Laurie Raymundo

Resilience of Coral-Associated Bacterial Communities Exposed to Fish Farm Effluent

Background The coral holobiont includes the coral animal, algal symbionts, and associated microbial community. These microbes help maintain the holobiont homeostasis; thus, sustaining robust mutualistic microbial communities is a fundamental part of long-term coral reef survival. Coastal pollution is one major threat to reefs, and intensive fish farming is a rapidly growing source of this pollution. Methodology & Principal Findings We investigated the susceptibility and resilience of the bacterial communities associated with a common reef-building coral, Porites cylindrica, to coastal pollution by performing a clonally replicated transplantation experiment in Bolinao, Philippines adjacent to intensive fish farming. Ten fragments from each of four colonies (total of 40 fragments) were followed for 22 days across five sites: a well-flushed reference site (the original fragment source); two sites with low exposure to milkfish (Chanos chanos) aquaculture effluent; and two sites with high exposure. Elevated levels of dissolved organic carbon (DOC), chlorophyll a, total heterotrophic and autotrophic bacteria abundance, virus like particle (VLP) abundances, and culturable Vibrio abundance characterized the high effluent sites. Based on 16S rRNA clone libraries and denaturing gradient gel electrophoresis (DGGE) analysis, we observed rapid, dramatic changes in the coral-associated bacterial communities within five days of high effluent exposure. The community composition on fragments at these high effluent sites shifted towards known human and coral pathogens (i.e. Arcobacter, Fusobacterium, and Desulfovibrio) without the host corals showing signs of disease. The communities shifted back towards their original composition by day 22 without reduction in effluent levels. Significance This study reveals fish farms as a likely source of pathogens with the potential to proliferate on corals and an unexpected short-term resilience of coral-associated bacterial communities to eutrophication pressure. These data highlight a need for improved aquaculture practices that can achieve both sustainable industry goals and long-term coral reef survival.

Global coral disease prevalence associated with sea temperature anomalies and local factors

Coral diseases are taking an increasing toll on coral reef structure and biodiversity and are important indicators of declining health in the oceans. We implemented standardized coral disease surveys to pinpoint hotspots of coral disease, reveal vulnerable coral families and test hypotheses about climate drivers from 39 locations worldwide. We analyzed a 3 yr study of coral disease prevalence to identify links between disease and a range of covariates, including thermal anomalies (from satellite data), location and coral cover, using a Generalized Linear Mixed Model. Prevalence of unhealthy corals, i.e. those with signs of known diseases or with other signs of compromised health, exceeded 10% on many reefs and ranged to over 50% on some. Disease prevalence exceeded 10% on 20% of Caribbean reefs and 2.7% of Pacific reefs surveyed. Within the same coral families across oceans, prevalence of unhealthy colonies was higher and some diseases were more common at sites in the Caribbean than those in the Pacific. The effects of high disease prevalence are potentially extensive given that the most affected coral families, the acroporids, faviids and siderastreids, are among the major reef-builders at these sites. The poritids and agaricids stood out in the Caribbean as being the most resistant to disease, even though these families were abundant in our surveys. Regional warm temperature anomalies were strongly correlated with high disease prevalence. The levels of disease reported here will provide a much-needed local reference point against which to compare future change.

Growth Anomalies on the Coral Genera Acropora and Porites Are Strongly Associated with Host Density and Human Population Size across the Indo-Pacific

Growth anomalies (GAs) are common, tumor-like diseases that can cause significant morbidity and decreased fecundity in the major Indo-Pacific reef-building coral genera, Acropora and Porites. GAs are unusually tractable for testing hypotheses about drivers of coral disease because of their pan-Pacific distributions, relatively high occurrence, and unambiguous ease of identification. We modeled multiple disease-environment associations that may underlie the prevalence of Acropora growth anomalies (AGA) (n = 304 surveys) and Porites growth anomalies (PGA) (n = 602 surveys) from across the Indo-Pacific. Nine predictor variables were modeled, including coral host abundance, human population size, and sea surface temperature and ultra-violet radiation anomalies. Prevalence of both AGAs and PGAs were strongly host density-dependent. PGAs additionally showed strong positive associations with human population size. Although this association has been widely posited, this is one of the first broad-scale studies unambiguously linking a coral disease with human population size. These results emphasize that individual coral diseases can show relatively distinct patterns of association with environmental predictors, even in similar diseases (growth anomalies) found on different host genera (Acropora vs. Porites). As human densities and environmental degradation increase globally, the prevalence of coral diseases like PGAs could increase accordingly, halted only perhaps by declines in host density below thresholds required for disease establishment.

