252 (2000) 159–180
www.elsevier.nl / locate / jembe
Nitrogen efflux from the sediments of a subtropical bay and
the potential contribution to macroalgal nutrient requirements
a ,* b
J. Stimson , S.T. Larned
a
Department of Zoology, University of Hawaii, Honolulu, HI 96822, USA
b
Coastal Ecology Branch, US Environmental Protection Agency, 2111 SE Marine Science Dr., Newport,
OR97365, USA
Received 15 October 1999; accepted 26 May 2000
Abstract
The concentration of dissolved inorganic nitrogen (DIN) in the porewaters of shallow-water tropical marine sediments can be as high as 50–100mM, at sediment depths of shallow as 20 cm. These concentrations are at least two-orders of magnitude greater than the DIN concentration in the overlying water. High porewater concentrations, and the resulting concentration gradient, result in substantial efflux of DIN from the sediments to the water column. This sediment-derived DIN may be an important nutrient source for benthic algae. In Kaneohe Bay, Hawaii, a mean
22 21
ammonium efflux rate of 490 mmol m day and a mean nitrate1nitrite efflux rate of 123
22 21
mmol m day were measured on reef slopes in the habitat occupied by benthic algae. It has been demonstrated that this nutrient source is essential for the growth of at least one abundant alga, Dictyosphaeria cavernosa, and possibly others. The DIN concentrations in Kaneohe Bay sediment porewaters, and the rates of DIN efflux from those sediments, are greater than porewater concentrations and efflux rates reported for other, more pristine tropical sites. The rate of sedimentation of particulate nitrogen is similar to rates reported from other tropical lagoons, and about twice as high as the efflux rate of total dissolved nitrogen. Given the present low nutrient concentrations in the water column of the Bay, these results support the view that nutrient efflux from the benthos is in part responsible for the persistence of D. cavernosa on these reefs. It is possible that efflux of DIN from sediments may be responsible for sustained benthic algal productivity in similar habitats on other tropical reefs. 2000 Elsevier Science B.V. All rights reserved.
Keywords: Nitrogen; Efflux; Sediment; Coral reef; Porewater; Macroalgae
*Corresponding author. Tel.: 11-808-956-6174; fax: 11-808-956-9812.
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 1.5mM and phosphate concentrations less than 0.5mM (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.
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).
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
2.1. Study sites
Fig. 1. Map of Kaneohe Bay and Moku o Loe, Hawaii. Unstippled areas represent fringing reef, patch reefs and the barrier reef. Sites 1 and 2 are sites of water-column nutrient samples, efflux rate measurements and sedimentation rate measurements.
from the nearest shoreline and at the same 2 m depth as the near-reef water column samples (Site 2, Fig. 1).
2.2. Water column and porewater sampling
Water-column samples and water samples from just above the sediment surface (1–15 cm) were collected with acid-washed 60-ml syringes fitted with Pasteur pipettes. All water samples were filtered (Whatman GF / C) into acid-washed polyethylene bottles and frozen within 10 min of collection. Analyses of nitrate1nitrite, ammonium, phosphate and total dissolved nitrogen concentrations in water samples were performed on a Technicon Autoanalyzer II by Analytical Services, University of Hawaii.
rod (Fig. 2). The intakes were constructed by wrapping 8315 cm sheets of plankton netting and window screen around a 4-mm diameter plexiglass tube. Numerous small holes had been drilled into the plexiglass tube prior to wrapping it with the screen. Both ends of the filter and the filter end of the plexiglass tube were sealed with polyolefin
adhesive (‘hot glue’). The plastic tube of the filter was attached to a length of flexible plastic tubing (3 mm internal diameter) long enough to extend above the sediment surface. The flexible tubing was then passed through a length of glass tubing, which was the same diameter as the filter. When the whole assembly was inserted into the hole in the sediment, the glass tube formed a well casing and sealed the upper walls of the well. The tygon tubing extended 15–20 cm above the sediment and was capped until water samples were to be drawn. The filter and tygon tubing were acid-washed prior to insertion into the sediment. To minimize the effects of disturbance created during installation, the samples were taken 2 or more days after installation. To draw a sample, the cap on the tygon tubing was removed, an acid-washed syringe was attached to the plastic tubing, a 5-ml volume was withdrawn and discarded, then a 30-ml sample was withdrawn. The sample was discharged through a GF / C filter into an acid-washed polyethylene bottle and frozen within 10 min.
