coral Reefs ,Porites compressa ,Microbiota ,microbiology ,lcsh:R ,Immunity ,Histology ,Anthozoa ,biology.organism_classification ,Lipids ,Colonisation ,030104 developmental biology ,cell proliferation ,lcsh:Q ,Microbiome ,medicine.symptom ,Indo-Pacific - Abstract
Corals are dependent upon lipids as energy reserves to mount a metabolic response to biotic and abiotic challenges. This study profiled lipids, fatty acids, and microbial communities of healthy and white syndrome (WS) diseased colonies of Acropora hyacinthus sampled from reefs in Western Australia, the Great Barrier Reef, and Palmyra Atoll. Total lipid levels varied significantly among locations, though a consistent stepwise decrease from healthy tissues from healthy colonies (HH) to healthy tissue on WS-diseased colonies (HD; i.e. preceding the lesion boundary) to diseased tissue on diseased colonies (DD; i.e. lesion front) was observed, demonstrating a reduction in energy reserves. Lipids in HH tissues were comprised of high energy lipid classes, while HD and DD tissues contained greater proportions of structural lipids. Bacterial profiling through 16S rRNA gene sequencing and histology showed no bacterial taxa linked to WS causation. However, the relative abundance of Rhodobacteraceae-affiliated sequences increased in DD tissues, suggesting opportunistic proliferation of these taxa. While the cause of WS remains inconclusive, this study demonstrates that the lipid profiles of HD tissues was more similar to DD tissues than to HH tissues, reflecting a colony-wide systemic effect and provides insight into the metabolic immune response of WS-infected Indo-Pacific corals. This project was funded in part by Earthwatch Institute and Mitsubishi Corporation. Scopus
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- 2020
19. Effects of coral restoration on fish communities: snapshots of long‐term, multiregional responses and implications for practice
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Fanny Couture, Reanna Willis, Tory J. Chase, Margaux Y. Hein, Lisa Terry, Naomi M. Gardiner, Kayla Ripple, R. Alastair Birtles, Nadine Marshall, Elouise Haskin, Roger Beeden, and Bette L. Willis
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0106 biological sciences ,geography ,geography.geographical_feature_category ,Ecology ,biology ,Coral reef fish ,010604 marine biology & hydrobiology ,Coral ,fungi ,biology.organism_classification ,010603 evolutionary biology ,01 natural sciences ,Fishery ,Habitat ,Abundance (ecology) ,Coral cover ,population characteristics ,%22">Fish ,natural sciences ,Damselfish ,Reef ,geographic locations ,Ecology, Evolution, Behavior and Systematics ,Nature and Landscape Conservation - Abstract
Coral restoration is widely used around the world to address dramatic declines in coral cover; however, very few studies have looked specifically at the temporal response of fish assemblages (i.e. abundance and diversity) to coral restoration. Several critical reef functions and processes are driven by fishes, thereby making their recovery and responses around restoration structures key indicators of success. This study evaluates fish abundance and community composition on restoration plots following 8–12 years of restoration activity, in four locations (two Caribbean and two Indo‐Pacific). Responses were very complex with region‐, site‐, and body size‐specific patterns. Overall, fish abundance only increased in Indo‐Pacific sites where damselfish responded positively to increased coral cover and topographic complexity. Restoration effects on other fish families and particularly on larger bodied reef fish were negative or neutral at all locations. If restoration initiatives are going to substantively improve the condition and recovery of degraded reef fish communities, restoration efforts need to be planned, designed, and monitored based on fish‐specific habitat requirements and locally specific community dynamics.
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- 2020
20. Predicting the spatial distribution of allele frequencies for a gene associated with tolerance to eutrophication and high temperature in the reef-building coral, Acropora millepora, on the Great Barrier Reef
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Petra Lundgren, Bette L. Willis, Stuart Kininmonth, Madeleine J. H. van Oppen, and Young Koo Jin
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0106 biological sciences ,geography ,geography.geographical_feature_category ,Environmental change ,biology ,Ecology ,010604 marine biology & hydrobiology ,Coral ,Effects of global warming on oceans ,Aquatic Science ,Spatial distribution ,biology.organism_classification ,010603 evolutionary biology ,01 natural sciences ,Gene flow ,Acropora millepora ,Allele frequency ,Reef - Abstract
In the face of unprecedented rates of environmental alterations, the necessity to predict the capacity of corals to respond adaptively in a complex ecological system is becoming increasingly urgent. Recent findings that bleaching-resistant Acropora millepora coral populations have high frequencies of specific alleles provide an opportunity to use spatial mapping of alleles to identify resistant populations. In this study, a Bayesian belief network (BBN) model was developed to predict the spatial distribution of allele frequencies for a specific locus associated with bleaching resistance in response to acute eutrophication during the summertime in A. millepora in the Palm Islands (Great Barrier Reef, Australia). The BBN model enabled the putative responses of populations investigated to be extrapolated to other ‘equivalent’ populations that were previously not surveyed due to constraints of time, cost and logistics. A combination of long-term environmental monitoring data, allele frequency data, expert input and statistical evaluation was used to build the model, with the goal of refining prior beliefs and examining dependencies among environmental variables. The Bayesian simulation approach demonstrates that synergism between highly fluctuating temperatures and high nitrate concentrations may be the primary driver of selection for this locus. Consistently, spatial mapping of predicted allele frequencies reveals the tolerance allele is most likely to be concentrated in populations near the mouths of the Burdekin and Fitzroy Rivers. Corals from these river mouths are good candidates for assisted gene flow initiatives and also to restore reefs that are likely to be affected by eutrophication and ocean warming in the future. This approach opens up new opportunities for more efficient and effective coral reef management and conservation through direct intervention to ensure coral populations have the genetic diversity needed to optimise adaptation to rapid environmental change.
- Published
- 2019
21. Transgenerational inheritance of shuffled symbiont communities in the coral Montipora digitata
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Kate M. Quigley, Bette L. Willis, and Carly D. Kenkel
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0301 basic medicine ,0106 biological sciences ,Environmental change ,Coral bleaching ,Offspring ,Acclimatization ,Coral ,Zoology ,lcsh:Medicine ,Locus (genetics) ,Environment ,Microbiology ,010603 evolutionary biology ,01 natural sciences ,Article ,Montipora digitata ,03 medical and health sciences ,Symbiodinium ,Symbiosis ,Stress, Physiological ,Animals ,14. Life underwater ,Photosynthesis ,Clade ,lcsh:Science ,030304 developmental biology ,0303 health sciences ,Multidisciplinary ,Ecology ,Shuffling ,biology ,Coral Reefs ,Pigmentation ,fungi ,lcsh:R ,Inheritance (genetic algorithm) ,food and beverages ,Pigments, Biological ,biochemical phenomena, metabolism, and nutrition ,Anthozoa ,biology.organism_classification ,030104 developmental biology ,Dinoflagellida ,DNA, Intergenic ,lcsh:Q ,Seasons - Abstract
Adult organisms may “prime” their offspring for environmental change through a number of genetic and non-genetic mechanisms, termed parental effects. Some coral species can alter their thermal tolerance by shuffling the proportions of Symbiodinium types within their endosymbiotic communities, but it is unclear if this plasticity can be transferred to offspring in corals that have maternal symbiont transmission. We evaluated symbiont community composition in tagged colonies of Montipora digitata from Orpheus Island, Australia, over two successive annual spawning seasons, the second of which overlapped with the 2016 mass coral bleaching event on the Great Barrier Reef. We applied amplicon sequencing of the ITS2 locus to samples of four families (parent colonies and 10-12 eggs per family) to characterize their potential for symbiont shuffling and to determine if shuffled abundances were preserved in gametes. Symbiont cell densities and photochemical efficiencies of the symbionts’ photosystem II differed significantly among adults in 2016, suggesting differential responses to increased temperatures. Although abundances of the dominant symbiont haplotype, a representative of clade C15, did not differ among families or over time, low-abundance (“background”) ITS2 types differed more among years (2015 vs. 2016) than between life stages (parent vs. offspring). Results indicate that background symbiont shuffling can occur in a canonically ‘stable’ symbiosis, and that such plastic changes to the symbiont community are heritable. To our knowledge, this is the first evidence that shuffled Symbiodinium communities can be inherited by early life-history stages and supports the hypothesis that plastic changes in microbial communities may serve as a mechanism of rapid coral acclimation to changing environmental conditions.