Coral disease in Micronesian reefs: a link between disease prevalence and host abundance.

Current information regarding the effects of coral diseases on Indo-Pacific reefs lags behind that of the Caribbean. Considering that these reefs are geographically widespread, speciose, often highly influenced by human coastal populations, and inadequately monitored, developing a baseline database is a primary management issue for local scientists. In a first attempt to quantify diseases in Micronesia, Guam reefs were assessed for disease prevalence, host abundance, and community structure. Surveys of 15 reefs revealed 6 disease states affecting 8 families of reef-building corals and highly variable prevalence between sites, ranging from 0.2 to 12.6%. Guam reefs are taxonomically diverse but dominated by the genus Porites. Coral generic host abundance showed a significant and positive link with total disease prevalence. Five out of 6 of the observed disease states affected Porites spp. (mean prevalence within the genus: 6.14 +/- 0.88%), and acroporids and pocilloporids also showed high susceptibility. As the coral genera currently most affected by diseases are those providing the most structure to Guams reefs, disease has the potential to have significant long-term effects, highlighting an urgent need for proactive management.

Local-scale projections of coral reef futures and implications of the Paris Agreement

Increasingly frequent severe coral bleaching is among the greatest threats to coral reefs posed by climate change. Global climate models (GCMs) project great spatial variation in the timing of annual severe bleaching (ASB) conditions; a point at which reefs are certain to change and recovery will be limited. However, previous model-resolution projections (~1 × 1°) are too coarse to inform conservation planning. To meet the need for higher-resolution projections, we generated statistically downscaled projections (4-km resolution) for all coral reefs; these projections reveal high local-scale variation in ASB. Timing of ASB varies >10 years in 71 of the 87 countries and territories with >500 km2 of reef area. Emissions scenario RCP4.5 represents lower emissions mid-century than will eventuate if pledges made following the 2015 Paris Climate Change Conference (COP21) become reality. These pledges do little to provide reefs with more time to adapt and acclimate prior to severe bleaching conditions occurring annually. RCP4.5 adds 11 years to the global average ASB timing when compared to RCP8.5; however, >75% of reefs still experience ASB before 2070 under RCP4.5. Coral reef futures clearly vary greatly among and within countries, indicating the projections warrant consideration in most reef areas during conservation and management planning.

Influence of marine reserves on coral disease prevalence.

Predicted increases in disease with climate warming highlight the need for effective management strategies to mitigate disease effects in coral communities. We examined the role of marine protected areas (MPAs) in reducing disease in corals and the hypothesis that the composition of fish communities can influence coral health, by comparing disease prevalence between MPA and non-protected (control) reefs in Palau. Overall, the prevalence of diseases pooled, as well as the prevalence of skeletal eroding band (SEB), brown band disease (BrB) and growth anomalies (GAs) individually in major disease hosts (families Acroporidae and Poritidae), were not significantly reduced within MPAs. In fact, the prevalence of SEB was 2-fold higher within MPAs overall; however, the 4 studied MPAs were ineffective in enhancing coral assemblage or fish stock health. A negative association between the prevalence of SEB and richness of a fish species targeted by fishers in Palau highlights the potential role that well-managed MPAs could play in reducing SEB. The composition of coral communities and their susceptibility to bleaching also influenced the prevalence of disease on the studied reefs. The prevalence of diseases pooled and SEB were positively associated with the cover of major disease hosts (families Acroporidae and Poritidae), and the prevalence of BrB and bleaching were also positively associated. Although our study did not show positive effects of MPAs on coral heath, we did identify the potential for increased fish diversity within MPAs to reduce coral disease. Our study also highlights the complexity of relationships between fish assemblages, coral community composition and coral health on Indo-Pacific reefs.

Link between sewage-derived nitrogen pollution and coral disease severity in Guam

The goals of this study were to evaluate the contribution of sewage-derived N to reef flat communities in Guam and to assess the impact of N inputs on coral disease. We used stable isotope analysis of macroalgae and a soft coral, sampled bimonthly, as a proxy for N dynamics, and surveyed Porites spp., a dominant coral taxon on Guams reefs, for white syndrome disease severity. Results showed a strong influence of sewage-derived N in nearshore waters, with δ(15)N values varying as a function of species sampled, site, and sampling date. Increases in sewage-derived N correlated significantly with increases in the severity of disease among Porites spp., with δ(15)N values accounting for more than 48% of the variation in changes in disease severity. The anticipated military realignment and related population increase in Guam are expected to lead to increased white syndrome infections and other coral diseases.

