A study published in Nature in estimated that 90 percent of the large predatory fish such as marlin, large cod, large sharks, tuna and swordfish have disappeared from the world's oceans. Overfishing affects not just those fish that are being caught, but the coral ecosystem as a whole. When large predatory fish are overfished, fisheries then turn to smaller herbivorous species such as parrotfish and surgeonfish affects the reef as whole.
These herbivorous fishes play an important role in keeping algal growth in check. If their numbers decline, areas of reef may become overgrown with algae. This also affects coral settlement as the coral larvae need rocky, bare substrate to begin to start a new coral colony. The process of smaller and smaller fish being targeted is known as fishing down the food chain. A study conducted by the ARC Centre of Excellence for Coral Reef Studies at James Cook University compiled a set of surveys over reef sites to investigate the relationship between fish stocks and reef health.
The results they found are worrying. The reef is healthy. This amount of fish was most often found in reef areas where there were fishing rules, such as protected reefs and no-fishing zones. On the basis of this research, several qualitative and quantitative models have been proposed for the effects of algal competition or temperature on the coral microbiome. The DDAM hypothesis dissolved organic carbon, disease, algae and microbes 27 suggests that turf and macroalgae secrete dissolved organic carbon 28 , which increases growth and oxygen consumption of bacteria 29 , 30 but see ref.
Two additional, non-mutually exclusive hypotheses are that algae produce allelochemicals that directly harm corals, with possible downstream effects on the microbiome 20 and that interactions with certain algae lead to transfer of algae-associated microbes to corals 19 , Sea-surface temperatures also strongly impact the coral microbiome 15 , 16 , 24 , While mass coral bleaching caused by high levels of thermal stress has received the greatest attention, even modest increases in temperature appear to make corals more vulnerable to opportunistic bacteria.
Elevated temperatures increase the release of dimethylsulfoniopropionate from corals. Many opportunistic microorganisms chemotax along gradients of dimethylsulfoniopropionate, potentially allowing them to target thermally stressed corals Elevated temperatures also increase expression of virulence genes in some opportunistic bacteria 35 , alter innate immune gene expression in corals 36 and inhibit the protective role of bacteria in the coral mucus These observations have prompted mathematical models of competition between coral mutualists and pathogens, suggesting that temperature variation mediates changes between pathogen- and mutualist-dominated stable states Together, this research strongly suggests that human impacts such as overfishing and nutrient pollution may interact with sea-surface temperatures to cause changes in coral reef benthic communities and their microbiomes that together contribute to coral mortality 17 , 18 , Much of the foundational work on how corals respond to global and local stressors has been done in short-term, small-scale lab and field experiments based at the organismal level for example, refs 16 , 17 , 19 , 24 , Therefore, it is difficult to extrapolate these prior results to determine how factors that are thought to contribute to coral decline interact to alter coral benthic communities and their microbiomes over ecologically realistic temporal and spatial scales.
Therefore, we designed a long-term field experiment to examine how altering herbivory and nutrient pollution impacted coral—algal—microbe interactions within the context of seasonal temperature variation. Specifically, we sought to test the following main hypotheses over ecologically relevant spatial and temporal scales: 1 exclusion of herbivores and nutrient pollution both increase the abundance, and diversity of turf and macroalgae, leading to intensified coral—algal competition and additive increases in coral tissue loss and mortality; 2 coral—algal competition interacts with above-average temperatures to shift coral microbiomes away from their normal configuration and towards distinct, pathogen-dominated stable states; and 3 alterations to the coral microbiome due to increased algal competition or above-average temperatures positively correlate with increased coral disease, and reduced coral growth and survivorship.
To test these hypotheses, we conducted a 3-year field experiment June —August that simulated overfishing and nutrient pollution on a reef in the Florida Keys, USA. We tracked their impacts on the benthic community, coral—microbe dynamics and coral survivorship across multiple seasons.
To simulate nutrient pollution, four 9-m 2 plots of reef benthos were enriched in nitrogen and phosphorus, while four control plots remained at ambient nutrient levels Methods. Enrichment increased nitrogen and phosphorous concentrations approximately four- eightfold above ambient, similar to reefs impacted by nutrient pollution Methods.