Vacuum filtration of sediment samples collected near the porewater samplers with a piston corer (2.5 cm diameter, 60 cc volume) yielded 22–24 ml of water per 100 ml of undrained sediment, giving a minimum estimate of porosity of 23%. Particle size distributions of these sediments were obtained using graded sieves; the modal size of particles was retained on the 0.125-mm sieve (26% of weight), 8% was retained on the 0.625-mm screen and 2.5% was less than 0.625 mm. Given the small volume of the water samples and the porosity of these sediments, it is unlikely that the shallowest wells (5–10 cm depth) contained water from above the sediment surface. Measurements of salinity have been conducted on porewaters drawn from wells on a nearby reef. These showed high salinities at depths of 1 and 2 m in four wells over a 300-h period, suggesting little groundwater input to the system (Tribble et al., 1992).
2.3. Efflux rates
Efflux rates of DIN, phosphate and dissolved organic nitrogen (DON) from the sediments of the windward reef flat of Moku o Loe, the windward reef slope of Moku o Loe and the Bay bottom were estimated by measuring the change in nitrate1nitrite, ammonium, phosphate and DON concentrations in open-bottomed benthic chambers placed over sediment patches. These samples were collected between January 1994 and April 1998. The sediment patches used on the reef flat and slope occur between limestone and coral outcrops. Chambers were installed on the windward reef slope of Moku o Loe at 1–5 m depth. This depth range spanned the zone of highest densities of
Dictyosphaeria cavernosa. Bay-bottom chambers were installed in very fine
homoge-neous sediment at a depth of 14 m at site 2 (Fig. 1). Reef flat chambers were installed on patches of coarse sediment at |1 m depth.
by the difficulty in finding large patches of unobstructed sediment on the reef flat and 2
slope. Chambers enclosed 0.075 m of sediments and, depending on the distance the pipe was inserted into the sediment, approximately 11 l of water. All sampling was done during daylight hours and was started in the late morning hours.
Water samples were withdrawn from the chambers by attaching an acid-washed syringe to the excurrent tube, un-crimping the tubes on both ports and withdrawing approximately 60 ml from the chamber. The samples were taken to the surface, filtered, and frozen as described above. The sediment enclosed by the chambers contained up to ten macroinvertebrate burrows, some of which were as large as 1 cm in diameter. The numbers and pumping activity of these animals presumably influenced the concen-trations of dissolved nutrients in the chambers. Ambient water samples were collected during nine of the efflux measurements by drawing water samples each hour from a position 10–15 cm above the sediment and approximately 1 m away from the chamber, i.e. in water equivalent in depth and position to that in the chambers. The estimates of efflux into the chambers were computed by calculating the slope of the nutrient concentration in the chambers versus elapsed time over the first 3 or 4 h of operation. This change in concentration and the volume and area of the chamber, were used to
22 21
calculate efflux rates inmmol m day . This rate is regarded as a net rate of exchange. Additional measurements of efflux were made at two exposed sites on the windward coast of Oahu southeast of Kaneohe Bay, Lanikai (1578439W, 218249N) and Waimanalo (1578419W, 218199N). These sites are in lagoon-like settings near patches of coral and macroscopic algae, with depths of 2–3 m. Each lagoon is protected by fringing reefs 100–300 m seaward, but wave action is stronger at these sites than in Kaneohe Bay and the sediments are correspondingly coarser. Measurements at Lanikai and Waimanalo were made in April and September 1997.
2.4. Sedimentation rate
Rates of sedimentation of particulate organic nitrogen (PON) from the water column to reef slopes in southern Kaneohe Bay were estimated indirectly by placing cylindrical sediment traps at various depths in open water 1 km from the nearest reefs at site 2 (Fig. 1). The traps were placed away from patch and fringing reefs in order to minimize the amount of material in traps that had been created on reefs and / or resuspended from reefs. An additional reason for estimating sedimentation at site 2 was that sedimentation rates had been measured at this site for a year in 1981, shortly after the diversion of sewage effluent from southern Kaneohe Bay. A pilot study of sedimentation rates at different distances from the slope of the fringing reef of Moku o Loe indicated that sedimentation rates at distances from 1 to 10 m off the reef were not higher than at comparable depths at site 2. The weight of sediment in traps placed directly on the reef slope were two times those of traps .1 m off the reef at the same depth. The water depth at site 2 is 14 m. The traps were positioned in the upper 10 m of the water column (2, 4, 7 and 10 m depth) to reduce the contribution of sediment resuspended from the Bay bottom (Taguchi, 1982). The depth range used for sediment traps corresponded with the depth distribution of Dictyosphaeria cavernosa on reef slopes.
