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. Stimson, S.T. Larned J. Exp. Mar. Biol. Ecol. 252 2000 159 –180
1. Introduction
It is often implicit in studies of benthic primary productivity that the primary source of dissolved nutrients is the overlying water column Hanisak, 1983. Nutrient
availability to benthic autotrophs in coral reef ecosystems is usually assessed on the basis of water column nutrient concentrations e.g. Littler et al., 1991, 1992; Lapointe et
al., 1992; Delgado and Lapointe, 1994. Water column nutrient concentrations in these coral reef ecosystems can be low, with average dissolved inorganic nitrogen DIN
concentrations less than 1.5 mM and phosphate concentrations less than 0.5 mM D’Elia and Wiebe, 1990; Furnas et al., 1990; Larned, 1998. Despite low water column nutrient
concentrations, macroalgae often achieve high rates of net productivity on oligotrophic
22 2l
coral reefs . 1000 g dry wt m
year , and high standing stocks . 1000 g dry wt
22
m Hatcher, 1988; Stimson et al., 1996. To maintain these standing stocks, coral reef
macroalgae must acquire nutrients at rates high enough to offset losses to herbivory, reproduction and detritus production. If standing stocks are increasing, i.e. biomass is
accumulating, nutrient requirements will be even higher. These observations raise the question of how benthic macroalgae sustain net productivity in oligotrophic waters.
One hypothesis proposed to explain high net productivity in coral reef macroalgae is that most of the nutrient requirements for long-term growth are met during short-lived
pulses that have little effect on average nutrient concentrations in the water column McGlathery et al., 1992; Stimson et al., 1996; Schaffelke and Klumpp, 1998. Episodes
of high discharge from coastal streams and groundwater have been suggested as major sources of nutrient pulses Lapointe and Matzie, 1996; Laws and Allen, 1996. Under
laboratory conditions, many coral reef macroalgae have been shown to acquire nutrients during pulses, and rates of photosynthesis or growth often increase following pulses e.g.
Lapointe, 1989; Lapointe et al., 1987; Littler et al., 1988, 1991; McGlathery et al., 1992; Delgado and Lapointe, 1994, Stimson et al., 1996. However, it is difficult to evaluate
the ecological importance of nutrient pulses to productivity in the field because little data is available concerning pulse frequency, magnitude and duration. Concentrations of
dissolved inorganic nutrients in stream water and groundwater are usually reduced by dilution and uptake shortly after moving offshore Lapointe and Clark, 1992; Laws and
Allen, 1996; Szmant and Forrester, 1996. With increasing distance from shore, the percentage of total nitrogen or phosphorus that is available as DIN and phosphate
decreases, and the percentage available in dissolved organic or particulate form increases Lapointe and Clark, 1992; Szmant and Forrester, 1996. Thus much of the nutrient load
reaching coral reefs from shore via the water column is in particulate form and must be converted to dissolved inorganic form before it is available to macroalgae.
As an alternative to the water column, benthic sources may provide inorganic nutrients at rates sufficient to sustain macroalgal productivity. Potential benthic nutrient
sources include excretion by macrofauna Meyer and Schultz, 1985; Williams and Carpenter, 1988 and meiofauna Gray, 1985, ground water discharge Johannes, 1980;
Lewis, 1987, Lapointe, 1997, N fixation Capone et al., 1992 and remineralization of
2
organic matter in sediments. Remineralization resulting in the net release efflux of dissolved inorganic nutrients from coral reef sediments has been documented at several
sites Williams et al., 1985; Hansen et al., 1987; Johnstone et al., 1989; Capone et al.,
J . Stimson, S.T. Larned J. Exp. Mar. Biol. Ecol. 252 2000 159 –180
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1992; Boucher et al., 1994; Haberstroh, 1994. When nutrients are released from the sediments at rates higher than the rate of mixing into the water column, a nutrient-
enriched zone develops and benthic algae may acquire nutrients from this zone Lapointe and O’Connell, 1989; Lavery and McComb, 1991; Stimson et al., 1996. The
nutrient-enriched zone corresponds to the boundary layer that forms when water flowing over coral reef surfaces loses velocity and turbulence to friction Shashar et al., 1996.
Diffusion, rather than turbulent mixing, dominates the transport of dissolved substances within and through the boundary layer. For this reason, nutrients may accumulate near
the sediment and are slow to mix into the overlying water column.
The distinction between water column and benthic nutrient sources described above may be exemplified by the nitrogen dynamics of Kaneohe Bay, a partially enclosed
lagoon on the windward side of the Island of Oahu, Hawaii. Fringing coral reefs border most of the shore of the Bay, and 60 patch reefs rise from the lagoon floor 15 m depth.
From 1951 to 1977, effluent from sewage treatment plants was discharged directly into the southern basin of Kaneohe Bay. During this period, parts of the Bay were
characterized by high phytoplankton biomass and a profusion of the benthic macroalga Dictyosphaeria cavernosa Chlorophyta on reef slopes Banner, 1974; Smith et al.,
1981; Maragos et al., 1985. The sediments of the Bay accumulated nutrients rapidly during this period, primarily by the sedimentation of particulate organic matter Smith et
al., 1981. In 1977 and 1978, the sewage effluent was diverted from the two largest sewage outfalls to a deep ocean outfall outside of the Bay. Water column DIN and
phosphate concentrations, phytoplankton biomass, and D
. cavernosa cover declined rapidly following sewage diversion Smith et al., 1981. Results from studies carried out
in 1985, 1989–1990, and 1994–1997 indicated that DIN and phosphate concentrations and phytoplankton biomass continued to decline Taguchi and Laws, 1989; Laws and
Allen, 1996; Larned and Stimson, 1996. The continued reduction of water column nutrient concentrations has been associated with a shift in phytoplankton composition
from an assemblage dominated by large diatoms to one dominated by picoplankton with lower half-saturation constants for nutrient uptake Laws and Allen, 1996; Larned,
1998.
In contrast to the changes observed in the water column, the abundance of Dictyosphaeria cavernosa in Kaneohe Bay has not continued to decline. Results of
surveys conducted in 1983 and 1990 suggested that D . cavernosa cover was increasing
in that 7-year period on a Bay-wide basis Hunter and Evans, 1995. Additional surveys conducted in 1990 and 1996 indicate that two non-native macroalgae, introduced to a
small number of sites in the Bay between 1974 and 1978, have spread to patch and fringing reefs throughout the Bay Russell, 1992; Rodgers and Cox, 1999. These
macroalgae, Gracilaria salicornia and Kappaphycus striatum Rhodophyta are pros- trate, mat-forming species, as is D
. cavernosa. Thus, while phytoplankton populations appear to be declining in response to the increasingly oligotrophic water column Laws
and Allen, 1996, mat-forming benthic algae continue to grow profusely and maintain high standing stocks. Results of nutrient enrichment experiments indicate that growth
rates in phytoplankton and in the macroalgae listed above are DIN-limited Laws and Allen, 1996; Larned and Stimson, 1996; Larned, 1998.
The questions posed in this study are whether efflux rates of DIN from Kaneohe Bay
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. Stimson, S.T. Larned J. Exp. Mar. Biol. Ecol. 252 2000 159 –180
sediments are high enough to sustain the growth of macroalgae, and whether these rates are higher than on other tropical reefs that do not support high standing crops of
macroalgae. A number of observations from previous studies suggest that growth and persistence of macroalgae on Kaneohe Bay reefs is due in part to the efflux of sediment
nutrients. Dictyosphaeria cavernosa, Gracilaria salicornia and Kappaphycus striatum maintained in flow-through culture could not sustain net growth in unenriched seawater,
but did grow when provided with DIN-enriched seawater Larned and Stimson, 1996; Larned, 1998. Results from a field experiment indicated that D
. cavernosa can sustain net growth when exposed to sediment-derived nitrogen, but cannot grow when isolated
from the sediment Larned and Stimson, 1996. DIN concentrations measured within and below thalli of the three algal species were significantly higher than DIN
concentrations adjacent to the thalli Larned and Stimson, 1996; Larned, 1998. While these observations imply that the success of macroalgae is related to sediment-derived
nutrients, it is not known if efflux rates in Kaneohe Bay are elevated relative to those in other coral reef systems, and if so, whether the elevation is due primarily to sewage
release, which ended 20 years ago, or to the current influx of nutrients to the sediments. Smith et al. 1981 predicted that efflux from the organic matter-rich sediments would
continue to add nutrients to the water column for several years following sewage diversion, then the sediment nutrient reservoir would be depleted. This prediction does
not seem compatible with our observation that DIN efflux is presently high enough to support a substantial macroalgal standing stock on reef slopes. In the present study, we
report rates of DIN and phosphate flux across the surface of reef and lagoon sediments in southern Kaneohe Bay. We also report rates of sedimentation of particulate nitrogen to
the lagoon floor for comparison with rates measured shortly before sewage diversion Taguchi, 1982. Finally, we compare efflux and sedimentation rates in Kaneohe Bay
with rates reported at other coral reef sites that have not been subject to high levels of anthropogenic nutrient enrichment.
2. Methods
