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

Abstract

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 (N2)-fixing prokaryotes (diazotrophs) may contribute a functional trait by providing bioavailable nitrogen (N) that could sustain coral productivity under oligotrophic conditions. This study quantified N2 fixation by diazotrophs associated with four genera of hermatypic corals on a northern Red Sea fringing reef exposed to high seasonality. We found N2 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, N2 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.

Keywords: Symbiodinium; diazotrophs; hermatypic corals; nitrogen fixation; organic matter release; photosynthesis.

Figure 1.

Seasonal environmental conditions with corresponding primary productivity and dinitrogen fixation in corals. (a) Seasonal weekly averages of the main environmental parameters at the sampling location. (b) Gross productivity and (c) N₂ fixation of Acropora (ACR), Pocillopora (POC), Stylophora (STY) and Goniastrea (GON) are presented here as means (n = 8) ± s.e.m. See electronic supplementary material, table S1–S6 for the complete set of environmental variables and for statistical results. Colours represent winter (WIN, blue), spring (SPR, green), summer (SUM, red) and autumn (AUT, orange). (Online version in colour.)

Figure 2.

Seasonal Symbiodinium and photopigment content in corals. (a) Symbiodinium density, (b) areal chl a content and (c) chl a per Symbiodinium cell. Colours represent spring (SPR, green) and summer (SUM, red). See electronic supplementary material, table S3–S6 for the statistical results. Data are presented as means (n = 4) ± s.e.m. See figure 1 legend for definitions of abbreviations on x-axis. (Online version in colour.)

Figure 3.

Seasonal relationships between N₂ fixation and gross primary productivity in corals. Data points for each season (n = 32) are colour coded in blue (winter, WIN), green (spring, SPR), red (summer, SUM) and orange (autumn, AUT). Best-fit linear regression lines (±95% CIs) are solid black if the relationship is significant. (Online version in colour.)

Figure 4.

C and N flux model of the diazotroph–dinoflagellate–coral symbiosis. Shown are models for (a) spring (SPR) and (b) summer (SUM). Arrows represent C (black) and N (blue) fluxes (‡ µmol cm⁻² d⁻¹), and the width of arrows highlights seasonal differences. Percentages are: contribution of Symbiodinium-acquired N to Symbiodinium N demands (CZND); contribution of Symbiodinium-acquired C to animal respiration (CZAR); contribution of heterotrophically acquired C to animal respiration (CHAR); loss by organic C release of the total acquired C (LOC); loss by organic N release of the total acquired N (LON). Parameters presented in the model (±s.d.) and the respective calculations are reported online (electronic supplementary material). (Online version in colour.)