21
at flow-rates less than 5 cm s , conditions which should result in accurate estimates of sedimentation rate (Gardner, 1980). Traps were recovered after 24 h to minimize the effects of colonizing organisms. Sediment in the traps was filtered onto pre-combusted GF / F filters, rinsed, dried at 608C, and weighed. A subset of the filters were ground and 40-mg aliquots were used for CHN analysis with a Perkin-Elmer 2400 CHN Analyser. Nitrogen content was only measured for samples collected between March and July 1997. The balance of the samples and the remainder of the ground samples were weighed, combusted at 4508C (4 h) and re-weighed for determination of AFDW. When sediment traps were collected, a 2-l sample of water was collected adjacent to each trap, and was processed in the same way as the sediment trap samples. Suspended sediment
21
concentrations (mg l ) in the traps were estimated from the 2-l water samples, and the dry weights of sediment in the traps were corrected for the suspended material. Suspended sediment usually comprised ,4% of the trapped material. The amount of material caught per day by sediment traps in this study is regarded as the trapping rate, consistent with the terminology of Taguchi (1982). This measure is distinct from the sedimentation rate, which is the trapping rate corrected for the rate of trapping of resuspended material.
3. Results
The concentration of DIN in the water column adjacent to the windward reef slope of Moku o Loe (site 1) was generally less than 0.5mM throughout the year (Fig. 3). The
samples collected at site 2, 1 km windward of the reef slope, had significantly lower nitrate1nitrite values than those in the water column just off the reef slope (site 1), and both of these sites had significantly lower concentrations than the near-substratum samples (Table 1). The concentration of ammonium within 15 cm of the sediments on the reef slope (near-substratum) was significantly greater than the concentrations at site 1 and site 2 (Table 1). Phosphate concentrations were less than 0.2mM at all sites.
Ammonium concentrations in porewater samples from reef slope sediment on the windward Moku o Loe fringing reef increased with sediment depth and reached a maximum value of 60mM at a depth of 50 cm (Fig. 4a). The sediment is anoxic a few centimeters below the surface and hence the concentration of ammonium is 10–40 times greater than the concentration of nitrate1nitrite. Nitrate1nitrite concentrations were generally less than 1 mM in porewater samples. Phosphate concentrations reached a maximum of 6 mM at a depth of about 20 cm.
Ammonium concentrations in the benthic chambers installed on reef slopes increased linearly over the first 6 h of each sampling period (Fig. 5). After 24 h, the ammonium concentration in the chambers with the most rapid rate of efflux had approached 2mM, and the rate of increase in concentration had slowed. The rate of change in concentration in each chamber was calculated by regressing concentration on time and this change was then compared to the change in concentration in each of the nine sets of control samples. The average slope for ammonium concentration versus time in the chamber incubations
21
(0.14mmol h , n524) was significantly greater than the average slope of ammonium
21
concentration versus time for the control runs (0.02 mmol h , n59) (t52.24,
P,0.05, df531). The average slope of ammonium concentrations versus time in the ambient water samples was not significantly different from 0. The average slopes of the nitrate1nitrite concentrations in control and chamber incubations were not significantly different from one another, and the average slope for the nitrate1nitrite concentration in the control incubations was not significantly different from zero.
Ammonium and nitrate1nitrite efflux rates measured on the reef slope varied greatly
Table 1
Concentration of dissolved inorganic nitrogen (mM) in samples from the water column and positions close to
a
the sediments (mean, standard deviation and sample size)
Water column Water column 1–15 cm above
Central So. |3 m above sediments
Bay reef slope of reef slope
(Site 2) (Site 1) (near-substratum)
NH4 NO31NO2 NH4 NO31NO2 NH4 NO31NO2
Mean 0.13 0.02 0.21 0.25 0.36 0.36
S.D. 0.10 0.02 0.12 0.29 0.17 0.21
Sample size 14 14 92 92 33 33
a
Stimson
,
S
.T
.
Larned
/
J.
Exp
.
Mar
.
Biol
.
Ecol
.