- Published
- 2019
22. Unravelling the links between heat stress, bleaching and disease: fate of tabular corals following a combined disease and bleaching event
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O. B. Brodnicke, Rachel Pears, Bette L. Willis, Hillary A. Smith, David G. Bourne, Jessica Stella, and Scott F. Heron
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0106 biological sciences ,geography ,Beaver ,geography.geographical_feature_category ,genetic structures ,biology ,Coral bleaching ,010604 marine biology & hydrobiology ,Coral ,Outbreak ,Aquatic Science ,biology.organism_classification ,010603 evolutionary biology ,01 natural sciences ,Heat stress ,Animal science ,Coral cover ,biology.animal ,Acropora ,sense organs ,Reef - Abstract
While links between heat stress and coral bleaching are clear and predictive tools for bleaching risk are well advanced, links between heat stress and outbreaks of coral diseases are less well understood. In this study, the effects of accumulated heat stress on tagged colonies of tabular Acropora were monitored over the 2017 austral summer at Beaver Reef, which is located in the central region of the Great Barrier Reef. The initial surveys in midsummer (21 February) coincided with an accumulated heat stress metric of 4.5 °C-weeks, and documented high coral cover (74.0 ± 6.5%), extensive bleaching (71% of all corals displayed bleaching signs) and an outbreak of white syndromes (WSs) (31% of tabular acroporid corals displayed white syndrome signs). Repeat assessments of the impacts of bleaching and disease on these corals provided real-time information to reef managers by tracking the unfolding reef health incident on 100 colonies of Acropora hyacinthus (Dana, 1846), tagged in mid-March and surveyed intermittently until late October 2017. Heat stress increased rapidly on Beaver Reef, peaking at 8.3 °C-weeks on 31 March, which coincided with the highest prevalence of WS recorded in the study. Of the 85 tagged colonies surviving on 31 March, 41 (~ 48%) displayed WS signs, indicating a link between heat stress and WS. When re-surveyed at eight months (24 October), 68 of 100 tagged colonies had suffered whole-colony mortality and only four colonies had not displayed signs of bleaching or disease (WS) in any of our surveys. Overall, coral cover on Beaver Reef was reduced by more than half to 31.0 ± 11.2%. Significant tissue loss due to severe bleaching was observed with up to 20 times greater tissue loss on severely bleached colonies (i.e. categorised as > 50% bleached) compared to mildly/moderately bleached colonies (
- Published
- 2019
23. Temporal and spatial variation in fatty acid composition in Acropora tenuis corals along water quality gradients on the Great Barrier Reef, Australia
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Line K. Bay, David S. Francis, Bette L. Willis, Katharina E. Fabricius, and Melissa M. Rocker
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0106 biological sciences ,chemistry.chemical_classification ,biology ,ved/biology ,010604 marine biology & hydrobiology ,Coral ,ved/biology.organism_classification_rank.species ,Scleractinia ,Aquatic Science ,biology.organism_classification ,010603 evolutionary biology ,01 natural sciences ,Symbiodinium ,Animal science ,Nutrient ,chemistry ,Galaxea fascicularis ,Water quality ,Acropora tenuis ,Polyunsaturated fatty acid - Abstract
Fatty acids (FA) play a vital role in coral physiology, metabolism and stress resistance. Optimal health requires a balance of fatty acids, and more specifically essential polyunsaturated fatty acids (PUFA), for efficient biochemical and physiological functioning. Therefore, it is necessary to fully assess and evaluate the viability of FA as biomarkers for monitoring the health of coral populations. This study explores seasonal and spatial variation in the abundance of 17 FA in the coral Acropora tenuis, along two water quality gradients on the central Great Barrier Reef. Ratios of key FA varied similarly along the two water quality gradients and were highest in corals from comparatively good water quality conditions. Strong differences in PUFA composition were found between wet and dry seasons, with high percentage n-3 PUFA defining the dry seasons (June 2013 and October 2013) and high percentage n-6 PUFA defining the wet seasons (February 2013 and 2014). Saturated FA and monounsaturated FA concentrations varied with season, positively correlated with Symbiodinium density, and had highest concentrations in corals exposed to relatively poor water quality. Overall, results demonstrate that essential FA and their derived ratios support FA as a potential indicator of coral holobiont health; however, strong seasonal variation may negate FA and their derived ratios as water quality indicators.
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- 2019
24. Plasticity in gene expression and fatty acid profiles of Acropora tenuis reciprocally transplanted between two water quality regimes in the central Great Barrier Reef, Australia
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Carly D. Kenkel, Line K. Bay, Bette L. Willis, Melissa M. Rocker, and David S. Francis
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0106 biological sciences ,chemistry.chemical_classification ,ved/biology ,010604 marine biology & hydrobiology ,Coral ,ved/biology.organism_classification_rank.species ,Zoology ,Fatty acid ,Ribosome biogenesis ,Translation (biology) ,Aquatic Science ,Biology ,010603 evolutionary biology ,01 natural sciences ,chemistry ,Gene expression ,Gene ,Acropora tenuis ,Ecology, Evolution, Behavior and Systematics ,Polyunsaturated fatty acid - Abstract
To investigate plasticity in biochemical and physiological health attributes of corals, identical colony fragments of the coral Acropora tenuis, from two inshore populations, were exposed to native and novel environmental regimes. Variation in global gene expression (GE) and lipid and fatty acid (FA) composition of surviving colony fragments were quantified after four months. Major FA classes, with the exception of short-chain (C18) polyunsaturated fatty acids (PUFA), decreased in concentration when coral fragments were exposed to lower water quality regardless of their source population. In contrast, a strong effect of source population was detected in the GE profiles of all coral fragments and was enriched with genes associated with translation, ribosome biogenesis and ribosome cellular components. One cluster of co-expressed genes positively correlated with multiple individual FA and included genes involved in developmental processes and cellular pathways. This study demonstrates the strong influence of a source effect defining gene expression relating to basic biological functions, including biosynthetic processing, translation and ribosome biogenesis. However, there is plasticity in FA composition and specific genes relating to elevated health and immunity, which can respond to changes in environmental conditions. These findings suggest hope for future corals, if we can reduce anthropogenic water quality stressors.
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- 2019
25. Coral restoration: Socio-ecological perspectives of benefits and limitations
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Nadine Marshall, Bette L. Willis, Margaux Y. Hein, Alastair Birtles, Naomi M. Gardiner, and Roger Beeden
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0106 biological sciences ,geography ,geography.geographical_feature_category ,010604 marine biology & hydrobiology ,media_common.quotation_subject ,Stakeholder ,Sustainability science ,Context (language use) ,Coral reef ,010603 evolutionary biology ,01 natural sciences ,Sustainability ,Psychological resilience ,Stewardship ,Reef ,Environmental planning ,Ecology, Evolution, Behavior and Systematics ,Nature and Landscape Conservation ,media_common - Abstract
Coral restoration is increasingly used globally as a management tool to minimize accelerating coral reef degradation resulting from climate change. Yet, the science of coral restoration is still very focused on ecological and technical considerations, impeding the understanding of how coral restoration can be used to improve reef resilience in the context of socio-ecological systems. Here, we visited four well-established coral restoration projects in different regions of the world (Thailand, Maldives, Florida Keys, and US Virgin Islands), and conducted key-informant interviews to characterize local stakeholder's perceptions of the key benefits and limitations associated with restoration efforts. Our results reveal that perceptions around coral reef restoration encompass far more than ecological considerations, and include all four dimensions of sustainability: ecological, social, economic, and governance, suggesting that effective coral restoration should be guided by the principles of sustainability science. Socio-cultural benefits were the most frequently mentioned (72.4% of all respondents), while technical problems were the most common theme for limitations of coral restoration efforts (58.3% of the respondents). Participants also revealed some key points likely to improve the outcomes of coral restoration efforts such as the need to better embrace socio-cultural dimensions in goal setting, evaluate ecological outcomes more broadly, secure long-term funding and improve management and logistics of day to day practices. While we identify several important limitations of coral reef restoration, particularly around amateur workforces and limited involvement of local communities, our results suggest that coral restoration can be used as a powerful conservation education tool to provide hope, enhance agency, promote stewardship and strengthen coral reef conservation strategies.