This created factorial treatments of: 1 control, 2 herbivore exclusion, 3 enriched nutrients and 4 herbivore exclusion plus enriched nutrients Supplementary Notes ; Supplementary Data 1 sheet b. Herbivore exclusion rapidly increased algal cover up to sixfold, species richness up to threefold Fig. Nutrient pollution only slightly increased algal richness Fig. Overall, removing herbivorous fishes, and to a lesser extent nutrient pollution, facilitated growth of algae known to increase coral tissue loss or mortality via shading, abrasion and allelopathy 38 , P values are from mixed effect models Supplementary Table Data 1c.
To identify how algal communities and nutrient pollution affected the coral microbiome, we collected DNA samples from the surface mucus layer of 80 coral colonies genera Porites, Siderastrea and Agaricia at approximately monthly intervals. Order Synechococcales phylum Cyanobacteria , a proposed coral mutualist 13 , was particularly abundant on control corals.
Increasing algal cover or elevated temperature suppressed the typical, Synechococcus -dominated microbiome of healthy corals and facilitated blooms of other microbes, including many putative opportunists or pathogens Fig.
Alteromonadales, and 10 other orders, many of which were Proteobacteria, increased in abundance as upright algal cover including tall turf algae, cyanobacteria and macroalgae increased. Vibrionales and Oscillatoriales increased in abundance with increasing temperature Fig.
The main pattern we seek to show here is a shift from Synechococcus -dominated communities cyan to dominance by a wide variety of other orders as one moves from left to right along PC1. Points are coloured to reflect the most dominant numerically abundant microbial order in each sample.
Sizes reflect quartiles of microbial community evenness measured by equitability. Parentheses next to each order note the number of samples, in which that order was dominant. Points plot the 1st PC axis a against the relative abundance of Synechococcales cyan squares, dot-dashed line , Proteobacteria orange triangles, dashed line and overall microbial community evenness blue circles, dotted line.
The position of each point, and its associated error bars, represents mean algal cover and temperature, and their s. Coloured polygons enclose suites of taxa whose mean abundance increased with temperature orange or upright algal cover green; Supplementary Data 3 sheets f—h. Vibrionales and Oscillatoriales responded to both temperature and algal cover, but for Vibrionales only temperature was significant.
Herbivore exclusion and ensuing coral—algal contact also increased the relative abundance of many otherwise rare microbial orders Supplementary Table 1 , increasing microbial community richness and evenness Supplementary Data 3 sheet f. In contrast, nutrient pollution suppressed many taxa, allowed fewer bacterial orders to dominate Supplementary Table 1 , and decreased community evenness Supplementary Data 3 sheet f. Principle coordinates analysis PCoA identified transitions from Synechococcus - to Proteobacteria dominance, as the most important axis structuring coral microbiomes First PCoA axis; Fig.
Proteobacteria blooms were accompanied by a drop-off in community evenness Fig. We used random forest analysis, a machine-learning method, to summarize the extent to which the dominant microbe on coral surfaces could be predicted from external conditions such as algal contact and sea-surface temperature. Random forest analysis predicted displacement of Synechococcus by blooms of other microbes with Temperature and upright algal cover including both macroalgae and tall turf algae were the most informative predictor variables Supplementary Data 3 sheet h.
Bacterial opportunists that displaced Synechococcus bloomed at different combinations of temperature and overall upright algal cover Fig. However, conditions favoring different opportunists overlapped, rendering the specific opportunist that displaced Synechococcales partially stochastic and not predictable from random forest analysis of ecological data Supplementary Data 3 sheet h.
Antibiotic-producing bacteria may play an important role in protecting corals from outbreaks of harmful bacteria Actinobacteria, in turn, decreased with increasing algal cover or elevated temperatures, suggesting that these stressors remove an important biotic barrier to potential pathogens Supplementary Fig.