252
(2000
)
159
–
180
169
Fig. 5. Average concentration of NH in domes over time (4 61 S.E.). Concentration values were included in this figure if they were measured within 20 min of the plotted time. The concentration values are from the operation of 25 domes on the reef slope. Numbers on the figure represent the sample sizes on which the statistics are based.
among runs, the standard deviations were large and some values were negative, but the frequency distribution of efflux values for both ammonium and nitrate1nitrite were not skewed (Fig. 6, Kaneohe Bay reef slopes, ,5 m depth). The mean ammonium efflux
22 21 22 21
rate was 490 mmol m day (equivalent to 6.9 mg N m day , Table 2) and was significantly different from zero. Nitrate1nitrite efflux rates were generally lower than
22 21
ammonium efflux rates (Fig. 6), and averaged 123mmol m day (equivalent to 1.7
22 21
mg N m day , Table 2). This rate was not significantly different from zero. Water samples from 8 of the reef slope chambers were analyzed for total dissolved nitrogen (TDN), and DON efflux rates were then calculated by subtracting DIN from TDN
22 21
concentrations. The average DON efflux rate, 1757mmol m day , was nearly three times greater than the average DIN efflux rate. The average efflux rate of all three forms
22 21
of nitrogen combined was 32.2 mg N m day . Efflux rates varied widely, because they were assessed at sites with heterogeneous sediments, over a range of depths on the slope, in different seasons, and varying numbers of burrowing animals occupied the sediments enclosed by the chambers.
Efflux rates were also measured in three other environments for comparison with Kaneohe Bay’s reef slope environment: the Bay bottom at site 2, the Moku o Loe reef flat, and the lagoons at Lanikai and Waimanalo. DIN efflux rates measured at the Bay bottom were much greater than those measured on the Moku o Loe reef slope (Table 2). DIN efflux from the shallow, coarse sediments of the Moku o Loe reef flat (1 m depth), and Lanikai and Waimanalo (2–3 m depth) were substantially lower than those measured on the reef slope or the Bay bottom (Table 2).
Fig. 6. Comparison of efflux rates in south Kaneohe Bay with efflux rates measured at other tropical reef sites. Reef slope values are from this study and can be compared to the values for ‘Other reefs ,5 m’ reported in Hansen et al. (1987), Johnstone et al. (1989), Iizume (cited in D’Elia and Wiebe (1990) and Williams et al. (1985). Deep Kaneohe Bay lagoon values are from Harrison (1981) and this study and can be compared with the vales for ‘Other reefs 10–16 m’ reported in Boucher and Clavier (1990), Boucher et al. (1994), Fisher et al. (1990), Hansen et al. (1987) and Harrison (1983). Reef flat values are from Haberstroh (1994) and the present study.
22 21
period was linearly related to depth (trapping rate (g dry sediment m day )50.62 depth (m)13.51, standard error of slope50.19, t-test of Ho b 50: t53.24, P,0.001,
n5224) over a range of depths from 3 to 10 m. The slope of the relationship between % organic content of the sediments and depth was not significantly different from zero for a subset of 134 of the samples. The mean % organic content was 29.2% (standard deviation514.1, n5134). PON concentrations were measured in 41 trap samples collected from 3 to 10 m depth at site 2; there was no significant regression between
22 21
PON concentration and depth, and the average trapping rate was 61 mg N m day (standard deviation533, n541) (Table 3). Trapping rates potentially overestimate rates of PON sedimentation in Kaneohe Bay because resuspension may be high in the shallow water column. The estimated rate of sedimentation of new material is much lower
22 according to Taguchi’s (1982) formula, which corrects for resuspension: 12 mg N m
21 day .
4. Discussion
Table 2
22 21 a
Comparison of efflux rates (mmol m day ) at coral reef sites on windward Oahu
Site NH4 NO31NO2 PO4 DON
Kaneohe
Reef flat Average 469.9 2490.7 34.6 nd
Range 2255, 1734 2950,2101 280, 145
Sample size 9 9 9
Reef slope Average 490.5 122.7 83.6 1757
S.D. 512.6 262.8 72.8 1719
Sample size 23 23 24 8
Bay bottom Average 1034.0 295.0 74.8 1645
(South Bay) S.D. 937.8 270.4 58.1 701, 3298
Sample size 13 13 13 3
Bay bottom (1978–1979, Post diversion, Harrison, 1981)
South Bay Average 959 218 82 nd
S.D. 556 161 60
Sample size 15 15 15
Mid Bay Average 1073 3 16 nd
S.D. 844 59 77
Sample size 17 17 18
North Bay Average 489 194 47 nd
S.D. 192 138 45
Sample size 18 18 18
Lanikai-Kailua
Lagoon floor Average 97 149 30 nd
S.D. 150 132 56
Sample size 7 7 7
a
Values are means, standard deviations (or range) and sample sizes. nd, no data.