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- 2019
26. Novel T4 bacteriophages associated with black band disease in corals
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M. J. H. van Oppen, Patrick Buerger, Bette L. Willis, Elisha M. Wood-Charlson, Yui Sato, and Karen D. Weynberg
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Operational taxonomic unit ,Virulence ,Microbiology ,Bacteriophage ,03 medical and health sciences ,Lysogenic cycle ,medicine ,Animals ,Bacteriophage T4 ,Seawater ,14. Life underwater ,skin and connective tissue diseases ,Phylogeny ,Ecology, Evolution, Behavior and Systematics ,030304 developmental biology ,0303 health sciences ,biology ,030306 microbiology ,Cyanophage ,Black band disease ,Anthozoa ,biology.organism_classification ,medicine.disease ,Prochlorococcus ,Bacteria - Abstract
Research into causative agents underlying coral disease have focused primarily on bacteria, whereas potential roles of viruses have been largely unaddressed. Bacteriophages may contribute to diseases through the lysogenic introduction of virulence genes into bacteria, or prevent diseases through lysis of bacterial pathogens. To identify candidate phages that may influence the pathogenicity of black band disease (BBD), communities of bacteria (16S rRNA) and T4-bacteriophages (gp23) were simultaneously profiled with amplicon sequencing among BBD-lesions and healthy-coral-tissue of Montipora hispida, as well as seawater (study site: the central Great Barrier Reef). Bacterial community compositions were distinct among BBD-lesions, healthy coral tissue and seawater samples, as observed in previous studies. Surprisingly, however, viral beta diversities based on both operational taxonomic unit (OTU)-compositions and overall viral community compositions of assigned taxa did not differ statistically between the BBD-lesions and healthy coral tissue. Nonetheless, relative abundances of three bacteriophage OTUs, affiliated to Cyanophage PRSM6 and Prochlorococcus phages P-SSM2, were significantly higher in BBD-lesions than in healthy tissue. These OTUs associated with BBD samples suggest the presence of bacteriophages that infect members of the cyanobacteria-dominated BBD community, and thus have potential roles in BBD pathogenicity.
- Published
- 2018
27. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny
- Author
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Rebecca Vega Thurber, Bette L. Willis, Mónica Medina, Ryan McMinds, David G. Bourne, F. Joseph Pollock, Styles Smith, and Jesse R. Zaneveld
- Subjects
0301 basic medicine ,Science ,Coral ,General Physics and Astronomy ,Biology ,DNA, Mitochondrial ,Article ,General Biochemistry, Genetics and Molecular Biology ,03 medical and health sciences ,Microbial ecology ,Symbiosis ,RNA, Ribosomal, 16S ,Animals ,14. Life underwater ,Microbiome ,lcsh:Science ,Phylogeny ,geography ,Multidisciplinary ,geography.geographical_feature_category ,Bacteria ,Geography ,Coral Reefs ,Ecology ,Microbiota ,fungi ,Australia ,technology, industry, and agriculture ,Sequence Analysis, DNA ,General Chemistry ,Coral reef ,biochemical phenomena, metabolism, and nutrition ,Anthozoa ,Archaea ,030104 developmental biology ,Microbial population biology ,RNA, Ribosomal ,Orbicella faveolata ,population characteristics ,lcsh:Q ,Species richness ,geographic locations - Abstract
Scleractinian corals’ microbial symbionts influence host health, yet how coral microbiomes assembled over evolution is not well understood. We survey bacterial and archaeal communities in phylogenetically diverse Australian corals representing more than 425 million years of diversification. We show that coral microbiomes are anatomically compartmentalized in both modern microbial ecology and evolutionary assembly. Coral mucus, tissue, and skeleton microbiomes differ in microbial community composition, richness, and response to host vs. environmental drivers. We also find evidence of coral-microbe phylosymbiosis, in which coral microbiome composition and richness reflect coral phylogeny. Surprisingly, the coral skeleton represents the most biodiverse coral microbiome, and also shows the strongest evidence of phylosymbiosis. Interactions between bacterial and coral phylogeny significantly influence the abundance of four groups of bacteria–including Endozoicomonas-like bacteria, which divide into host-generalist and host-specific subclades. Together these results trace microbial symbiosis across anatomy during the evolution of a basal animal lineage., Associations between corals and symbiotic microorganisms could be driven by the environment or shared evolutionary history. Here, the authors examine relationships between coral phylogenies and associated microbiomes, finding evidence of phylosymbiosis in microbes from coral skeleton and tissue, but not mucus.
- Published
- 2018
28. Experimental evolution of the coral algal endosymbiont, Cladocopium goreaui : lessons learnt across a decade of stress experiments to enhance coral heat tolerance
- Author
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Carlos Alvarez Roa, Bette L. Willis, Kate M. Quigley, Bill Leggat, and Victor H. Beltran
- Subjects
0106 biological sciences ,geography ,Experimental evolution ,geography.geographical_feature_category ,Ecology ,Host (biology) ,ved/biology ,010604 marine biology & hydrobiology ,Coral ,Symbiodiniaceae ,ved/biology.organism_classification_rank.species ,Zoology ,Coral reef ,Biology ,Photosynthesis ,010603 evolutionary biology ,01 natural sciences ,Heat tolerance ,Acropora tenuis ,Ecology, Evolution, Behavior and Systematics ,Nature and Landscape Conservation - Abstract
Projected increases in sea surface temperatures will exceed corals' ability to withstand heat stress within this century. Experimental evolution of cultured symbionts (Symbiodiniaceae) at high temperatures followed by reintroduction into corals can enhance coral heat tolerance. Several studies have selected for enhanced tolerance in Cladocopium goreaui (C1) over multiple time scales and then compared the performance of coral juveniles infected with the heat-tolerant C1 selected strain (SS) to the performance of juveniles infected with the C1 wild type (WT). To derive lessons about host benefits when symbionts are experimentally selected, here we compare the performance of SS- and WT-juveniles after 21 cell generations of heat selection versus longer periods (73–131) in recently published experiments. After 21 generations, we found rapid improvement in heat tolerance of SS through an overall shift in the mean tolerance to temperature. This did not translate to improved growth and survivorship of the coral. Specifically, survival did not differ significantly between juveniles of Acropora tenuis hosting WT versus SS at any temperature. Juveniles infected with WT exhibited greater skeletal growth than those infected with SS at 27 and 31°C but not at 32.5°C. SS-juvenile symbiont cell densities increased significantly at 27°C relative to SS-juveniles in the 31 and 32.5°C. Photosynthetic efficiencies in SS-juveniles were higher compared to WT-juveniles at 31°C, equal at 27°C, and lower at 32.5°C. These results suggest that selection over longer generation (>130) times will be needed to confer host benefits and will be dependent on the stability of this association being maintained in nature.
