Nutrient enrichment can increase the susceptibility of reef corals to bleaching

Wiedenmann, Jörg; D’Angelo, Cecilia; Smith, Edward G.; Hunt, Alan N.; Legiret, François-Eric; Postle, Anthony D.; Achterberg, Eric P.

doi:10.1038/nclimate1661

Cited by 507 publications

(609 citation statements)

References 26 publications

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“…Phosphorus (P) may also be limiting to coral metabolism [47], particularly in the case of an imbalanced nutrient supply with excess inorganic N (e.g. of anthropogenic origin) [48]. At our study site, the reef-surrounding seawater exhibits particulate organic C to N (POC : PN) and dissolved inorganic N to phosphate (DIN : PO 4 32 ) ratios that are respectively higher and lower than the Redfield ratio (106 : 16 : 1) during all seasons (electronic supplementary material, table S1), suggesting that N rather than P is the limiting nutrient in the Gulf of Aqaba.…”

Section: Discussionmentioning

confidence: 99%

Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions

et al. 2015

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Functional traits define species by their ecological role in the ecosystem. Animals themselves are host–microbe ecosystems (holobionts), and the application of ecophysiological approaches can help to understand their functioning. In hard coral holobionts, communities of dinitrogen (N 2 )-fixing prokaryotes (diazotrophs) may contribute a functional trait by providing bioavailable nitrogen (N) that could sustain coral productivity under oligotrophic conditions. This study quantified N 2 fixation by diazotrophs associated with four genera of hermatypic corals on a northern Red Sea fringing reef exposed to high seasonality. We found N 2 fixation activity to be 5- to 10-fold higher in summer, when inorganic nutrient concentrations were lowest and water temperature and light availability highest. Concurrently, coral gross primary productivity remained stable despite lower Symbiodinium densities and tissue chlorophyll a contents. In contrast, chlorophyll a content per Symbiodinium cell increased from spring to summer, suggesting that algal cells overcame limitation of N, an essential element for chlorophyll synthesis. In fact, N 2 fixation was positively correlated with coral productivity in summer, when its contribution was estimated to meet 11% of the Symbiodinium N requirements. These results provide evidence of an important functional role of diazotrophs in sustaining coral productivity when alternative external N sources are scarce.

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Section: Discussionmentioning

confidence: 99%

Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions

et al. 2015

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“…Furthermore, the threshold for heat-induced bleaching can be lowered by unfavourable concentrations of inorganic nutrients in the water column . Particularly, elevated levels of dissolved inorganic nitrogen can increase bleaching susceptibility (Wagner et al, 2010;Wiedenmann et al, 2012;Wooldridge, 2009) and this may be exacerbated by higher densities of symbionts in nutrient-enriched corals (Cunning and Baker, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…While other fields of (molecular) biology rely heavily on the thorough analysis of a few model organisms, at the moment there are not many coral models for laboratory studies (Weis et al, 2008). However, recent progress in coral culture enables the propagation of these organisms in excellent physiological conditions over many years or even decades Leewis and Janse, 2008) and experiments with laboratory strains have already yielded important insights into physiological processes in reef corals (Allemand et al, 2004;D'Angelo et al, , 2008Wiedenmann et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: Prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance

Hume

D’Angelo

Burt

et al. 2013

Marine Pollution Bulletin

162

148

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a b s t r a c tCorals in the Arabian/Persian Gulf endure summer temperatures of up to 36°C, making them ideal subjects to study the mechanisms underlying thermal tolerance. Unexpectedly, we found the ''generalist'' Symbiodinium clade C3 to be the prevalent symbiont among seven coral species from Abu Dhabi (UAE) waters. Moreover, C3 represented the only dominant symbiont type in Porites spp. from this region. The ''thermotolerant'' symbionts D1a and C15 were not encountered, indicating that the association with these symbionts cannot be the sole reason for the heat tolerance of Gulf corals. The association of Porites lobata with specific symbiont types (C3 vs. C15) in samples from habitats with very different temperature regimes (Abu Dhabi vs. Fiji) remained unaffected by laboratory culture. During temperature stress experiments specimens from both locations strongly downregulated green fluorescent protein (GFP)-like pigments. However, the Abu Dhabi samples were less prone to bleaching and showed lower mortality.Crown

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“…The proposed mechanism for this link is that high concentrations of DIN lead to high zooxanthellae MI, resulting in an increased demand for all (other) essential plant nutrients by the proliferating endosymbiont population, resulting in a relative under-supply of phosphate. The latter is suggested to lead to altered thylakoid membrane structures with enhanced susceptibility to thermal and light damage (Wiedenmann et al, 2012). Future testing within natural reef settings is required to compare the relative merits of this alternative view with the cellular mechanism proposed here.…”

Section: Bleaching Thresholds Linked To Zooxanthellae MImentioning

confidence: 99%

“…Red Sea -no summer river runoff (Genin et al, 1995), western Pacific warm pool -restricted upwelling due to strong thermal stratification (Tomczak and Godfrey, 1994), northern Australialow nutrient loads in summer river runoff (Wooldridge et al, 2006). Recently, an alternative hypothesis has been suggested for why corals exposed to high levels of dissolved inorganic nitrogen (DIN) experience greater bleaching susceptibility compared with corals in low nutrient environments (see Wiedenmann et al, 2012). The proposed mechanism for this link is that high concentrations of DIN lead to high zooxanthellae MI, resulting in an increased demand for all (other) essential plant nutrients by the proliferating endosymbiont population, resulting in a relative under-supply of phosphate.…”

Section: Bleaching Thresholds Linked To Zooxanthellae MImentioning

confidence: 99%

Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae

Wooldridge

2013

Biogeosciences

130

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Impairment of the photosynthetic machinery of the algal endosymbiont ("zooxanthellae") is the proximal driver of the thermal breakdown of the coral-algae symbiosis ("coral bleaching"). Yet, the initial site of damage, and early dynamics of the impairment are still not well resolved. In this perspective essay, I consider further a recent hypothesis which proposes an energetic disruption to the carbon-concentrating mechanisms (CCMs) of the coral host, and the resultant onset of CO₂-limitation within the photosynthetic "dark reactions" as a unifying cellular mechanism. The hypothesis identifies the enhanced retention of photosynthetic carbon for zooxanthellae (re)growth following an initial irradiance-driven expulsion event as a strong contributing cause of the energetic disruption. If true, then it implies that the onset of the bleaching syndrome and setting of upper thermal bleaching limits are emergent attributes of the coral symbiosis that are ultimately underpinned by the characteristic growth profile of the intracellular zooxanthellae; which is known to depend not just on temperature, but also external (seawater) nutrient availability and zooxanthellae genotype. Here, I review this proposed bleaching linkage at a variety of observational scales, and find it to be parsimonious with the available evidence. Future experiments are suggested that can more formally test the linkage. If correct, the new cellular model delivers a valuable new perspective to consider the future prospects of the coral symbiosis in an era of rapid environmental change, including: (i) the underpinning mechanics (and biological significance) of observed changes in resident zooxanthellae genotypes, and (ii) the now crucial importance of reef water quality in co-determining thermal bleaching resistance

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Nutrient enrichment can increase the susceptibility of reef corals to bleaching

Cited by 507 publications

References 26 publications

Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions

Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions

Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: Prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance

Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae

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