detectable effect on algal productivity (Larkum and Koop, 1997), no detectable effect on algal biomass (Kinsey and Domm, 1974; Larkum and Koop, 1997), or an effect on biomass in one season and not in another (Hatcher and Larkum, 1983). The frequent lack of effect of experimental nitrogen addition at these sites may have been because many macroalgae require only low concentrations to sustain maximum growth (DeBoer et al., 1978; Lapointe, 1997), or because nitrogen concentrations in the benthic microenvironments occupied by the algae were already elevated or near-saturating. Elevated nitrogen concentrations in the benthic microenvironment may have been due to efflux from the sediments (Larkum and Koop, 1997; Larned and Stimson, 1996; Larned, 1998), and the experimental enrichment levels, though large relative to water column concentrations, may not have been large enough to markedly increase nitrogen availability to the algae. A corollary of this second interpretation is that nutrient concentrations measured in the benthic microenvironment are more representative of nutrient availability to benthic autotrophs than nutrient concentrations in the overlying water column.
Table 3
Characteristics of trapped sediments in south Kaneohe Bay
Characteristics Samples collected Samples collected Results of June 1996 to March, June, and Taguchi (1982) July 1997 July 1997 Sept. 1977–Dec. 1978
Depth (m) 7–10 3–10 10
Sediment nitrogen was estimated using Eq. 2 in Taguchi (1982). Values are means, standard deviations and sample sizes.
(Stimson et al., 1996; Larned, 1998) lend support to the view that nutrient-enriched benthic microenvironments preclude macroalgae from responding to experimental fertilization. The morphologies of several macroalgal species have been shown to reduce the diffusion of nutrients released from underlying sediments into the water column, resulting in elevated nutrient concentrations beneath thalli (Thybo-Christesen et al., 1993; Larned and Stimson, 1996; Larned, 1998). Results of the field experiment carried out by Larned and Stimson (1996) indicated that, if D. cavernosa thalli have access to DIN released from underlying sediments, the thalli can grow, but if a barrier is placed between the sediment and the thalli, the thalli cannot grow.
ammonium concentration with depth; a similar pattern is seen in Fig. 4b for the results from the other tropical sites, but the average values in Kaneohe Bay are consistently higher.
The DIN efflux rates in Kaneohe Bay can also be compared to published values for similar tropical sites (Fig. 6). For the purpose of these comparisons, only direct measurements of efflux rates reported in other studies are included; efflux rates calculated from porewater DIN concentrations have been omitted because they are generally an order of magnitude lower than measured rates (Callender and Hammond, 1982). Among the studies with measured efflux rates, there are some in which the water within the chamber was stirred to prevent the development of concentration gradients. If the efflux rates measured in chambers is to simulate actual rates, such stirring should at least simulate prevailing water flow-rates, but this is not usually stated to be the case. One study (Callender and Hammond, 1982) compared the efflux rate in stirred and unstirred chambers and found that stirring resulted in a 43% increase in the efflux rate; a difference which is comparable to the published within and between study variability in efflux rates. For this analysis stirred chambers are not distinguished from unstirred chambers.