- Published
- 2021
29. An Indo-Pacific coral spawning database
- Author
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David Abrego, Erika Woolsey, Yoko Nozawa, Jean-François Flot, Chieh Jhen Chen, Nur Fadli, Jude Keyse, Mila Grinblat, Eugenia M. Sampayo, Elizaldy A. Maboloc, Gaetan Hoarau, Christopher Doropoulos, Alasdair J. Edwards, Akira Iguchi, Satoshi Nojima, Tom Shlesinger, Choo Zhi Min, Srisakul Piromvaragorn, Selina Ward, Wei Jen Chen, Kareen Vicentuan, Chung Hong Tan, Kate M. Quigley, Zarinah Waheed, Tracy D. Tabalanza, Sakanan Plathong, Tullia Isotta Terraneo, James R. Guest, Davies Austin Spiji, Joshua S. Madin, Syafyudin Yusuf, Karenne Tun, Russel C. Babcock, Gal Eyal, Ching-Fong Chang, Miguel Barbosa, Masayuki Hatta, Matthew R. Nitschke, Vivian R. Cumbo, Emmeline A. Jamodiong, Jeffrey Low, Seiya Kitanobo, Andrew H. Baird, Maria Dornelas, Takuma Mezaki, Kazuhiko Sakai, Gerard F. Ricardo, John A. Burt, Emily J. Howells, Fung Chen Chung, Erin Graham, Charlon A. Ligson, Sze Hoon Gan, Chaolun Allen Chen, Sean R. Connolly, Bette L. Willis, Patrick C. Cabaitan, Peter Harrison, Narinratana Kongjandtre, Lee Eyal-Shaham, Carrie A. Sims, Yossi Loya, Suchana Chavanich, Eneour Puill-Stephan, Andrew G. Bauman, Victor E. Bonito, Rachael M. Woods, Frederic Sinniger, Su Hwei Neo, James True, Leony Sikim, Naoko Isomura, Masaya Morita, Suppakarn Jandang, Jessica Bouwmeester, Che-Hung Lin, Joana Figueiredo, Nina Ann Jin Ho, Elizabeth J. Gomez, Hiromi Yamamoto, Aurelie Moya, Mia O. Hoogenboom, Mariana Álvarez-Noriega, Nataly Gutierrez-Isaza, Chris Simpson, Saki Harii, Hanaka Mera, Chao-Yang Kuo, Gergely Torda, Voranop Viyakarn, Catalina Ramírez-Portilla, University of St Andrews. School of Biology, University of St Andrews. Centre for Biological Diversity, University of St Andrews. Fish Behaviour and Biodiversity Research Group, and University of St Andrews. Marine Alliance for Science & Technology Scotland
- Subjects
0106 biological sciences ,Statistics and Probability ,Data Descriptor ,Science ,QH301 Biology ,Coral ,Evolution des espèces ,Library and Information Sciences ,computer.software_genre ,010603 evolutionary biology ,01 natural sciences ,Education ,Databases ,QH301 ,Reproductive biology ,Animals ,Océanographie biologique ,ZA4450 ,Indian Ocean ,Marine biology ,GC ,Pacific Ocean ,ZA4450 Databases ,Database ,Conservation biology ,010604 marine biology & hydrobiology ,Reproduction ,Biologie moléculaire ,DAS ,Population ecology ,Anthozoa ,Great barrier reef ,Computer Science Applications ,Geography ,Génétique, cytogénétique ,Systématique des espèces [zoologie] ,GC Oceanography ,Evolutionary ecology ,Statistics, Probability and Uncertainty ,computer ,Indo-Pacific ,Information Systems - Abstract
The discovery of multi-species synchronous spawning of scleractinian corals on the Great Barrier Reef in the 1980s stimulated an extraordinary effort to document spawning times in other parts of the globe. Unfortunately, most of these data remain unpublished which limits our understanding of regional and global reproductive patterns. The Coral Spawning Database (CSD) collates much of these disparate data into a single place. The CSD includes 6178 observations (3085 of which were unpublished) of the time or day of spawning for over 300 scleractinian species in 61 genera from 101 sites in the Indo-Pacific. The goal of the CSD is to provide open access to coral spawning data to accelerate our understanding of coral reproductive biology and to provide a baseline against which to evaluate any future changes in reproductive phenology., info:eu-repo/semantics/published
- Published
- 2021
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30. Deciphering Coral Disease Dynamics: Integrating Host, Microbiome, and the Changing Environment
- Author
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Ernesto Weil, Marilyn E. Brandt, Allison M. Tracy, Katherine C. Prager, Bette L. Willis, Rebecca Vega Thurber, Stan Langevin, C. Drew Harvell, Raechel A. Littman, Laura D. Mydlarz, Phoebe D. Dawkins, Melissa Garren, Joleah B. Lamb, Keri M. Kemp, and Laurie J. Raymundo
- Subjects
Coral ,Wildlife ,lcsh:Evolution ,microbiome ,Disease ,reefs ,lcsh:QH540-549.5 ,lcsh:QH359-425 ,Microbiome ,Reef ,coral ,Ecology, Evolution, Behavior and Systematics ,geography ,disease ,geography.geographical_feature_category ,Ecology ,fungi ,technology, industry, and agriculture ,Outbreak ,Coral reef ,dysbiosis ,biochemical phenomena, metabolism, and nutrition ,climate change ,Foundation species ,lcsh:Ecology - Abstract
Diseases of tropical reef organisms is an intensive area of study, but despite significant advances in methodology and the global knowledge base, identifying the proximate causes of disease outbreaks remains difficult. The dynamics of infectious wildlife diseases are known to be influenced by shifting interactions among the host, pathogen, and other members of the microbiome, and a collective body of work clearly demonstrates that this is also the case for the main foundation species on reefs, corals. Yet, among wildlife, outbreaks of coral diseases stand out as being driven largely by a changing environment. These outbreaks contributed not only to significant losses of coral species but also to whole ecosystem regime shifts. Here we suggest that to better decipher the disease dynamics of corals, we must integrate more holistic and modern paradigms that consider multiple and variable interactions among the three major players in epizootics: the host, its associated microbiome, and the environment. In this perspective, we discuss how expanding the pathogen component of the classic host-pathogen-environment disease triad to incorporate shifts in the microbiome leading to dysbiosis provides a better model for understanding coral disease dynamics. We outline and discuss issues arising when evaluating each component of this trio and make suggestions for bridging gaps between them. We further suggest that to best tackle these challenges, researchers must adjust standard paradigms, like the classic one pathogen-one disease model, that, to date, have been ineffectual at uncovering many of the emergent properties of coral reef disease dynamics. Lastly, we make recommendations for ways forward in the fields of marine disease ecology and the future of coral reef conservation and restoration given these observations.
- Published
- 2020
31. Coral Restoration Effectiveness: Multiregional Snapshots of the Long-Term Responses of Coral Assemblages to Restoration
- Author
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Jessica Levy, Lisa Terry, Alastair Birtles, Bette L. Willis, Margaux Y. Hein, Thomas Le Berre, Naomi M. Gardiner, Roger Beeden, Nadine Marshall, and Chad M. Scott
- Subjects
0106 biological sciences ,media_common.quotation_subject ,Coral ,effectiveness ,010603 evolutionary biology ,01 natural sciences ,Ecosystem services ,Coral health ,coral assemblages ,coral restoration ,lcsh:QH301-705.5 ,Reef ,Nature and Landscape Conservation ,media_common ,geography ,geography.geographical_feature_category ,Ecology ,business.industry ,010604 marine biology & hydrobiology ,Ecological Modeling ,Environmental resource management ,Agricultural and Biological Sciences (miscellaneous) ,Term (time) ,monitoring ,lcsh:Biology (General) ,Coral cover ,Psychological resilience ,business - Abstract
Coral restoration is rapidly becoming a mainstream strategic reef management response to address dramatic declines in coral cover worldwide. Restoration success can be defined as enhanced reef functions leading to improved ecosystem services, with multiple benefits at socio-ecological scales. However, there is often a mismatch between the objectives of coral restoration programs and the metrics used to assess their effectiveness. In particular, the scales of ecological benefits currently assessed are typically limited in both time and space, often being limited to short-term monitoring of the growth and survival of transplanted corals. In this paper, we explore reef-scale responses of coral assemblages to restoration practices applied in four well-established coral restoration programs. We found that hard coral cover and structural complexity were consistently greater at restored compared to unrestored (degraded) sites. However, patterns in coral diversity, coral recruitment, and coral health among restored, unrestored, and reference sites varied across locations, highlighting differences in methodologies among restoration programs. Altogether, differences in program objectives, methodologies, and the state of nearby coral communities were key drivers of variability in the responses of coral assemblages to restoration. The framework presented here provides guidance to improve qualitative and quantitative assessments of coral restoration efforts and can be applied to further understanding of the role of restoration within resilience-based reef management.
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- 2020
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32. Decadal erosion of coral assemblages by multiple disturbances in the Palm Islands, central Great Barrier Reef
- Author
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Yui Sato, Tessa Hill, Gergely Torda, Vimoksalehi Lukoschek, Georgina Torras Jorda, Bette L. Willis, Katie Sambrook, Peter Cross, Aurelie Moya, and David G. Bourne
- Subjects
0106 biological sciences ,Coral ,Population Dynamics ,Climate change ,lcsh:Medicine ,010603 evolutionary biology ,01 natural sciences ,Article ,Stress, Physiological ,Acropora ,Animals ,lcsh:Science ,Reef ,Islands ,geography ,Multidisciplinary ,geography.geographical_feature_category ,biology ,Coral Reefs ,Cyclonic Storms ,010604 marine biology & hydrobiology ,fungi ,lcsh:R ,Community structure ,technology, industry, and agriculture ,Storm ,biochemical phenomena, metabolism, and nutrition ,biology.organism_classification ,Anthozoa ,Oceanography ,Disturbance (ecology) ,Environmental science ,population characteristics ,lcsh:Q ,Tropical cyclone ,geographic locations - Abstract
Increases in the frequency of perturbations that drive coral community structure, such as severe thermal anomalies and high intensity storms, highlight the need to understand how coral communities recover following multiple disturbances. We describe the dynamics of cover and assemblage composition of corals on exposed inshore reefs in the Palm Islands, central Great Barrier Reef, over 19 years encapsulating major disturbance events such as the severe bleaching event in 1998 and Cyclone Yasi in 2011, along with other minor storm and heat stress events. Over this time, 47.8% of hard coral cover was lost, with a concomitant shift in coral assemblage composition due to taxon-specific rates of mortality during the disturbances, and asymmetric recovery in the aftermath thereof. High recruitment rates of some broadcast-spawning corals, particularly corymbose Acropora spp., even in the absence of adult colonies, indicate that a strong external larval supply replenished the stocks. Conversely, the time required for recovery of slow-growing coral morphologies and life histories was longer than the recurrence times of major disturbances. With interludes between bleaching and cyclones predicted to decrease, the probability of another severe disturbance event before coral cover and assemblage composition approximates historical levels suggests that reefs will continue to erode.
