Limited phosphorus availability is the Achilles heel of tropical reef corals in a warming ocean

Ezzat, Leïla; Maguer, Jean‐François; Grover, Renaud; Ferrier‐Pagés, Christine

doi:10.1038/srep31768

Cited by 87 publications

(97 citation statements)

References 74 publications

(93 reference statements)

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“…It adds to the growing body of evidence that the chemical form of N, as well as its concentration, may play a large role in the physiological response of corals to N enrichment (Ezzat et al, ; Shantz & Burkepile, ). The only detectable effect of thermal stress on NH 4 ‐enriched corals was a significant decrease in

{NH}_{4}^{+}

uptake rates, consistent with previous studies reporting an impairment of inorganic nutrient uptake by stressed corals (Ezzat, Maguer et al, ; Godinot et al, ).…”

Section: Discussionsupporting

confidence: 90%

“…Conversely, corals under control conditions were affected by increased temperatures and showed significant decreases in chlorophyll, symbiont density, protein content and rates of gross photosynthesis and ammonium uptake (Ezzat, Maguer et al, ; Godinot et al, ; Hoegh‐Guldberg & Smith, ). However, grazing rates as well as assimilation of heterotrophic nutrients from zooplankton were comparable or higher at increased temperature compared to control conditions (25°C).…”

Section: Discussionmentioning

confidence: 99%

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Nutrient starvation impairs the trophic plasticity of reef‐building corals under ocean warming

et al. 2019

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Global warming of the world's oceans is driving reef‐building corals towards their upper thermal limit, inducing bleaching, nutrient starvation and mortality. In addition, corals are predicted to experience large fluctuations in seawater nutrient concentrations, following water column stratification or eutrophication problems, which can further alter their nutritional capacities and ultimately their resilience to global change. We investigated the effect of thermal stress and dissolved inorganic nutrient (DINUT) availability on the auto‐ and heterotrophic nutritional capacities of corals. In particular, we assessed the effect of nitrogen enrichment or DINUT depletion (both in nitrogen and in phosphorus) on the assimilation of heterotrophic nutrients and on the heat‐stress tolerance of the reef‐building coral Stylophora pistillata. Here, we show that DINUT depletion enhanced coral bleaching under thermal stress and more importantly, significantly impaired rates of heterotrophic nutrient assimilation, inducing coral starvation. In contrast, corals grown under nitrogen enrichment maintained high rates of heterotrophic nutrient assimilation and avoided bleaching, although nutrient uptake rates were lowered. We therefore observed a positive coupling between auto‐ and heterotrophy within the coral–dinoflagellate symbiosis, indicating that heterotrophic processes require a minimum of autotrophically acquired nutrients to be functional. These findings show that the trophic plasticity of corals directly depends on the availability of dissolved inorganic nutrients in seawater. The lack of a shift towards greater heterotrophy under DINUT depletion may lead to substantial modifications of the role that feeding plays in the response of reef‐building corals to climate change. A plain language summary is available for this article.

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{NH}_{4}^{+}

uptake rates, consistent with previous studies reporting an impairment of inorganic nutrient uptake by stressed corals (Ezzat, Maguer et al, ; Godinot et al, ).…”

Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Nutrient starvation impairs the trophic plasticity of reef‐building corals under ocean warming

et al. 2019

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“…Warm-acclimation reduced nitrogen incorporation from external seawater nitrate on average by 79% in the symbionts, 81% in the gastrodermis, and 55% in the epidermis. Significant reductions in nitrate uptake at elevated temperatures have been observed in Stylophora pistillata (Godinot et al, 2011) and P. damicornis (Ezzat et al, 2016) but, in both cases the decreases were linked to a decline in photosynthesis. Here, the relative reduction in nitrate uptake in warm-acclimated corals observed at the end of the heat stress event is independent of the photosynthetic performance of the symbionts (i.e., O 2 -production), suggesting a general impact on nitrate supply to the symbiont and/or specific thermal impact on the enzymes involved in nitrate reduction.…”

