Anthropogenic nutrient enrichment affects the biogeochemical cycles and nutrient stoichiometry of coastal ecosystems and is often associated with coral reef decline. However, the mechanisms by which dissolved inorganic nutrients, and especially nitrogen forms (ammonium versus nitrate) can disturb the association between corals and their symbiotic algae are subject to controversial debate. Here, we investigated the coral response to varying N : P ratios, with nitrate or ammonium as a nitrogen source. We showed significant differences in the carbon acquisition by the symbionts and its allocation within the symbiosis according to nutrient abundance, type and stoichiometry. In particular, under low phosphate concentration (0.05 mM), a 3 mM nitrate enrichment induced a significant decrease in carbon fixation rate and low values of carbon translocation, compared with control conditions (N : P ¼ 0.5 : 0.05), while these processes were significantly enhanced when nitrate was replaced by ammonium. A combined enrichment in ammonium and phosphorus (N : P ¼ 3 : 1) induced a shift in nutrient allocation to the symbionts, at the detriment of the host. Altogether, these results shed light into the effect of nutrient enrichment on reef corals. More broadly, they improve our understanding of the consequences of nutrient loading on reef ecosystems, which is urgently required to refine risk management strategies.

During the 20th century, seawater temperatures have significantly increased, leading to profound alterations in biogeochemical cycles and ecosystem processes. Elevated temperatures have also caused massive bleaching (symbiont/pigment loss) of autotrophic symbioses, such as in coral-dinoflagellate association. As symbionts provide most nutrients to the host, their expulsion during bleaching induces host starvation. However, with the exception of carbon, the nutritional impact of bleaching on corals is still unknown, due to the poorly understood requirements in inorganic nutrients during stress. We therefore assessed the uptake rates of nitrogen and phosphate by five coral species maintained under normal and thermal stress conditions. Our results showed that nitrogen acquisition rates were significantly reduced during thermal stress, while phosphorus uptake rates were significantly increased in most species, suggesting a key role of this nutrient. Additional experiments showed that during thermal stress, phosphorus was required to maintain symbiont density and photosynthetic rates, as well as to enhance the translocation and retention of carbon within the host tissue. These findings shed new light on the interactions existing between corals and inorganic nutrients during thermal stress, and highlight the importance of phosphorus for symbiont health.

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Reef building corals can host different symbiont genotypes (clades), and form distinct holobionts in response to environmental changes. Studies on the functional significance of genetically different symbionts have focused on the thermal tolerance rather than on the nutritional significance. Here, we characterized the nitrogen and carbon assimilation rates, the allocation patterns of these nutrients within the symbiosis, and the trophic condition of two distinct holobionts of Stylophora pistillata: one associated with Symbiodinium clade A in shallow reefs and the other one associated with clade C in mesophotic reefs. The main findings are that: (1) clade C-symbionts have a competitive advantage for the acquisition of carbon at low irradiance compared to clade A-symbionts; (2) light is however the primary factor that determines the positive relationship between the amount of carbon fixed in photosynthesis by the symbionts and the amount of carbon translocated to the host; and (3) by contrast, the dominant Symbiodinium type preferentially determines a negative relationship between rates of coral feeding and nitrogen assimilation, although light still plays a relevant role in this relationship. Clade C-holobionts had indeed higher heterotrophic capacities, but lower inorganic nitrogen assimilation rates than clade A-holobionts, at all light levels. Broadly, our results show that the assimilation and translocation rates of inorganic carbon and nitrogen are clade and light-dependent. In addition, the capacity of S. pistillata to form mesophotic reefs in the Red Sea relies on its ability to select Symbiodinium clade C, as this symbiont type is more efficient to fix carbon at low light.

Corallivory is the predation of coral mucus, tissue, and skeleton by fishes and invertebrates, and a source of chronic stress for many reef-building coral species. Corallivores often prey on corals repeatedly, and this predation induces wounds that require extensive cellular resources to heal. The effects of corallivory on coral growth, reproduction, and community dynamics are well-documented, and often result in reduced growth rates and fitness. Given the degree of anthropogenic pressures that threaten coral reefs, it is now imperative to focus on understanding how corallivory interacts with anthropogenic forces to alter coral health and community dynamics. For example, coral bleaching events that stem from global climate change often reduce preferred corals species for many corallivorous fishes. These reductions in preferred prey may result in declines in populations of more specialized corallivores while more generalist corallivores may increase. Corallivory may also make corals more susceptible to thermal stress and exacerbate bleaching. At local scales, overfishing depletes corallivorous fish stocks, reducing fish corallivory and bioerosion, whilst removing invertivorous fishes and allowing population increases in invertebrate corallivores (e.g., urchins, Drupella spp.). Interactive effects of local stressors, such as overfishing and nutrient pollution, can alter the effect of corallivory by increasing coral-algal competition and destabilizing the coral microbiome, subsequently leading to coral disease and mortality. Here, we synthesize recent literature of how global climate change and local stressors affect corallivore populations and shape the patterns and effect of corallivory. Our review indicates that the combined effects of corallivory and anthropogenic pressures may be underappreciated and that these interactions often drive changes in coral reefs on scales from ecosystems to microbes. Understanding the ecology of coral reefs in the Anthropocene will require an increased focus on how anthropogenic forcing alters biotic interactions, such as corallivory, and the resulting cascading effects on corals and reef ecosystems.