Increasing algal cover or elevated temperatures also shifted the predicted functional profiles of corals towards microbial pathogenesis. According to these estimates, microbiomes subject to algal competition or above-average temperatures became enriched in pathways involved in opportunism for example, cell motility and secretion systems and depleted in pathways for antibiotic production that may help healthy coral microbiomes resist invasion Supplementary Fig.
Increasing upright algal cover was also correlated with predicted increases in the abundance of genes for utilization of glycans and pentose sugars in the coral microbiome Supplementary Fig.
Conversely, upright algal cover was associated with decreases in seven categories of metabolic pathways related to amino acid metabolism and four related to lipid and fatty acid metabolism Supplementary Fig. These data support the idea that increased algal cover promotes growth of microbes on the coral surface that are capable of rapid microbial metabolism of algal sugars 17 , 26 , 32 , Stressful conditions may shift coral microbiomes from one stable state to another We had originally hypothesized that algal competition would produce such a shift in the structure of coral microbiomes.
However, we did not find any evidence for such treatment-induced shifts between alternative stable states Supplementary Fig. Rather, we found that algal contact and increased ambient temperatures reduced the overall stability of the microbiome as a whole. This notion has also been generalized to measure species turnover within individuals over time intra-individual variation.
However, few studies notably ref. Significant microbiome destabilization was also found upon reanalysis of a previous study 19 , in which Porites corals were placed in contact with macroalgae Supplementary Fig. In this long-term experiment, we found that radical changes to the coral microbiome were strongly correlated with coral tissue loss and mortality in the field Fig.
Although corals in control plots grew, gaining Red line marks null expectation of equal mortality across seasons. P values reflect non-parametric t -tests of distances. Direct algal contact increased coral microbiome instability Supplementary Fig. Competition with Dictyota algae caused the most severe microbiome disruptions Supplementary Fig.
Further, as the diversity of algal competitors increased, so did microbiome instability, the prevalence of tissue loss and coral mortality Fig. In Siderastrea corals, algal contact also increased by twofold the prevalence of dark spot syndrome DSS , a coral disease with poorly understood aetiology Fig.
DSS-affected Siderastrea had 5-fold greater prevalence of tissue loss and, on average, lost tissue, while Siderastrea without DSS had positive growth Supplementary Fig. Random Forest analysis predicted coral tissue loss with Because this analysis compared the susceptibility of colonies to tissue loss rather than the timing of tissue loss, temperature was not included as a variable. The abundance of macroalgae and tall turf algae, which increased coral morality Supplementary Fig. The next best predictors were the abundance of Rhodobacterales and Rhodospirallales, two putatively opportunistic microbial orders, both in the Proteobacteria and both commonly enriched in diseased corals for example ref.
In this study, Rhodospirallales were enriched by herbivore exclusion Supplementary Table 1. Together, these data show that the rise of algae following chronic nutrient enrichment and removal of consumer species disrupts coral microbiomes, facilitates disease, increases tissue loss and causes coral death.
Surprisingly, coral mortality caused by simulated overfishing and nutrient pollution was strongly seasonal. Yet this seasonal mortality occurred only when herbivores were removed or nutrients increased, suggesting that local stressors and temperature interact to kill corals. If seasonal temperature variation and local stressors do interact to drive coral mortality, we might expect years in which corals suffer greater sub-bleaching thermal stress to correspond to greater coral mortality.
To put treatment outcomes in the context of seasonal temperature variation and coral thermal stress, we calculated raw sea-surface temperatures for our study site using both the Pathfinder v5. From these we calculated several standard derived measures of coral thermal stress The maximum monthly mean MMM is the average temperature of the warmest month in long-term climate data for our site, excluding the study period that is, — Regressions using local temperature data Supplementary Fig.
This finding suggests that the local MMM may be a critical temperature threshold for the onset of bacterial opportunism. Temperature variation explained differences in microbial community structure over time better than other measured seasonal parameters Supplementary Notes. The accumulation of thermal stress due to periods of above-average temperature also appeared to influence microbial communities.
Cumulative thermal stress also had small, but significant effects on microbial communities after accounting for daily temperature variation. These microbiological changes were probably not due to confounding effects of coral bleaching, as cumulative thermal stress stayed well below the four DHW threshold for mass coral bleaching 5 Supplementary Fig.
Coral mortality patterns showed that nutrient pollution changes the impact of important consumers on reefs. Parrotfishes preyed on However, the ultimate outcome of predation for coral health varied greatly under ambient versus nutrient-enriched conditions.
Because other stressors increased potentially opportunistic Proteobacteria compared with Cyanobacteria primarily Synechococcales , we compared the ratio of these bacterial phyla in bitten corals. The combination of predation and nutrient pollution, but not predation alone, increased the ratio of Proteobacteria relative to Cyanobacteria Fig. Parrotfish predation columns in red reflect samples taken after the first evidence of parrotfish predation. P values are from non-parametric t -tests.
We demonstrate that overfishing and nutrient pollution alter benthic communities, causing coral microbiome disruption, blooms of opportunistic coral pathogens and long-term increases in coral disease, tissue loss and mortality. This experimental framework, which combines classical ecological field experiments with microbial time series, allowed us to test key predictions of how coral reefs respond to human impacts over ecologically important time scales and with much greater microbiological detail than has previously been possible in field experiments.
The results changed our view of how coral microbiomes respond to environmental stressors; uncovered new interactions among corallivory, nutrient pollution and bacterial opportunism; and quantified how local stressors interact with seasonal temperature variation to impact coral microbiomes and, ultimately, coral survivorship. Together, these results show how altering important trophic interactions can fundamentally reorganize coral reefs down to microbial scales, with multiple negative consequences for reef health.
We predicted that simulated overfishing or nutrient pollution would drive distinct benthic community changes and that these benthic changes would additively increase coral mortality. More specifically, we predicted that exclusion of herbivores would lead to large increases in the abundance and diversity of macroalgae.
In contrast, nutrient pollution would only modestly increase macroalgal cover and diversity, instead driving growth of nutrient-limited but unpalatable members of the benthic community such as Cyanobacteria. Similar to past work for example, refs 6 , 7 , 8 , we show that herbivore removal rapidly leads to over sixfold increases in algal abundance and threefold increases in algal diversity, as well as intense coral—algal competition.
Many of the algal genera that increased, such as Sargassum , Dictyota , Amphiroa and Turbinaria , cause coral tissue loss or mortality via shading, abrasion and allelopathy 38 , Nutrient enrichment led to lower overall increases in algal abundance, but facilitated growth of certain taxa such as Cyanobacteria and filamentous turf algae, which can compete intensely with corals However, the consequences of these local stressors for coral mortality deviated greatly from our prior expectations.
We expected herbivore removal and nutrient pollution to have additive effects on corals, with their combined effects causing much greater coral mortality than either individually. Yet, while all treatments significantly increased coral tissue loss and coral mortality above controls, levels of mortality and tissue loss were similar under nutrient pollution, herbivore removal or combined treatments.
This pattern likely resulted from different mechanisms of coral tissue loss and mortality operating in the different treatments. In the nutrient pollution treatment, we traced coral decline to an unexpected interaction among corallivory, nutrient pollution, bacterial opportunism and coral death. Parrotfishes are key herbivores on reefs, but also prey on corals as part of their diet This corallivory is relatively intense in the Florida Keys, USA where populations of parrotfishes are robust Here we found that Porites corals bitten by parrotfish lost tissue and died at much higher rates under nutrient-enriched conditions than in ambient conditions.
In fact, parrotfish corallivory caused no mortality in ambient nutrient conditions. Microbial community shifts towards Proteobacteria on the surface of bitten and nutrient-enriched corals but not bitten corals in ambient nutrient conditions suggest that increased bacterial opportunism following wounding may cause this increased tissue loss and mortality. It is not clear whether the observed increase in Proteobacteria is due to a proliferation of pathogens vectored by parrotfish as suggested for butterflyfishes 50 or represents a more general nutrient-driven increase in susceptibility to infection following wounding.