The average efflux rates of ammonium and nitrate1nitrite measured on the Moku o Loe reef slope and the bottom of the south Bay (sites 1 and 2) are higher than the values measured at the other windward Oahu sites, Lanikai and Waimanalo (Table 2), and are higher than those measured at St. Croix, Enewetak, One Tree Island and Davies Reef (Fig. 6, ‘other reefs 10–16 m’). Comparisons of efflux rates can also be made within depth classes between this and other coral reef studies; the shallow reef slope values from Moku o Loe (,5 m depth) can be compared to values from ‘other reefs ,5 m’, and the values from the bottom of Kaneohe Bay (14 m depth) can be compared to those from ‘other reefs 10–16 m depth’. In both cases, Kaneohe Bay values are greater. Efflux rates were also measured on the Moku o Loe reef flat and are comparable to those measured by Haberstroh (1994) on a nearby reef using similar techniques, but no other reef flat efflux values are available to compare with these. Across the three depth classes within the Bay, and across the two depth classes reported in other studies, there appears to be an increase in efflux rate with depth (Fig. 6). The average DIN efflux rate we have measured at the bay-bottom is very similar to the post sewage-diversion rates reported by Harrison (1981) in the southern, central and northern basins of the Bay (Table 2), but higher than the value reported for the north bay by Harrison (1981). The high DIN efflux rates reported for the Kaneohe Bay lagoon floor in this study and in Harrison’s (1981) study are probably of little direct consequence to the productivity and persistence of
Dictyosphaeria cavernosa which grows in shallow water. The lagoon floor is too silty
and turbid to support D. cavernosa or corals; the distribution of D. cavernosa generally extends only to 6–7 m depth and is restricted to reef slopes (Hunter and Evans, 1995). Although efflux was measured in this study in a manner similar that of other studies, we may have underestimated the rate at which DIN is supplied to Dictyosphaeria
cavernosa from reef slope sediments. Our benthic chambers were positioned on well-lit
patches of sediment between coral colonies and D. cavernosa thalli. Microalgae in and on these sediments may have taken up some of the DIN released from the sediments
¨ ´
less abundant beneath D. cavernosa thalli because the irradiance (photosynthetically active radiation) beneath thalli is less than 1% of the irradiance above thalli (unpublished in situ measurements). Thus DIN efflux rates from shaded sediments beneath D.
cavernosa thalli may be higher than from the sediments enclosed by our chambers.
Additionally, efflux rates were measured in the day; these rates may be lower than those which could be measured at night due to uptake by micro-flora in the upper layer of the sediments during the day.
The generally higher efflux rates of DIN in Kaneohe Bay compared with other tropical sites could be due to a number of causes: (1) high current rates of input of PON to the sediments due to proximity to suburban areas; (2) high rates of PON input prior to
3
1978, when 20 000 m per day of sewage effluent was being discharged into southern Kaneohe Bay; or (3) high rates of nutrient recycling. The current rate of PON input to the lagoon floor of Kaneohe Bay (the trapping rate at 10 m) is comparable to values from other tropical sites (Table 4), and is much lower than the rate measured earlier at the same site (Taguchi, 1982; Table 4). Both trapping and sedimentation rates of PON are now substantially lower than the values reported for the year following the diversion of sewage from the South Bay. In that year, Taguchi (1982) measured a trapping rate of
22 21 22 21
229 mg m day and a sedimentation rate of 59 mg m day at a depth of 10 m. The decrease in the rate of sedimentation over the last 20 years is consistent with the declines in phytoplankton productivity, declines in water column DIN concentration and
Table 4
Comparisons of particulate organic nitrogen trapping rates among studies carried out in the tropics.
Site Depth Rate Citation
22 21
(m) (mg PON m day ) Great Barrier Reef, One Tree Island
Back reef 1.2 160 Koop and Larkum (1987)
Lagoon 3 94 Koop and Larkum (1987)
Lagoon 4.5 96 Koop and Larkum (1987)
Tuamotu Atoll, French Polynesia
Lagoon 15 36 Charpy and Charpy-Roubaud (1991)
New Caledonia
a
Lagoon 11–12 23–35 Clavier et al. (1995)
Kaneohe Bay Central so. Bay
a decrease in the cell-size of phytoplankton in the water column of the Bay over the same period (Laws and Allen, 1996).
The estimated PON trapping rate on shallow reef slopes where Dictyosphaeria
cavernosa occurs (1–6 m depth) would be somewhat lower than the rate reported for
22 21
depths of 7–10 m (61 mg m day , Table 3). At present, the PON trapping rate on
22 21
shallow reef slopes (1–6 m depth) is estimated to be 55 mg m day . This rate is
22 higher than the rate of dissolved nitrogen efflux from these sediments (32 mg m
21
day , Table 2), suggesting that the present PON sedimentation rate could account for a
22 21
large fraction of the present efflux rate. The 55 mg m day value includes resuspended material in sediment traps deployed in the upper water column, but does not include PON produced on the reef and settling onto the reef slope. Some fraction of the DIN efflux could be the result of N2 fixation which has been measured in similar environments (O’Neil and Capone, 1989; King et al., 1990; O’Donohue et al., 1991; Capone et al., 1992).
