Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: A review on interactions and control by carbonate chemistry

Photosynthesis and Calcification at Cellular, Organismal and Community Levels in Coral Reefs: A Review on Interactions and Control by Carbonate Chemistry1

SYNOPSIS. Photosynthesis and calcification in zooxanthellate scleractinian corals and coral reefs are reviewed at several scales: cellular (pathways and transport mechanisms of inorganic carbon and calcium), organismal (interaction between photosynthesis and calcification, effect of light) and ecosystemic (community primary production and calcification, and air-sea CO2 exchanges).

The coral host plays a major role in supplying carbon for the photosynthesis by the algal symbionts through a system similar to the carbon-concentrating mechanism described in free living algal cells. The details of carbon supply to the calcification process are almost unknown, but metabolic CO^sub 2^ seems to be a significant source. Calcium supply for calcification is diffusional through oral layers, and active membrane transport only occurs between the calicoblastic cells and the site of calcification. Photosynthesis and calcification are tightly coupled in zooxanthellate scleractinian corals and coral reef communities. Calcification is, on average, three times higher in light than in darkness. The recent suggestion that calcification is dark-repressed rather than light-enhanced is not supported by the literature. There is a very strong correlation between photosynthesis and calcification at both the organism and community levels, but the ratios of calcification to gross photosynthesis (0.6 in corals and 0.2 in reef communities) differ from unity, and from each other as a function of level.

The potential effect of global climatic changes (pCO^sub 2^ and temperature) on the rate of calcification is also reviewed. In various calcifying photosynthetic organisms and communities, the rate of calcification decreases as a function of increasing pCO^sub 2^ and decreasing calcium carbonate saturation state. The calculated decrease in CaCO^sub 3^ production, estimated using the scenarios considered by the International Panel on Climate Change (IPCC), is 10% between 1880 and 1990, and 9-30% (mid estimate: 22%) from 1990 to 2100. Inadequate understanding of the mechanism of calcification and its interaction with photosynthesis severely limits the ability to provide an accurate prediction of future changes in the rate of calcification.

INTRODUCTION

Coral reefs are the most striking example of benthic, photosynthetic and calcifying ecosystems. They display the greatest abundance and diversity of CaCO^sub 3^-depositing organisms that carry out photosynthesis (calcareous algae) or harbor photosynthetic symbionts (scleractinian corals, foraminiferans and mollusks). The photosynthetic fixation of carbon dioxide (CO^sub 2^) and precipitation of CaCO^sub 3^ are intimately linked both at spatial (cell to ecosystem) and temporal (day-night) scales. Large fluxes of carbon and calcium carbonate occur at the cell and community levels on reefs. Transepithelial calcium transport in scleractinian corals can reach 1,700 nmol cm^sup -2^ h^sup -1^ (Wilbur and Simkiss, 1979), which would be equivalent to 149 mol Ca m^sup -2^ yr^sup -1^, while the rates of community gross primary production and respiration of coral reef flats range, respectively, from 79 to 584 and from 76 to 538 mol C m^sup 2^ yr^sup -1^, the rate of net calcification ranges from 5 to 126 mol C m^sup -2^ yr^sup -1^ (Gattuso et al., 1998b).

The modern study of coral calcification began more than 40 years ago with the pioneering works of Goreau and collaborators (Goreau and Bowen, 1955; Goreau, 1959; Goreau and Goreau, 1959; Goreau, 1963) but many aspects, such as the transport mechanisms of calcium and inorganic carbon from the surrounding seawater to the sites of photosynthesis and skeletogenesis, and their environmental controls, remain poorly known. Likewise, the concentrations and transport of secondary products (OH and H+), as well as the interaction between photosynthesis and calcification, are poorly understood; the latter is a matter of recent controversy (Carlon, 1996; Goreau et al., 1996; Marshall, 1996a, b).

Photosynthetic CO^sub 2^ fixation and CO^sub 2^ release by calcification are relatively minor components of the present global carbon cycle (Ware et al., 1992; Smith, 1995) but may have contributed to the control of atmospheric pCO^sub 2^ during glacial-interglacial cycles (Opdyke and Walker, 1992). Global climatic changes, such as the predicted increases in temperature and pCO^sub 2^ (Houghton et al., 1996), and changes in related parameters, such as pH and aragonite saturation state, are likely to have significant effects on the cycling of carbon and carbonate in coral reefs. These effects are discussed using the limited information available about scleractinian corals and coral communities, as well as some data for temperate coralline algae.

The aim of our paper is to review the cycles of carbon and carbonate in zooxanthellate scleractinian corals and coral reefs. We first provide background information on processes (photosynthesis, respiration and calcification) and carbonate chemistry. We then consider several scales: molecular and cellular (pathways and transport mechanisms of inorganic carbon and calcium), organismal (interaction between photosynthesis and calcification, effect of light), and ecosystemic (community production and calcification, and air-sea CO^sub 2^ fluxes). We also review the effect of changes in the seawater carbonate chemistry and provide a tentative prediction of the effect of increased pCO^sub 2^ and temperature on the rate of calcification.