In either case, this unexpected observation is especially worrisome, as it shows that nutrient pollution turns parrotfishes, which are normally thought of as coral allies, into agents of mortality for some corals. This finding is important given that nutrient pollution is a problem on many reefs and that restoration of parrotfish populations is an important goal as part of coral conservation and management Our data suggest that restoration of parrotfishes without efforts to combat water quality issues could have surprisingly negative consequences.
When herbivorous fishes were removed, coral—algal competition and disruption of the coral microbiome appeared to be the main drivers of coral mortality. We showed that algal contact increases coral microbiome richness, facilitates growth of many conditionally rare taxa and increases overall microbiome destabilization. In keeping with the prediction that local algal competition will increase disease 27 , 33 for example, through dissolved organic carbon 27 or other mechanisms 33 , we found that the presence of algal competition corresponded to an increased prevalence of DSS 52 in Siderastrea corals.
These algae-induced changes to coral microbiology and disease prevalence correlate with increased long-term coral tissue loss and mortality in the field. Thus, our work shows that microbial interactions that were predicted to be important drivers of coral mortality in laboratory studies can be induced by overfishing and nutrient pollution, with important and ecologically meaningful effects for the long-term health of corals.
Our long-term results also provide strong contrasts with existing models of coral microbiome dynamics. Qualitative and quantitative models of the coral microbiome have generally assumed that stress would shift coral microbiomes towards stable states dominated by pathogens for example, ref. While we did confirm the general idea that multiple stressors increase the abundance of fast-growing opportunists on the coral surface, our data do not support a model in which overfishing and nutrient pollution, ensuing algal competition, or seasonal temperature variation drive coral microbiomes to specific alternative stable states.
Instead, we found that above-average temperatures or algal contact destabilized the microbiome, shifting microbial communities from a stable to an unstable configuration. This finding mirrors recent reports in disturbed human and primate microbiomes 42 , 53 , suggesting an underexplored pattern that may be common to many host—microbe systems.
In other animal systems, increased microbiome variability during stress is thought to reflect decreased ability of the host, or its native microbiota, to regulate microbial community composition Here we show that algal competition and periods of above-average temperature intersect to influence, which bacteria dominate coral microbiomes.
Both of these factors promote stochastic blooms of opportunistic bacteria that displace typically dominant members of the coral surface mucus layer. This is interesting because some coral pathogens, such as Vibrio coralliilyticus have been shown to suppress coral innate immune pathways Similarly, many reports have quantified the anti-microbial properties of coral mucus 14 , including the contribution of antibiotic-producing Actinobacteria Our long-term data set suggests that Actinobacteria are important for suppressing opportunists, as outbreaks of Proteobacteria opportunists were more common when Actinobacteria were in low abundance on the coral surface.
In agreement with this model, corals exposed to above-average temperature or algal contact showed lower predicted abundances of microbial pathways involved in antibiotic production. Algal contact also reduced the abundance of Actinobacteria, suggesting that algal competition following herbivore removal will lower the natural defenses of corals against potential pathogens, including genera such as Vibrio that are especially problematic at high temperatures.
Finally, we find that local overfishing and nutrient pollution interact with seasonal temperature variation to render corals more vulnerable to blooms of harmful bacteria and increased mortality during the warmest months.
In contrast, mild, sub-bleaching thermal stress during summer months did not increase coral mortality under control conditions.
Connections between local stressors and temperature variation are often discussed in the field in the context of climate change, and have been incorporated into models of reef vulnerability or resilience 55 , 56 , as well as coral disease susceptibility However, experimental evidence connecting laboratory studies of microbial dynamics to coral mortality in the field has been lacking.
In our data, bacterial opportunism increased at temperatures around the local MMM, consistent with past predictions of a threshold at which bacterial pathogenesis becomes especially problematic based on laboratory studies Also in agreement with previous coral microbiome field studies 16 , we observe blooms of Vibrio during periods of above-average temperatures.
Motility genes were enriched in these microbiomes, supporting the idea that chemotaxis towards thermally stressed corals, previously shown in microfluidic experiments, may play an important role in coral microbiome dynamics at above-average temperatures We extend these observations both by documenting how various combinations of algal competition and temperature favour different bacterial opportunists, and linking these blooms to losses of protective symbionts such as Actinobacteria caused by local stressors.
Finally, our data connects microbiome destabilization caused by these blooms to coral tissue loss in the experiment overall, and especially in periods of high temperature.
Thus, multiple lines of evidence collected in this study support an ecologically relevant role for coral microbiomes in mediating coral mortality driven by the intersection of local stressors and seasonal temperature variation. Together, our results provide experimental data linking prevailing models of how human impacts alter reef ecology 6 with models of how coral microbiomes respond to algal competition and temperature 15 , They show that overfishing and nutrient pollution increase the vulnerability of corals to blooms of opportunistic microorganisms and that the impacts of these local stressors are exacerbated by above-average temperatures.
Importantly, the coral species that suffered high mortality rates in our experiments are now some of the most abundant on Caribbean reefs 57 , Thus, some coral species that have withstood the recent decline of more vulnerable relatives may nonetheless be susceptible to increasing local stressors.
Clearly, sufficiently extreme thermal anomalies and mass bleaching events will kill corals regardless of local factors. However, our work suggests that conserving natural trophic interactions by protecting herbivorous fishes and reducing nutrient pollution may help stabilize coral microbiomes and shield corals against temperature-driven bacterial opportunism and mortality, at least in the near term To simulate the effects of overfishing, nutrient loading or the combination of these stressors, we conducted a 3-year field experiment.
Four pairs of 9-m 2 plots were established. One member of each of these pairs was enriched with nitrogen and phosphorous, while the other remained at ambient nutrient levels Supplementary Fig. Each 9-m 2 plot was delineated into nine 1-m 2 subplots with metal nails driven into the reef at the corners and centre of each plot.
The locations of the plots were selected such that initial variation in rugosity and algal cover within each subplot was minimal. Within each plot, two randomly selected subplots were enclosed with herbivore exclosures, while two other random subplots were selected as exclosure controls. Exclosure controls were fitted with open-topped exclosures. These controls allowed access by herbivorous fishes, but acted as controls for other potential artifacts of the cages.
All exclosures were made of plastic-coated wire mesh with 2. Smaller or juvenile herbivorous fishes are able to enter the exclosures, but these smaller herbivores generally contribute little to overall grazing rates on reefs and have minimal impacts on the algal communities In addition, access by smaller herbivores reflects patterns seen under intensive fishing, in which larger fish species are preferentially harvested while leaving smaller size classes of fish 60 , We scrubbed both exclosures and exclosure controls every 4—6 weeks to remove fouling organisms.
Nutrient pollution was simulated using slow-release fertilizer diffusers applied to each nutrient enrichment plot. Each diffuser was a cm diameter PVC tube, perforated with six 1. The open ends of the PVC tube were wrapped in fine plastic mesh to keep fertilizer pellets inside, but allow diffusion of soluble nutrients.
PVC enrichment tubes were attached to each metal nail within the 9-m 2 enrichment plots for a total of 25 enrichment tubes per enrichment plot. Nutrients were replaced every 30—40 days to ensure continued delivery of N and P. Previous studies have shown Osmocote delivery using similar methods to be an effective way of enriching water column nutrients in benthic systems for example, ref. Nitrogen and phosphorus levels were assessed in the water column above each enrichment and control plot as in ref.
We also assessed nutrient enrichment efficiency by analysing tissue carbon:nitrogen C:N levels in the common alga Dictyota menstrualis. The nutrient content of macroalgae such as D. We collected D. Nutrient data from both water and algal tissue for each replicate were averaged across summers for statistical analysis via analysis of variance ANOVA. Divers slowly swam the length of each transect counting individuals of the different herbivorous fishes in the genera Sparisoma , Scarus , Acanthurus and Kyphosus.
The study calls for a broader perspective in coral reef restoration that incorporates fundamental ecological processes into management actions.
The Center for Biological Diversity is a national, nonprofit conservation organization with more than 1. Go back. More press releases. Abel Valdivia, , avaldivia biologicaldiversity.
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