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- 2018
33. Leveraging new knowledge of Symbiodinium community regulation in corals for conservation and reef restoration
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Kate M. Quigley, Bette L. Willis, and Line K. Bay
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0106 biological sciences ,geography ,geography.geographical_feature_category ,Ecology ,biology ,Coral bleaching ,010604 marine biology & hydrobiology ,media_common.quotation_subject ,Library science ,Coral reef ,Aquatic Science ,biology.organism_classification ,010603 evolutionary biology ,01 natural sciences ,Scholarship ,Symbiodinium ,Research council ,Excellence ,Political science ,Postgraduate research ,Reef ,Ecology, Evolution, Behavior and Systematics ,media_common - Abstract
This manuscript was improved by constructive comments from the Responsible Editor and 2 anonymous reviewers. This study was supported by the Endeavour International and JCU Postgraduate Research Scholarship to K.M.Q., the Australian Research Council grant, through the ARC Centre of Excellence for Coral Reef Studies, to B.L.W., and by funding from the Australian Institute of Marine Science to L.K.B.
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- 2018
34. Selective feeding by corallivorous fishes neither promotes nor reduces progression rates of black band disease
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Mia O. Hoogenboom, Bette L. Willis, Katia J. Nicolet, and Pratchett
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0106 biological sciences ,Host resistance ,Ecology ,010604 marine biology & hydrobiology ,Coral ,Disease progression ,Zoology ,Black band disease ,Disease ,Aquatic Science ,Biology ,medicine.disease ,Natural variation ,010603 evolutionary biology ,01 natural sciences ,Predation ,medicine ,Progression rate ,skin and connective tissue diseases ,Ecology, Evolution, Behavior and Systematics - Abstract
Black band disease (BBD) is a virulent coral disease, and although its microbiology has been studied extensively, the aetiology of BBD remains poorly understood. Here we used aquaria and field experiments to determine if feeding on BBD lesions by corallivorous fishes influences disease progression rates. Although selective predation on lesions was observed in both controlled laboratory experiments and field-based observations, we found no evidence that fish feeding either reduced or enhanced progression rates of BBD. Variability in disease progression rates in the field was explained by variation among coral colonies (24.46%) and among sample days (37.77%) rather than by predation treatment (
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- 2018
35. Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef‐building coral
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Madeleine J. H. van Oppen, Maryam Chaib De Mares, David G. Bourne, Jean-Baptiste Raina, Jeroen A. J. M. van de Water, Bette L. Willis, and Groves Dixon
- Subjects
0301 basic medicine ,ved/biology.organism_classification_rank.species ,Montipora aequituberculata ,Pocillopora damicornis ,Oceanospirillales ,Montipora digitata ,Microbiology ,03 medical and health sciences ,Symbiodinium ,Anti-Infective Agents ,Stress, Physiological ,Genetics ,Animals ,Seawater ,Ecology, Evolution, Behavior and Systematics ,Innate immune system ,biology ,Coral Reefs ,ved/biology ,Vibrio coralliilyticus ,Temperature ,biochemical phenomena, metabolism, and nutrition ,Anthozoa ,biology.organism_classification ,Holobiont ,030104 developmental biology ,Gene Expression Regulation ,Transcriptome - Abstract
Global increases in coral disease prevalence have been linked to ocean warming through changes in coral-associated bacterial communities, pathogen virulence and immune system function. However, the interactive effects of temperature and pathogens on the coral holobiont are poorly understood. Here, we assessed three compartments of the holobiont (host, Symbiodinium and bacterial community) of the coral Montipora aequituberculata challenged with the pathogen Vibrio coralliilyticus and the commensal bacterium Oceanospirillales sp. under ambient (27°C) and elevated (29.5 and 32°C) seawater temperatures. Few visual signs of bleaching and disease development were apparent in any of the treatments, but responses were detected in the holobiont compartments. V. coralliilyticus acted synergistically and negatively impacted the photochemical efficiency of Symbiodinium at 32°C, while Oceanospirillales had no significant effect on photosynthetic efficiency. The coral, however, exhibited a minor response to the bacterial challenges, with the response towards V. coralliilyticus being significantly more pronounced, and involving the prophenoloxidase-activating system and multiple immune system-related genes. Elevated seawater temperatures did not induce shifts in the coral-associated bacterial community, but caused significant gene expression modulation in both Symbiodinium and the coral host. While Symbiodinium exhibited an antiviral response and upregulated stress response genes, M. aequituberculata showed regulation of genes involved in stress and innate immune response processes, including immune and cytokine receptor signalling, the complement system, immune cell activation and phagocytosis, as well as molecular chaperones. These observations show that M. aequituberculata is capable of maintaining a stable bacterial community under elevated seawater temperatures and thereby contributes to preventing disease development.
- Published
- 2018
36. The need for broader ecological and socioeconomic tools to evaluate the effectiveness of coral restoration programs
- Author
-
Bette L. Willis, Margaux Y. Hein, Roger Beeden, and Alastair Birtles
- Subjects
0106 biological sciences ,geography ,geography.geographical_feature_category ,Ecology ,business.industry ,010604 marine biology & hydrobiology ,Environmental resource management ,Coral reef ,010603 evolutionary biology ,01 natural sciences ,Ecosystem services ,Sustainable community ,Transplantation ,Ecological indicator ,Sustainability ,business ,Restoration ecology ,Reef ,Ecology, Evolution, Behavior and Systematics ,Nature and Landscape Conservation - Abstract
Coral reef restoration initiatives are burgeoning in response to the need for novel management strategies to address dramatic global declines in coral cover. However, coral restoration programs typically lack rigor and critical evaluation of their effectiveness. A review of 83 peer-reviewed papers that used coral transplantation for reef restoration reveals that growth and survival of coral fragments were the most widely used indicators of restoration success, with 88% of studies using these two indicators either solely (55%) or in combination with a limited number of other ecological factors (33%). In 53% of studies, reef condition was monitored for 1 year or less, while only 5% of reefs were monitored for more than 5 years post-transplantation. These results highlight that coral reef restoration science has focused primarily on short-term experiments to evaluate the feasibility of techniques for ecological restoration and the initial establishment phase post-transplantation, rather than on longer-term outcomes for coral reef communities. Here, we outline 10 socioecological indicators that comprehensively evaluate the effectiveness of coral reef restoration across the four pillars of sustainability (i.e. environmental, sociocultural, governance, and economic contributions to sustainable communities). We recommend that evaluations of the effectiveness of coral restoration programs integrate ecological indicators with sociocultural, economic, and governance considerations. Assessing the efficacy of coral restoration as a tool to support reef resilience will help to guide future efforts and ensure the sustainable maintenance of reef ecosystem goods and services.
- Published
- 2017
37. Variation in the health and biochemical condition of the coral Acropora tenuis along two water quality gradients on the Great Barrier Reef, Australia
- Author
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Bette L. Willis, Katharina E. Fabricius, Melissa M. Rocker, Line K. Bay, and David S. Francis
- Subjects
0106 biological sciences ,010504 meteorology & atmospheric sciences ,Coral ,ved/biology.organism_classification_rank.species ,Aquatic Science ,Biology ,Oceanography ,01 natural sciences ,River source ,Water Quality ,River mouth ,Animals ,natural sciences ,Acropora tenuis ,Reef ,0105 earth and related environmental sciences ,Biomass (ecology) ,geography ,geography.geographical_feature_category ,Coral Reefs ,Ecology ,ved/biology ,010604 marine biology & hydrobiology ,fungi ,Australia ,technology, industry, and agriculture ,Coral reef ,biochemical phenomena, metabolism, and nutrition ,Anthozoa ,Adaptation, Physiological ,Pollution ,Fishery ,population characteristics ,Water quality - Abstract
This study explores how plasticity in biochemical attributes, used as indicators of health and condition, enables the coral Acropora tenuis to respond to differing water quality regimes in inshore regions of the Great Barrier Reef. Health attributes were monitored along a strong and weak water quality gradient, each with three reefs at increasing distances from a major river source. Attributes differed significantly only along the strong gradient; corals grew fastest, had the least dense skeletons, highest symbiont densities and highest lipid concentrations closest to the river mouth, where water quality was poorest. High nutrient and particulate loads were only detrimental to skeletal density, which decreased as linear extension increased, highlighting a trade-off. Our study underscores the importance of assessing multiple health attributes in coral reef monitoring. For example, autotrophic indices are poor indicators of coral health and condition, but improve when combined with attributes like lipid content and biomass.