Dictyosphaeria cavernosa remains abundant in parts of Kaneohe Bay despite low
nutrient concentrations in the water column. There are at least three reasons for its persistence on many reef slopes, an environment usually occupied by macroalgae only if the reefs are heavily disturbed. First, its persistence is partly due to localized sources of DIN in close proximity to D. cavernosa thalli. The localized sources are sediments beneath D. cavernosa with high porewater DIN concentrations, and invertebrates growing on the undersides of thalli and on solid surfaces below thalli. Efflux of sediment-derived DIN and excretion by invertebrates result in the development of high DIN concentrations beneath D. cavernosa, concentrations which are substantially higher than those in the adjacent water column (Stimson et al., 1996; Larned and Stimson, 1996; Larned, 1997). The morphology of D. cavernosa contributes to the development of a nutrient-rich microenvironment because its solid thallus slows the diffusion of DIN from the sub-thallus space. Secondly, the persistence of D. cavernosa is due in part to its ability to capitalize on high nutrient concentrations. Its growth rate increases with increased nutrient concentrations up to |17mM (Larned and Stimson, 1996). Finally, its persistence is also attributable to the fact that this species ranks low in the preference hierarchy of grazing fishes in Kaneohe Bay (Stimson et al., 2000), and the intensity of their grazing on D. cavernosa is not high enough to prevent its encroachment into the zone of most active coral growth on the outer reef flat and upper reef slope.
Acknowledgements
reflect the views of NOAA or any of its subagencies. UNIHI SEAGRANT contribution] [JC-99-10. This research was completed before S. Larned joined the US Environmental
Protection Agency. It has been subjected to the Agency’s peer and administrative review, and it had been approved for publication as an EPA document. Mention of trade names or commercial products does not constitute endorsement or recommendation for use. [RW]
References
Boon, P.I., 1986. Uptake and release of nitrogen compounds in coral reef and seagrass, Thalassia hemprichii (Ehrenb.) Aschers., bed sediments at Lizard Island, Queensland. Aust. J. Mar. Freshw. Res. 37, 11–19. Banner, A.H., 1974. Kaneohe Bay, Hawaii: Urban pollution and a coral reef ecosystem. Proc. 2nd Int. Coral
Reef Symp. 2, 685–702.
Boucher, G., Clavier, J., 1990. Contribution of benthic biomass to overall metabolism in New Caledonia lagoon sediments. Mar. Ecol. Prog. Ser. 64, 271–280.
Boucher, G., Clavier, J., Garrigue, C., 1994. Estimation of bottom ammonium affinity in the New Caledonia lagoon. Coral Reefs 13, 13–19.
Callender, E., Hammond, D.E., 1982. Nutrient exchange across the sediment water interface in the Potomac River Estuary. Estuar. Coast. Shelf Sci. 15, 395–413.
Capone, D.G., Dunham, S.E., Horrigan, S.G., Dugay, L.E., 1992. Microbial nitrogen transformations in unconsolidated coral reef sediments. Mar. Ecol. Prog. Ser. 80, 75–88.
Charpy, L., Charpy-Roubaud, C.J., 1991. Particulate organic matter fluxes in a Tuamotu atoll lagoon (French Polynesia). Mar. Ecol. Prog. Ser. 71, 53–63.
Charpy-Roubaud, C., Charpy, L., Sarazin, G., 1996. Diffusional nutrient fluxes at the sediment water interface and organic matter mineralization in an atoll lagoon (Tikehau, Tuamotu Archipelago, French Polynesia). Mar. Ecol. Prog. Ser. 132, 181–190.
Clavier, J., Chardy, P., Chevillon, C., 1995. Sedimentation of particulate matter in the south-west lagoon of New Caledonia: Spatial and temporal patterns. Estuar. Coast. Shelf Sci. 40, 281–294.
Corredor, J.E., Morell, J., 1985. Inorganic nitrogen in coral reef sediments. Mar. Chem. 16, 379–384. Corredor, J.E., Capone, D.G., 1985. Studies on nitrogen diagenesis in coral reef sands. Proc. 5th Int. Coral
Reef Symp. 3, 395–399.
DeBoer, J.A., Guigli, H.J., Israel, T.L., D’Elia, C.F., 1978. Nutritional studies of two red algae. I. Growth rate as a function of nitrogen source and concentration. J. Phycol. 14, 261–266.