Unprecedented coral bleaching across the Marianas Archipelago

In 1998, many reefs around the world experienced severe, widespread bleaching and mortality coinciding with anomalously high sea surface temperatures (SSTs). The Marianas Archipelago was an exception in the Indo-Pacific region in which SSTs remained within normal ranges during this period (Rayner et al. 2006). Prior to 1998 and during non-El Niño years, surveys across the Marianas reported mild to moderate bleaching (68 % of taxa showed signs of bleaching in 1994; Paulay and Benayahu 1999). Since 1998, cumulative evidence from published and anecdotal reports suggests that Marianas reefs have not experienced extensive impacts from coral bleaching over the past two decades (Burdick et al. 2008; P. Houk pers. obs). We report the first known severe, widespread bleaching and mortality event across the three largest islands in the lower Marianas Archipelago: Guam, Rota, and Saipan (Fig. 1). In 2013, 85 % of taxa on nearshore reefs showed signs of bleaching. The 2013 bleaching event coincided with local offshore SSTs exceeding the maximum monthly mean by 0.5–1.6 C, from July 2013 through October 2013, ending after Typhoon Francisco formed southwest of Guam. The National Weather Service monitoring recorded wind speeds ~2 m s slower than monthly averages in July and August. This produced sustained, low wave energy along the windward (eastern) side of the islands simultaneously with elevated SSTs. As global SSTs continue to increase, reefs worldwide will remain vulnerable to bleaching events. Understanding differential responses among taxa and reefs to better predict bleachinginduced changes is a critical first step to managing for reef resilience and promoting recovery from such events.

Effects of Coralliophila violacea on tissue loss in the scleractinian corals Porites spp. depend on host response.

We investigated interactions between the corallivorous gastropod Coralliophila violacea and its preferred hosts Porites spp. Our objectives were to experimentally determine whether tissue loss could progress in Porites during or after Coralliophila predation on corals with and without tissue loss and to histologically document snail predation. In 64% of feeding scars, tissue regenerated within 3 wk, leaving no trace of predation. However, in roughly 28% of scars, lesions progressed to subacute tissue loss resembling white syndrome. In feeding experiments, scars from snails previously fed diseased tissue developed progressive tissue loss twice as frequently as scars from snails previously fed healthy tissue. Scars from previously healthy-fed snails were 3 times as likely to heal as those from previously diseased-fed snails. Histology revealed marked differences in host responses to snails; P. cylindrica manifested a robust inflammatory response with fewer secondary colonizing organisms such as algae, sponges, and helminths, whereas P. rus showed no evident inflammation and more secondary colonization. We conclude that lesion progression associated with Coralliophila may be associated with secondary colonization of coral tissues damaged by predator-induced trauma and necrosis. Importantly, variation at the cellular level should be considered when explaining interspecific differences in host responses in corals impacted by phenomena such as predation.

Contrasting Lesion Dynamics of White Syndrome among the scleractinian corals Porites spp

White syndrome (WS) is currently the most prevalent disease of scleractinian corals in the Indo-Pacific region, with an ability to exist in both epizootic and enzootic states. Here, we present results of an examination of WS lesion dynamics and show that potentially associated traits of host morphology (i.e., branching vs. massive), lesion size, and tissue deposition rate influence disease severity and recovery. Lesion healing rate was positively correlated with initial lesion size in both morphologies, but the rate at which lesions healed differed between morphologies. New lesions in branching Porites cylindrica appeared less frequently, were smaller and healed more quickly, but were more abundant than in closely-related massive Porites sp(p). The positive association between lesion size and healing rate was partly explained by geometry; branching limited lesion maximum size, and larger lesion margins contained more polyps producing new tissue, resulting in faster healing. However, massive colonies deposited tissue more slowly than branching colonies, resulting in slower recovery and more persistent lesions. Corallite size and density did not differ between species and did not, therefore, influence healing rate. We demonstrated multiple modes of pathogen transmission, which may be influenced by the greater potential for pathogen entrainment in branching vs. massive morphologies. We suggest that attributes such as colony morphology and species-specific growth rates require consideration as we expand our understanding of disease dynamics in colonial organisms such as coral.