- Published
- 2017
38. Characterization of coral-associated microbial aggregates (CAMAs) within tissues of the coral Acropora hyacinthus
- Author
-
F. Joseph Pollock, Naohisa Wada, Nobuhiro Mano, Bette L. Willis, Tracy D. Ainsworth, Mizuki Ishimochi, Taeko Matsui, Sen-Lin Tang, and David G. Bourne
- Subjects
DNA, Bacterial ,0301 basic medicine ,Microorganism ,Coral ,030106 microbiology ,lcsh:Medicine ,Microbial communities ,Biology ,Article ,Acropora hyacinthus ,03 medical and health sciences ,Japan ,Symbiosis ,Phylogenetics ,RNA, Ribosomal, 16S ,Animals ,lcsh:Science ,In Situ Hybridization, Fluorescence ,Phylogeny ,geography ,Multidisciplinary ,geography.geographical_feature_category ,Environmental microbiology ,Bacteria ,Coral Reefs ,Host (biology) ,Ecology ,Microbiota ,lcsh:R ,Australia ,Sequence Analysis, DNA ,Coral reef ,Anthozoa ,Great barrier reef ,Holobiont ,030104 developmental biology ,%22">Fish ,lcsh:Q - Abstract
Bacterial diversity associated with corals has been studied extensively, however, localization of bacterial associations within the holobiont is still poorly resolved. Here we provide novel insight into the localization of coral-associated microbial aggregates (CAMAs) within tissues of the coral Acropora hyacinthus. In total, 318 and 308 CAMAs were characterized via histological and fluorescent in situ hybridization (FISH) approaches respectively, and shown to be distributed extensively throughout coral tissues collected from five sites in Japan and Australia. The densities of CAMAs within the tissues were negatively correlated with the distance from the coastline (i.e. lowest densities at offshore sites). CAMAs were randomly distributed across the six coral tissue regions investigated. Within each CAMA, bacterial cells had similar morphological characteristics, but bacterial morphologies varied among CAMAs, with at least five distinct types identified. Identifying the location of microorganisms associated with the coral host is a prerequisite for understanding their contributions to fitness. Localization of tissue-specific communities housed within CAMAs is particularly important, as these communities are potentially important contributors to vital metabolic functions of the holobiont.
- Published
- 2019
39. Co-dynamics of Symbiodiniaceae and bacterial populations during the first year of symbiosis with Acropora tenuis juveniles
- Author
-
Kate M. Quigley, David G. Bourne, Bette L. Willis, Carlos Alvarez Roa, and Greg Torda
- Subjects
Coral ,ved/biology.organism_classification_rank.species ,lcsh:QR1-502 ,Bacterial Physiological Phenomena ,Microbiology ,lcsh:Microbiology ,coral‐associated bacteria ,Symbiosis ,Symbiodiniaceae ,RNA, Ribosomal, 16S ,Gammaproteobacteria ,DNA, Ribosomal Spacer ,Animals ,Relative species abundance ,Acropora tenuis ,coral ,co‐occurrence ,biology ,Ecology ,ved/biology ,Microbiota ,Planctomycetes ,Alphaproteobacteria ,Age Factors ,Computational Biology ,Original Articles ,biology.organism_classification ,Anthozoa ,ITS2 rDNA gene ,Molecular Typing ,Gene Ontology ,juvenile ,Original Article ,Metagenomics ,16S rRNA gene ,Proteobacteria - Abstract
Interactions between corals and their associated microbial communities (Symbiodiniaceae and prokaryotes) are key to understanding corals' potential for and rate of acclimatory and adaptive responses. However, the establishment of microalgal and bacterial communities is poorly understood during coral ontogeny in the wild. We examined the establishment and co‐occurrence between multiple microbial communities using 16S rRNA (bacterial) and ITS2 rDNA (Symbiodiniaceae) gene amplicon sequencing in juveniles of the common coral, Acropora tenuis, across the first year of development. Symbiodiniaceae communities in juveniles were dominated by Durusdinium trenchii and glynnii (D1 and D1a), with lower abundances of Cladocopium (C1, C1d, C50, and Cspc). Bacterial communities were more diverse and dominated by taxa within Proteobacteria, Cyanobacteria, and Planctomycetes. Both communities were characterized by significant changes in relative abundance and diversity of taxa throughout the year. D1, D1a, and C1 were significantly correlated with multiple bacterial taxa, including Alpha‐, Deltra‐, and Gammaproteobacteria, Planctomycetacia, Oxyphotobacteria, Phycisphaerae, and Rhizobiales. Specifically, D1a tended to associate with Oxyphotobacteria and D1 with Alphaproteobacteria, although these associations may represent correlational and not causal relationships. Bioenergetic modeling combined with physiological measurements of coral juveniles (surface area and Symbiodiniaceae cell densities) identified key periods of carbon limitation and nitrogen assimilation, potentially coinciding with shifts in microbial community composition. These results demonstrate that Symbiodiniaceae and bacterial communities are dynamic throughout the first year of ontology and may vary in tandem, with important fitness effects on host juveniles., We characterized the establishment and maintenance of bacterial and Symbiodiniaceae communities in the coral Acropora tenuis across the first year of juvenile ontogeny, identifying potentially key co‐occurrence patterns using network modeling. Bioenergetic modeling combined with physiological measurements of coral juveniles (surface area and Symbiodiniaceae cell densities) identified periods of carbon limitation and nitrogen assimilation, potentially coinciding with shifts in microbial community composition. These dynamic communities vary in tandem with important fitness effects on host juvenile corals.
- Published
- 2019
40. Reduced diversity and stability of coral-associated bacterial communities and suppressed immune function precedes disease onset in corals
- Author
-
Britta Schaffelke, David G. Bourne, F. Joseph Pollock, Jeroen A. J. M. van de Water, Hillary A. Smith, Bette L. Willis, and Joleah B. Lamb
- Subjects
0106 biological sciences ,marine infrastructure ,Coral ,coral microbes ,Disease ,Biology ,010603 evolutionary biology ,01 natural sciences ,03 medical and health sciences ,Immune system ,Ecosystem ,lcsh:Science ,bacteria ,Reef ,white syndrome ,030304 developmental biology ,0303 health sciences ,geography ,disease ,Multidisciplinary ,geography.geographical_feature_category ,Ecology ,fungi ,technology, industry, and agriculture ,Biology (Whole Organism) ,Coral reef ,biochemical phenomena, metabolism, and nutrition ,immunity ,Holobiont ,population characteristics ,lcsh:Q ,Immunocompetence ,geographic locations ,Research Article - Abstract
Disease is an emerging threat to coral reef ecosystems worldwide, highlighting the need to understand how environmental conditions interact with coral immune function and associated microbial communities to affect holobiont health. Increased coral disease incidence on reefs adjacent to permanently moored platforms on Australia's Great Barrier Reef provided a unique case study to investigate environment–host–microbe interactions in situ . Here, we evaluate coral-associated bacterial community (16S rRNA amplicon sequencing), immune function (protein-based prophenoloxidase-activating system), and water quality parameters before, during and after a disease event. Over the course of the study, 31% of tagged colonies adjacent to platforms developed signs of white syndrome (WS), while all control colonies on a platform-free reef remained visually healthy. Corals adjacent to platforms experienced significant reductions in coral immune function. Additionally, the corals at platform sites that remained visually healthy throughout the study had reduced bacterial diversity compared to healthy colonies at the platform-free site. Interestingly, prior to the observation of macroscopic disease, corals that would develop WS had reduced bacterial diversity and significantly greater community heterogeneity between colonies compared to healthy corals at the same location. These results suggest that activities associated with offshore marine infrastructure impacts coral immunocompetence and associated bacterial community, which affects the susceptibility of corals to disease.