Delgado, O., Lapointe, B.E., 1994. Nutrient-limited productivity of calcareous versus fleshy macroalgae in a eutrophic, carbonate-rich tropical marine environment. Coral Reefs 13, 151–159.
D’Elia, C.F., Wiebe, W.J., 1990. Biogeochemical nutrient cycles in coral-reef ecosystems. In: Dubinsky, Z. (Ed.), Ecosystems of the World. Coral Reefs, Vol. 25. Elsevier, Amsterdam, pp. 49–74.
Entsch, B., Boto, K.G., Sim, R.G., Wellington, J.T., 1983. Phosphorus and nitrogen in coral reef sediments. Limnol. Oceanogr. 28, 465–476.
Fisher, T.R., Morrissey, K.N., Smith, L.K., Williams, S.L., Baptist, G., Ward, L.G., Twilley, R., D’Elia, C.F., Zimba, P.F. (Eds.), 1990. Final Science Report of NURP Hydrolab Mission 85-1. NOAA, Washington, DC. Furnas, M.J., Mitchell, A.W., Gilmartin, M., Revelante, N., 1990. Phytoplankton biomass and primary production in semi-enclosed reef lagoons of the central Great Barrier Reef, Australia. Coral Reefs 9, 1–10. Gardner, W.D., 1980. Sediment trap dynamics and calibration a laboratory evaluation. J. Mar. Res. 38, 17–39. Gray, J.S., 1985. Nitrogenous excretion by meiofauna from coral reef sediments: Mecor 5. Mar. Biol. 89,
31–35.
Haberstroh, P.R., 1994. Wave-forced porewater mixing and nutrient flux in a coral reef framework. PhD dissertation, University of Hawaii, Honolulu, Hawaii, 249 pp.
Hansen, J.A., Alongi, D.M., Moriarty, D.J.W., Pollard, P.C., 1987. The dynamics of benthic microbial communities at Davies Reef, Central Great Barrier Reef. Coral Reefs 6, 63–70.
Harrison, J.T. III, 1981. The influence of Alpheus mackayi on ecosystem dynamics in Kaneohe Bay. PhD dissertation, University of Hawaii, Honolulu, Hawaii, 112 pp.
Harrison, III J.T., 1983. Metabolism of interreef sediment communities. In: Reaka, M.L. (Ed.), Ecology of Deep and Shallow Coral Reefs. NOAA, Washington, DC, pp. 145–149.
Hatcher, B.G., 1988. Coral reef primary productivity: a beggar’s banquet. Trends Ecol. Evol. 3, 106–111. Hatcher, B.G., Larkum, A.W.D., 1983. An experimental analysis of factors controlling the standing crop of the
epilithic algal community on a coral reef. J. Exp. Mar. Biol. Ecol. 69, 61–84.
Hunter, C.L., Evans, C.W., 1995. Reefs in Kaneohe Bay, Hawaii: two centuries of western influence and two decades of data. Bull. Mar. Sci. 57, 501–515.
Johannes, R.E., 1980. The ecological significance of submarine discharge of groundwater. Mar. Ecol. Prog. Ser. 3, 365–373.
Johnstone, R., Koop, K., Larkum, A.W.D., 1989. Fluxes of inorganic nitrogen between sediments and water in a coral reef lagoon. Proc. Linn. Soc. NSW 110, 220–227.
King, G.M., Carlton, R.G., Sawyer, T.E., 1990. Anaerobic metabolism and oxygen distribution in the carbonate sediments of a submarine canyon. Mar. Ecol. Prog. Ser. 58, 275–285.
Kinsey, D.W., Domm, A., 1974. Effects of fertilization on a coral reef environment: Primary production studies. Proc. 2nd Int. Coral Reef Symp. 1, 49–66.
Koop, K., Larkum, A.W.D., 1987. Deposition of organic material in a coral reef lagoon, One Tree Island, Great Barrier Reef. Estuar. Coast. Shelf Sci. 25, 1–9.
Lapointe, B.E., 1989. Macroalgal production and nutrient relations in oligotrophic areas of Florida Bay. Bull. Mar. Sci. 44, 312–323.
Lapointe, B.F., 1997. Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol. Oceanogr. 42, 1119–1131.
Lapointe, B.E., O’Connell, J., 1989. