Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida

During the past two decades coral reefs in the greater Caribbean area have been altered by phase shifts away from corals and toward macroalgae or algal turfs. This study tested the hypothesis that because the phase shift on reefs in Jamaica and southeast Florida involved frondose macroalgae, bottom-up control via nutrient enrichment must be a causal factor. The approach was multifaceted and included measurement of near-bottom nutrient concentrations, salinity, nutrient enrichment bioassays, alkaline phosphatase assays, tissue C : N : P ratios, and tissue 15N : 14N (6”N) ratios. In both locations, concentrations of dissolved inorganic nitrogen (DIN) and soluble reactive phosphorus (SRP) exceeded nutrient thresholds (1 .O PM DIN, 0.1 PM SRP) noted to sustain macroalgal blooms on Caribbean coral reefs. High seawater DIN : SRP ratios, alkaline phosphatase activity, and tissue C : P and N : P ratios of macroalgae on the carbonate-rich Jamaican reef suggested SRP limitation of productivity compared to lower values of these variables on siliciclastic reefs in Florida that suggested DIN limitation. This pattern was corroborated experimentally when SRP enrichment increased P,,,, (photosynthetic capacity at light saturation) of the chlorophyte Chaetomorpha Zinum in Jamaica compared to DIN enrichment that increased (x (the photosynthetic efficiency under low irradiance) of the deeper growing chlorophyte Codium isthmocladum in southeast Florida. Increased DIN concentrations were associated with reduced salinity on both reefs, indicating submarine groundwatcr discharge was a significant source of DIN. Elevated S15N values of C. isthmocladum tissue further pointed to wastewater DIN as a source of nitrogen contributing to the blooms in southeast Florida. A basic objective in marine ecology is to understand the mechanisms by which various natural and anthropogenic factors maintain and alter structure in biotic communities. Coral reefs are the most diverse and complex of all marine ecosystems yet flourish in shallow tropical waters with very low and often undetectable concentrations of dissolved inorganic nitrogen (DIN) and soluble reactive phosphorus (SRP, see Lewis 1977). Coral reefs are noted for their fragile ecological balance, high rates of gross productivity, and unique ability to accrete massive limestone formations over geological time (Goreau et al. 1979). Ecologists studying the controls of aquatic food webs have used the concepts “bottom up” and “top down” to describe how resource availability or the actions of consumers regulate the structure of food webs (Carpenter et al. 1985). A complex interaction of bottom-up and top-down controls are similarly important on coral reefs (Littler and Littler 1984), where standing crops of benthic macroalgae are usually inconspicuous on undisturbed coral reefs due to the combined effects of low nutrient Acknowledgments I thank Jeremy Woodley and Thomas J. Goreau for inspiring the research at the Discovery Bay. William Matzie, Julie Bishop, Cy Macfarlane, Steve Krupa, Bill Parks, Sylvia Cook, Connie Gasque, Carmen Vare, and Jim Vaughn are gratefully acknowledged for their technical support of this work. Bill Burnett analyzed seawater samples for radon-radium analysis and Suzanne Macintosh drafted the location figures. The comments of Mark Littler, Tom Gorcau, and two anonymous reviewers improved the manuscript. This research was supported by National Science Foundation grants OCE 85-15492 and OCE 88-l 2055 and the Florida Sea Grant College Program with support from NOAA, Office of Sea Grant (R/C-E-34). This is Contribution 1159 from the Harbor Branch Oceanographic Inslitution. availability and grazing by herbivorous fish and invertebrates (i.e. relative-dominance model, Fig. I ). The very low or undetectable concentrations of dissolved inorganic nutrients in the water column of undisturbed coral reefs results in nutrient-limited productivity of epilithic algae and sets the upper limit to algal standing crops. The term “nutrient-limited productivity” is defined here as a condition where an increase in the concentration (or flux) of a nutrient increases a metabolic response, such as net photosynthesis or other physiological processes related to growth (Droop 1983). The epilithic algal community on coral reefs includes small microfilamentous forms referred to as “turfs,” larger frondose macroalgae including both fleshy and calcareous forms, and coralline algae that form crusts on exposed reef substrata (Littler and Littler 1984). The productivity or standing crop of algal turfs (Hatcher and Larkum 1983; Williams and Carpenter 1988), frondose macroalgae (Lapointe 1987; Lapointe et al. 1987), and coralline algae (Littler 1973) increase with increased nutrient availability on coral reefs, confirming their nutrient-limited status. This nutrientlimited status is most pronounced in the larger, rapidly growing macroalgae, and it greatly restricts their ability to favorably compete with corals and turf algae in low nutrient environments (Atkinson 1988; Littler and Littler 1984; Fig. 1). Accordingly, increases in water-column nutrient concentrations associated with exponentially expanding human populations and coastal eutrophication can lead to increased productivity and biomass of frondose macroalgae. The first well-documented example of a coral reef shifting to a macroalgal-dominated reef occurred almost 25 yr ago in Kaneohe Bay, Hawaii, where nutrient enrichment from domestic sewage led to overgrowth of corals by the green bubble alga Dictyosphaeria cavernosa (Banner 1974). Since then, case studies from Reunion Island (Cuet et al. 1988; Naim