- Published
- 2019
41. Uncoupling temperature-dependent mortality from lipid depletion for scleractinian coral larvae
- Author
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Erin Graham, Bette L. Willis, Andrew H. Baird, Sean R. Connolly, and Mary A. Sewell
- Subjects
0106 biological sciences ,Larva ,geography ,geography.geographical_feature_category ,ved/biology ,Ecology ,010604 marine biology & hydrobiology ,Coral ,fungi ,ved/biology.organism_classification_rank.species ,Climate change ,Coral reef ,Aquatic Science ,Biology ,010603 evolutionary biology ,01 natural sciences ,Abundance (ecology) ,Biological dispersal ,Acropora tenuis ,Reef - Abstract
Predicted increases in sea-surface temperatures due to climate change are likely to alter the physiology of marine organisms and ultimately influence the distribution and abundance of their populations. The consequences of increased temperatures for marine species, including decreased survival and altered rates of development, growth and settlement, are well known and often attributed to imbalances between energy supply and demand. To test this hypothesis, we calibrated the effect of temperature on rates of survival and lipid depletion for larvae of the common stony coral Acropora tenuis over a 7 °C temperature range. Temperature had a pronounced, linearly increasing effect on larval mortality, with a sixfold decrease in median survival time. Contrary to expectation, however, temperature had a quasi-parabolic effect on lipid use; rates declined as temperatures either increased above or decreased below the ambient temperature at the time of spawning. This contrasts with previous work suggesting that increased energy depletion is the cause of larval mortality at higher temperatures. Our results highlight the sensitivity of coral larvae to temperature and have implications for dispersal potential because fewer larvae will survive to disperse. Such projected declines in connectivity among coral populations are likely to undermine reef resilience.
- Published
- 2016
42. The transcriptomic response of the coral Acropora digitifera to a competent Symbiodinium strain: the symbiosome as an arrested early phagosome
- Author
-
David G. Bourne, Mark A. Ragan, Nori Satoh, Saki Harii, Cheong Xin Chan, David J. Miller, Eldon E. Ball, Vivian R. Cumbo, Bette L. Willis, Amin R. Mohamed, and Chuya Shinzato
- Subjects
0106 biological sciences ,0301 basic medicine ,Biology ,Sea anemone ,010603 evolutionary biology ,01 natural sciences ,Transcriptome ,03 medical and health sciences ,Symbiodinium ,Phagosomes ,Botany ,Genetics ,Acropora digitifera ,Animals ,Acropora ,14. Life underwater ,Symbiosis ,Ecology, Evolution, Behavior and Systematics ,Phagosome ,Sequence Analysis, RNA ,Early phagosome ,High-Throughput Nucleotide Sequencing ,Anthozoa ,biology.organism_classification ,030104 developmental biology ,Symbiosome ,Dinoflagellida - Abstract
Despite the ecological significance of the relationship between reef-building corals and intracellular photosynthetic dinoflagellates of the genus Symbiodinium, very little is known about the molecular mechanisms involved in its establishment. Indeed, microarray-based analyses point to the conclusion that host gene expression is largely or completely unresponsive during the establishment of symbiosis with a competent strain of Symbiodinium. In this study, the use of Illumina RNA-Seq technology allowed detection of a transient period of differential expression involving a small number of genes (1073 transcripts
- Published
- 2016
43. Microsatellite allele sizes alone are insufficient to delineate species boundaries inSymbiodinium
- Author
-
Bette L. Willis, M. J. H. van Oppen, Line K. Bay, and Emily J. Howells
- Subjects
0106 biological sciences ,0301 basic medicine ,Genetic diversity ,education.field_of_study ,Ecology ,Population ,Population genetics ,Biology ,biology.organism_classification ,010603 evolutionary biology ,01 natural sciences ,03 medical and health sciences ,Symbiodinium ,030104 developmental biology ,Evolutionary biology ,Genetic marker ,Genetic structure ,Genetics ,Microsatellite ,Allele ,education ,Ecology, Evolution, Behavior and Systematics - Abstract
Symbiodinium are a diverse group of unicellular dinoflagellates that are important nutritional symbionts of reef-building corals. Symbiodinium putative species ('types') are commonly identified with genetic markers, mostly nuclear and chloroplast encoded ribosomal DNA regions. Population genetic analyses using microsatellite loci have provided insights into Symbiodinium biogeography, connectivity and phenotypic plasticity, but are complicated by: (i) a lack of consensus criteria used to delineate inter- vs. intragenomic variation within species; and (ii) the high density of Symbiodinium in host tissues, which results in single samples comprising thousands of individuals. To address this problem, Wham & LaJeunesse (2016) present a method for identifying cryptic Symbiodinium species from microsatellite data based on correlations between allele size distributions and nongeographic genetic structure. Multilocus genotypes that potentially do not recombine in sympatry are interpreted as secondary 'species' to be discarded from downstream population genetic analyses. However, Symbiodinium species delineations should ideally incorporate multiple physiological, ecological and molecular criteria. This is because recombination tests may be a poor indicator of species boundaries in Symbiodinium due to their predominantly asexual mode of reproduction. Furthermore, discontinuous microsatellite allele sizes in sympatry may be explained by secondary contact between previously isolated populations and by mutations that occur in a nonstepwise manner. Limitations of using microsatellites alone to delineate species are highlighted in earlier studies that demonstrate occasional bimodal distributions of allele sizes within Symbiodinium species and considerable allele size sharing among Symbiodinium species. We outline these issues and discuss the validity of reinterpretations of our previously published microsatellite data from Symbiodinium populations on the Great Barrier Reef (Howells et al. 2013).
- Published
- 2016
44. Integrated approach to understanding the onset and pathogenesis of black band disease in corals
- Author
-
Yui Sato, Sara C. Bell, Bette L. Willis, David G. Bourne, and Michael Civiello
- Subjects
0106 biological sciences ,0301 basic medicine ,geography ,geography.geographical_feature_category ,Ecology ,010604 marine biology & hydrobiology ,Virulence ,Black band disease ,Disease ,Coral reef ,Biology ,Microbial consortium ,medicine.disease ,01 natural sciences ,Microbiology ,03 medical and health sciences ,030104 developmental biology ,Microbial ecology ,Infectious disease (medical specialty) ,medicine ,Microbial mat ,skin and connective tissue diseases ,Ecology, Evolution, Behavior and Systematics - Abstract
Emerging infectious diseases are contributing to global declines in coral reef ecosystems, highlighting a growing need for aetiological knowledge to develop effective management strategies. In this review, we focus on black band disease (BBD), one of the most virulent diseases and the only polymicrobial disease so far known to affect corals. A multipartite microbial consortium dominated by Cyanobacteria, but also including sulfur-cycling bacteria, other bacterial groups and members of the Archaea and Eukarya, forms a sulfide-rich anaerobic mat that migrates across the surface of coral colonies, killing the underlying tissues. The polymicrobial nature of the disease challenges classic aetiological approaches to unravelling disease causation. Here, we synthesize current knowledge on the range of pathogens forming the microbial consortium with recent studies on the transmission, biogeochemistry and environmental drivers of BBD to develop a conceptual model of BBD pathogenesis. The model illustrates how the development of BBD virulence factors is linked to a cascade of microbial community shifts and associated functional roles that progressively develop the microbial consortium from comparatively benign cyanobacterial patches to virulent BBD lesions. This review showcases how an approach that integrates multiple key aspects of the disease provides insights essential to elucidating the aetiology of BBD.
- Published
- 2016
45. Imaging the uptake of nitrogen-fixing bacteria into larvae of the coral Acropora millepora
- Author
-
Bette L. Willis, Kimberley A. Lema, Ruth B. Thornton, Peta L. Clode, David G. Bourne, and Matt R. Kilburn
- Subjects
Nitrogen-Fixing Bacteria ,0301 basic medicine ,Cyanobacteria ,Nitrogen ,Short Communication ,Microorganism ,Coral ,Biology ,Microbiology ,03 medical and health sciences ,Acropora millepora ,Nitrogen Fixation ,Botany ,Animals ,14. Life underwater ,In Situ Hybridization, Fluorescence ,Ecology, Evolution, Behavior and Systematics ,fungi ,Anthozoa ,biology.organism_classification ,Vibrio ,030104 developmental biology ,Larva ,Nitrogen fixation ,Diazotroph ,Bacteria - Abstract
Diazotrophic bacteria are instrumental in generating biologically usable forms of nitrogen by converting abundant dinitrogen gas (N-2) into available forms, such as ammonium. Although nitrogen is crucial for coral growth, direct observation of associations between diazotrophs and corals has previously been elusive. We applied fluorescence in situ hybridization (FISH) and nanoscale secondary ion mass spectrometry to observe the uptake of N-15-enriched diazotrophic Vibrio sp. isolated from Acropora millepora into conspecific coral larvae. Incorporation of Vibrio sp. cells was observed in coral larvae after 4-h incubation with enriched bacteria. Uptake was restricted to the aboral epidermis of larvae, where Vibrio cells clustered in elongated aggregations. Other bacterial associates were also observed in epidermal areas in FISH analyses. Although the fate and role of these bacteria requires additional investigation, this study describes a powerful approach to further explore cell associations and nutritional pathways in the early life stages of the coral holobiont.
