Journal of Experimental Marine Biology and Ecology
Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata
Introduction
Corals reefs are one of the most productive coastal marine ecosystems (Sorokin, 1993) despite low concentrations of nutrients in the surrounding waters (Furnas, 1992). The establishment and maintenance of scleractinian corals in such nutrient-poor conditions are partly due to their symbiosis with unicellular dinoflagellates commonly called zooxanthellae (zoox), which translocate a large fraction of photosynthetically fixed carbon to the host for its nutritional needs (Muscatine and Porter, 1977). Questions regarding nutrient limitation in such a system have therefore taken center stage Rees, 1991, Cook et al., 1992, Falkowski et al., 1993, Davy and Cook, 2001. Many investigators have shown that zooxanthellae can be carbon-limited with respect to dissolved inorganic carbon (DIC), especially when rates of photosynthesis greatly exceed the respiratory rate of the coral colony Muscatine et al., 1989b, Weis, 1990, Lesser et al., 1994. At the organismal level, the effects of DIC limitation could limit translocation and affect coral energy budgets (Lesser et al., 1994). Photosynthates are also considered junk food—deficient in nitrogen, phosphorus, and amino acids (Battey and Patton, 1987), which are essential nutrients for growth Falkowski et al., 1984, Rinkevitch, 1989, Davies, 1991. It has therefore been suggested that corals are nitrogen-limited Cook and D'Elia, 1987, Muller-Parker et al., 1988. External food supplies are considered to be a major nutritive source of nitrogen, phosphorus Farrant et al., 1987, Sorokin, 1991, Lewis, 1992, Ayukai, 1995, Sebens et al., 1996, and also carbon (Reynaud et al., 2002) for corals. Feeding can increase the respiration rates of the animal (Ferrier-Pagès et al., in press), thereby making CO2 more available for photosynthesis and growth.
With some exceptions Porter, 1976, Witting, 1999, most corals can be voracious predators Sebens, 1977, Sebens et al., 1996 and are able to use a variety of food sources such as sediment (Rosenfeld et al., 1999), dissolved and particulate organic matter Lasker, 1981, Anthony, 1999, bacteria Sorokin, 1973, Sorokin, 1991, Farrant et al., 1987, and zooplankton Sorokin, 1991, Lewis, 1992, Sebens, 1977, Sebens et al., 1996, Ferrier-Pagès et al., 1998. The relative dependence of corals on heterotrophic nutrition is still partially understood. In particular, few studies have measured the ingestion rates of natural zooplankton by corals Lewis, 1992, Sebens et al., 1996. The effect of feeding on coral physiology (on both photosynthesis, and tissue and skeletal growth) also deserves further investigation. Some studies have shown that feeding tends to increase the algal density as well as the rates of areal photosynthesis Muscatine et al., 1989a, Titlyanov et al., 2000a, Titlyanov et al., 2000b, Titlyanov et al., 2001. However, the amount of photosynthates translocated by the algae seems to remain unchanged between starved and fed animals (Davy and Cook, 2001). Studies of the effect of feeding on coral growth have also given controversial results Johannes, 1974, Wellington, 1982, Anthony and Fabricius, 2000, Ferrier-Pagès et al., 2003. For example, Johannes (1974) and Wellington (1982) determined that heterotrophy has minimal effect on the skeletal growth of scleractinian corals, while Anthony and Fabricius (2000) and Ferrier-Pagès et al. (in press) show that heterotrophy increases both tissue and skeletal growth. The importance of feeding as a supplemental source of nutrients depends on several environmental parameters, such as light availability (Falkowski et al., 1984) or seawater turbidity (Anthony and Fabricius, 2000). In the zooxanthellae coral Stylophora pistillata (Veron, 1995), for example, the total energy requirement in well-lit, shallow waters may be met by photosynthetic production, whereas under shaded conditions, corals may obtain up to 60% of their energy through feeding (Falkowski et al., 1984).
The aim of this work was to investigate the simultaneous effect of light and feeding on the rates of tissue growth, photosynthesis, and calcification of S. pistillata. Physiological changes were examined after 2, 5, and 9 weeks in order to investigate the effect of time on the response of corals to feeding. This study addresses several questions: (1) Does feeding influence the tissue composition and growth, and is this influence light-dependent? (2) If feeding does change tissue composition, does it also affect the coral photosynthetic capacities? (3) Finally, if feeding has a direct effect on photosynthesis, does this process enhance calcification rates, particularly in terms of dark versus light calcification? It has indeed been shown that coral growth (calcification rate) is dependent on photosynthesis, with a ratio of light:dark calcification equal to approximately 4. This has led to the ‘light-enhanced calcification’ theory Goreau and Goreau, 1959, Barnes and Chalker, 1990, Marshall, 1996, Furla et al., 2000.
Section snippets
Biological material
Different colonies of S. pistillata were collected in the Gulf of Aqaba (Jordan) from depths of 5 m and maintained for at least 3 months in the laboratory under the same controlled conditions as described below (T: 26 °C, light: 250 μmol photons m−2 s−1 with a photoperiod 12:12 h light:dark). Experiments were then carried out with microcolonies consisting of 1-cm-long branch tips. Microcolonies are necessary when calcification is measured using 45Ca because this procedure relies on small
Results
Chlorophylls a and c2 were measured only after 9 weeks of incubation. Results showed that chlorophyll concentrations per unit surface area differed according to treatment (Fig. 1a and c). For each light level, chl-a concentrations were four to seven times greater in fed corals than in control corals (F1=174, p<0.001). FC also contained five to seven times more chlorophyll c2 per square centimeter of skeleton than CC (F1=156, p<0.05). Light intensity significantly changed the amounts of
Discussion
For most corals, total energy requirement in well-lit shallow waters may be met by photosynthetic production (Muscatine and Porter, 1977), whereas under shaded conditions, corals may obtain up to 60% of their energy through feeding (Falkowski et al., 1984). In shallow waters, the δ15N abundance of coral tissue (4–6‰) suggests that zooplankton is not the main source of nitrogen, which mostly originates from recycled dissolved inorganic nitrogen Sammarco et al., 1999, Yamamuro et al., 1995.
Acknowledgements
Thanks are due to two anonymous reviewers, as well as to Dr. P. Furla and Prof. D. Allemand, for their helpful comments. Special thanks to Dr. M. Hayes for pertinent remarks and linguistic improvements. [SS]
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