Landscape-scale patterns of nutrient enrichment in a coral reef ecosystem: implications for coral to algae phase shifts.

Nutrient pollution is altering coastal ecosystems worldwide. On coral reefs, excess nutrients can favor the production of algae at the expense of reef-building corals, yet the role of nutrients in driving community changes such as shifts from coral to macroalgae is not well understood. Here we investigate the potential role of anthropogenic nutrient loading in driving recent coral-to-macroalgae phase shifts on reefs in the lagoons surrounding the Pacific island of Moorea, French Polynesia. We use nitrogen (N) tissue content and stable isotopes (δ15 N) in an abundant macroalga (Turbinaria ornata) together with empirical models of nutrient discharge to describe spatial and temporal patterns of nutrient enrichment in the lagoons. We then employ time series data to test whether recent increases in macroalgae are associated with nutrients. Our results revealed that patterns of N enrichment were linked to several factors, including rainfall, wave-driven circulation, and distance from anthropogenic nutrient sources, especially human sewage. Reefs near large watersheds, where inputs of N from sewage and agriculture are high, have been consistently enriched in N for at least the last decade. In many of these areas, corals have decreased and macroalgae have increased, while reefs with lower levels of N input have maintained high cover of coral and low cover of macroalgae. Importantly, these patchy phase shifts to macroalgae have occurred despite substantial island-wide increases in the density and biomass of herbivorous fishes over the time period. Together, these results indicate that nutrient loading may be an important driver of coral-to-macroalgae phase shifts in the lagoons of Moorea even though the reefs harbor an abundant and diverse herbivore assemblage. These results emphasize the important role that bottom-up factors can play in driving coral-to-macroalgae phase shifts and underscore the critical importance of watershed management for reducing inputs of nutrients and other land-based pollutants to coral reef ecosystems.

Adam TC ，Burkepile DE ，Holbrook SJ ，Carpenter RC ，Claudet J ，Loiseau C ，Thiault L ，Brooks AJ ，Washburn L ，Schmitt RJ ... -  《ECOLOGICAL APPLICATIONS》

Spatial covariation in nutrient enrichment and fishing of herbivores in an oceanic coral reef ecosystem.

Both natural and anthropogenic stressors are increasing on coral reefs, resulting in large-scale loss of coral and potential shifts from coral- to macroalgae-dominated community states. Two factors implicated in shifts to macroalgae are nutrient enrichment and fishing of reef herbivores. Although either of these factors alone could facilitate establishment of macroalgae, reefs may be particularly vulnerable to coral-to-algae phase shifts in which strong bottom-up forcing from nutrient enrichment is accompanied by a weakening of herbivore control of macroalgae via intense fishing. We explored spatial heterogeneity and covariance in these drivers on reefs in the lagoons of Moorea, French Polynesia, where the local fishery heavily targets herbivorous fishes and there are spatially variable inputs of nutrients from agricultural fertilizers and wastewater systems. Spatial patterns of fishing and nutrient enrichment were not correlated at the two landscape scales we examined: among the 11 interconnected lagoons around the island or among major habitats (fringing reef, mid-lagoon, back reef) within a lagoon. This decoupling at the landscape scale resulted from patterns of covariation between enrichment and fishing that differed qualitatively between cross-shore and long-shore directions. At the cross-shore scale, nutrient enrichment declined but fishing increased from shore to the crest of the barrier reef. By contrast, nutrient enrichment and fishing were positively correlated in the long-shore direction, with both increasing with proximity to a pass in the barrier reef. Contrary to widespread assumptions in the scientific literature that human coastal population density correlates with impact on marine ecosystems and that fishing effort declines linearly with distance from the shore, these local stressors produced a complex spatial mosaic of reef vulnerabilities. Our findings support spatially explicit management involving the control of anthropogenic nutrients and strategic reductions in fishing pressure on herbivores by highlighting specific areas to target for management actions.

Holbrook SJ ，Wencélius J ，Dubel AK ，Adam TC ，Cook DC ，Hunter CE ，Lauer M ，Lester SE ，Miller SD ，Rassweiler A ，Schmitt RJ ... -  《-》

Priority effects in coral-macroalgae interactions can drive alternate community paths in the absence of top-down control.

The outcomes of species interactions can vary greatly in time and space with the outcomes of some interactions determined by priority effects. On coral reefs, benthic algae rapidly colonize disturbed substrate. In the absence of top-down control from herbivorous fishes, these algae can inhibit the recruitment of reef-building corals, leading to a persistent phase shift to a macroalgae-dominated state. Yet, corals may also inhibit colonization by macroalgae, and therefore the effects of herbivores on algal communities may be strongest following disturbances that reduce coral cover. Here, we report the results from experiments conducted on the fore reef of Moorea, French Polynesia, where we: (1) tested the ability of macroalgae to invade coral-dominated and coral-depauperate communities under different levels of herbivory, (2) explored the ability of juvenile corals (Pocillopora spp.) to suppress macroalgae, and (3) quantified the direct and indirect effects of fish herbivores and corallivores on juvenile corals. We found that macroalgae proliferated when herbivory was low but only in recently disturbed communities where coral cover was also low. When coral cover was <10%, macroalgae increased 20-fold within 1 year under reduced herbivory conditions relative to high herbivory controls. Yet, when coral cover was high (50%), macroalgae were suppressed irrespective of the level of herbivory despite ample space for algal colonization. Once established in communities with low herbivory and low coral cover, macroalgae suppressed recruitment of coral larvae, reducing the capacity for coral replenishment. However, when we experimentally established small juvenile corals (2 cm diameter) following a disturbance, juvenile corals inhibited macroalgae from invading local neighborhoods, even in the absence of herbivores, indicating a strong priority effect in macroalgae-coral interactions. Surprisingly, fishes that initially facilitated coral recruitment by controlling algae had a net negative effect on juvenile corals via predation. Corallivores reduced the growth rates of corals exposed to fishes by ~30% relative to fish exclosures, despite increased competition with macroalgae within the exclosures. These results highlight that different processes are important for structuring coral reef ecosystems at different successional stages and underscore the need to consider multiple ecological processes and historical contingencies to predict coral community dynamics.

Adam TC ，Holbrook SJ ，Burkepile DE ，Speare KE ，Brooks AJ ，Ladd MC ，Shantz AA ，Vega Thurber R ，Schmitt RJ ... -  《-》

Potential impacts of anthropogenic nutrient enrichment on coral reefs in the South China Sea: evidence from nutrient and chlorophyll a levels in seawater.

Guo J ，Yu K ，Wang Y ，Zhang R ，Huang X ，Qin Z ... -  《-》

Herbivory, connectivity, and ecosystem resilience: response of a coral reef to a large-scale perturbation.

Adam TC ，Schmitt RJ ，Holbrook SJ ，Brooks AJ ，Edmunds PJ ，Carpenter RC ，Bernardi G ... -  《PLoS One》