- Published
- 2015
46. Coral propagation: a review of techniques for ornamental trade and reef restoration
- Author
-
Bette L. Willis, Jonathan A. Barton, and Kate S. Hutson
- Subjects
0106 biological sciences ,0301 basic medicine ,geography ,geography.geographical_feature_category ,Ecology ,010604 marine biology & hydrobiology ,Coral ,fungi ,technology, industry, and agriculture ,Endangered species ,Coral reef ,Management, Monitoring, Policy and Law ,Aquatic Science ,Biology ,01 natural sciences ,Transplantation ,Fishery ,03 medical and health sciences ,030104 developmental biology ,Propagule ,Aquaculture of coral ,Coral reef protection ,Reef - Abstract
Aquaculture of coral offers an alternative to wild harvest for the ornamental trade and shows considerable promise for restoring reefs and preserving biodiversity. Here, we compare advantages and disadvantages of asexually derived fragments versus sexually derived propagules and in situ versus ex situ nursery phases for the ornamental trade and reef restoration. Asexual propagules, sourced from a donor coral colony that is cut into smaller parts and attached to artificial substrate, are most commonly used. The most suitable corals are typically branching species, although fragments from species with other growth forms can be successful, albeit slower growing. Sexually derived propagules are collected from the wild or from colonies in aquaria during spawning, with an artificial substrate provided for settlement. The timing of spawning is known for many broadcast spawning corals, but opportunities for collection of gametes are generally limited to only once or a few times per year. Brooding species with multiple periods of larval release provide better options for culture of sexually derived propagules. Propagation techniques have developed considerably over the past 20 years, yielding faster growth rates, reduced mortality and reduced detachment from substrates. Simple and cost–effective propagation techniques can be used to restore denuded reefs, preserve endangered species, provide live corals to the international ornamental trade, enable livelihood diversification for coastal communities and provide experimental materials for marine research. This review provides a comprehensive synthesis of recent developments in aquaculture propagation techniques for the purpose of ornamental trade and coral reef restoration, including asexual and sexual propagation, nursery and transplantation stages.
- Published
- 2015
47. Elevated CO
- Author
-
Paul A, O'Brien, Hillary A, Smith, Stewart, Fallon, Katharina, Fabricius, Bette L, Willis, Kathleen M, Morrow, and David G, Bourne
- Subjects
Porites ,fungi ,microbiome ,ocean acidification ,Microbiology ,coral ,geographic locations ,Original Research ,volcanic seep - Abstract
Ocean acidification (OA) as a result of increased anthropogenic CO2 input into the atmosphere carries consequences for all ocean life. Low pH can cause a shift in coral-associated microbial communities of pCO2-sensitive corals, however, it remains unknown whether the microbial community is also influenced in corals known to be more tolerant to high pCO2/low pH. This study profiles the bacterial communities associated with the tissues of the pCO2-tolerant coral, massive Porites spp., from two natural CO2 seep sites in Papua New Guinea. Amplicon sequencing of the hypervariable V3-V4 regions of the 16S rRNA gene revealed that microbial communities remained stable across CO2 seep sites (pH = 7.44–7.85) and adjacent control sites (ambient pH = 8.0–8.1). Microbial communities were more significantly influenced by reef location than pH, with the relative abundance of dominant microbial taxa differing between reefs. These results directly contrast with previous findings that increased CO2 has a strong effect on structuring microbial communities. The stable structure of microbial communities associated with the tissues of massive Porites spp. under high pCO2/low pH conditions confirms a high degree of tolerance by the whole Porites holobiont to OA, and suggest that pH tolerant corals such as Porites may dominate reef assemblages in an increasingly acidic ocean.
- Published
- 2018
48. Predation scars may influence host susceptibility to pathogens: evaluating the role of corallivores as vectors of coral disease
- Author
-
Karen M. Chong-Seng, Mia O. Hoogenboom, Morgan S. Pratchett, Bette L. Willis, and Katia J. Nicolet
- Subjects
0106 biological sciences ,Chaetodon plebeius ,Coral ,Porites ,Butterflyfish ,Population ,Snails ,lcsh:Medicine ,Zoology ,010603 evolutionary biology ,01 natural sciences ,Article ,Predation ,Cicatrix ,Animals ,Drupella ,lcsh:Science ,education ,education.field_of_study ,Multidisciplinary ,biology ,010604 marine biology & hydrobiology ,lcsh:R ,biology.organism_classification ,Anthozoa ,Perciformes ,Predatory Behavior ,lcsh:Q ,Skeletal eroding band - Abstract
Infectious diseases not regulated by host density, such as vector-borne diseases, have the potential to drive population declines and extinctions. Here we test the vector potential of the snail Drupella sp. and butterflyfish Chaetodon plebeius for two coral diseases, black band (BBD) and brown band (BrB) disease. Drupella transmitted BrB to healthy corals in 40% of cases immediately following feeding on infected corals, and even in 12% of cases 12 and 24 hours following feeding. However, Drupella was unable to transmit BBD in either transmission treatment. In a field experiment testing the vector potential of naturally-occurring fish assemblages, equivalent numbers of caged and uncaged coral fragments became infected with either BrB, BBD or skeletal eroding band, indicating that corallivorous fish were unlikely to have caused transmission. In aquaria, C. plebeius did not transmit either BBD or BrB, even following extended feeding on both infected and healthy nubbins. A literature review confirmed only four known coral disease vectors, all invertebrates, corroborating our conclusion that polyp-feeding fishes are unlikely to be vectors of coral diseases. This potentially because polyp-feeding fishes produce shallow lesions, not allowing pathogens to invade coral tissues. In contrast, corallivorous invertebrates that create deeper feeding scars increase pathogens transmission.
- Published
- 2017
49. Protected Areas Moderate Diseases of Reef-Building Corals
- Author
-
David H. Williamson, Bette L. Willis, Garry R. Russ, and Joleah B. Lamb
- Subjects
Fishery ,Geography ,geography.geographical_feature_category ,General Medicine ,Reef - Published
- 2015
50. Protected areas mitigate diseases of reef-building corals by reducing damage from fishing
- Author
-
David H. Williamson, Joleah B. Lamb, Garry R. Russ, and Bette L. Willis
- Subjects
Conservation of Natural Resources ,Coral ,Fishing ,Fishing line ,medicine ,Animals ,Ecology, Evolution, Behavior and Systematics ,Ecosystem health ,geography ,geography.geographical_feature_category ,biology ,Coral Reefs ,Ecology ,Marine reserve ,Australia ,Fishes ,technology, industry, and agriculture ,Black band disease ,Biodiversity ,Coral reef ,Anthozoa ,medicine.disease ,biology.organism_classification ,Fishery ,Host-Pathogen Interactions ,Skeletal eroding band - Abstract
Parks and protected areas have been instrumental in reducing anthropogenic sources of damage in terrestrial and aquatic environments. Pathogen invasion often succeeds physical wounding and injury, yet links between the reduction of damage and the moderation of disease have not been assessed. Here, we examine the utility of no-take marine reserves as tools for mitigating diseases that affect reef-building corals. We found that sites located within reserves had fourfold reductions in coral disease prevalence compared to non-reserve sites (80 466 corals surveyed). Of 31 explanatory variables assessed, coral damage and the abundance of derelict fishing line best explained differences in disease assemblages between reserves and non-reserves. Unexpectedly, we recorded significantly higher levels of disease, coral damage, and derelict fishing line in non-reserves with fishing gear restrictions than in those without gear restrictions. Fishers targeting stocks perceived to be less depleted, coupled with enhanced site access from immediately adjacent boat moorings, may explain these unexpected patterns. Significant correlations between the distance from mooring sites and prevalence values for a ciliate disease known to infest wounded tissue (r = −0.65), coral damage (r = −0.64), and the abundance of derelict fishing line (r = −0.85) corroborate this interpretation. This is the first study to link disease with recreational use intensity in a park, emphasizing the need to evaluate the placement of closures and their direct relationship to ecosystem health. Since corals are modular, ecological processes that govern reproductive and competitive fitness are frequently related to colony surface area therefore, even low levels of cumulative tissue loss from progressing diseases pose significant threats to reef coral persistence. Disease mitigation through reductions in physical injury in areas where human activities are concentrated is another mechanism by which protected areas may improve ecosystem resilience in a changing climate.
- Published
- 2015
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