Section: Discussionmentioning

confidence: 99%

Short-Term Thermal Acclimation Modifies the Metabolic Condition of the Coral Holobiont

et al. 2018

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The nutritional symbiosis between coral hosts and photosynthetic dinoflagellates is fundamental to the functioning of coral reefs. Rising seawater temperatures destabilize this relationship, resulting in drastic declines in world-wide coral cover. Thermal history is thought to play an important role in shaping a coral's response to subsequent thermal stress. Here, we exposed Pocillopora damicornis to two thermal acclimation regimes (ambient vs. warm) and compared the effect that acclimation had on the coral holobiont's response to a subsequent seven day heat stress event. We conducted daily physiological measurements at the holobiont level (gross photosynthesis, respiration, host protein content, symbiont density and chlorophyll content) throughout the heating event, as well as cellular-level imaging of 13 C-bicarbonate and 15 N-nitrate assimilation (using NanoSIMS) at the end of the heat stress event. Thermal acclimation history had a negligible effect on the measurements conducted at the holobiont level during the heat stress event. No differences were observed in the O 2 -budget between ambient and warm-acclimated corals and only small fluctuations in host protein, symbiont density and chlorophyll content were detected. In contrast, this lack of differential response, was not mirrored at the cellular level. Warm-acclimated corals had substantially higher 13 C enrichment in the host gastrodermis and lipid bodies, but significantly lower 15 N-nitrate assimilation in the symbionts and the host tissue layers, relative to the ambient-acclimated corals. We discuss potential reasons for the disconnect that occurred between symbiont bicarbonate and nitrate assimilation (in the absence of photosynthetic breakdown) in the warm-acclimated corals. We suggest this represents either a shift in nitrogen utilization, or supply limitation by the host. Our findings raise several interesting hypotheses regarding the role that nitrogen metabolism plays in thermal stress, which will warrant further investigation if we are to understand the acclimatization capacity of the coral holobiont.

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“…Indeed, biological nutrient inputs may foster resistance to bleaching by providing nitrogen and phosphorous in optimal ratios for maintaining the mutualism between coral hosts and their algal symbionts (Allgeier, Layman, Mumby, & Rosemond, 2014;Ezzat, Maguer, Grover, & Ferrier-Pagès, 2016;Meyer & Schultz, 1985;Wiedenmann et al, 2013). However, there have been no field studies to date testing whether natural nutrient subsidies influence the response of corals to major warming events.…”

Section: Introductionmentioning

confidence: 99%

Seabird nutrient subsidies alter patterns of algal abundance and fish biomass on coral reefs following a bleaching event

Benkwitt

Wilson

Graham

2019

Global Change Biology

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Cross‐ecosystem nutrient subsidies play a key role in the structure and dynamics of recipient communities, but human activities are disrupting these links. Because nutrient subsidies may also enhance community stability, the effects of losing these inputs may be exacerbated in the face of increasing climate‐related disturbances. Nutrients from seabirds nesting on oceanic islands enhance the productivity and functioning of adjacent coral reefs, but it is unknown whether these subsidies affect the response of coral reefs to mass bleaching events or whether the benefits of these nutrients persist following bleaching. To answer these questions, we surveyed benthic organisms and fishes around islands with seabirds and nearby islands without seabirds due to the presence of invasive rats. Surveys were conducted in the Chagos Archipelago, Indian Ocean, immediately before the 2015–2016 mass bleaching event and, in 2018, two years following the bleaching event. Regardless of the presence of seabirds, relative coral cover declined by 32%. However, there was a post‐bleaching shift in benthic community structure around islands with seabirds, which did not occur around islands with invasive rats, characterized by increases in two types of calcareous algae (crustose coralline algae [CCA] and Halimeda spp.). All feeding groups of fishes were positively affected by seabirds, but only herbivores and piscivores were unaffected by the bleaching event and sustained the greatest difference in biomass between islands with seabirds versus those with invasive rats. By contrast, corallivores and planktivores, both of which are coral‐dependent, experienced the greatest losses following bleaching. Even though seabird nutrients did not enhance community‐wide resistance to bleaching, they may still promote recovery of these reefs through their positive influence on CCA and herbivorous fishes. More broadly, the maintenance of nutrient subsidies, via strategies including eradication of invasive predators, may be important in shaping the response of ecological communities to global climate change.

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Limited phosphorus availability is the Achilles heel of tropical reef corals in a warming ocean

Cited by 87 publications

References 74 publications

Nutrient starvation impairs the trophic plasticity of reef‐building corals under ocean warming

Nutrient starvation impairs the trophic plasticity of reef‐building corals under ocean warming

Short-Term Thermal Acclimation Modifies the Metabolic Condition of the Coral Holobiont

Seabird nutrient subsidies alter patterns of algal abundance and fish biomass on coral reefs following a bleaching event

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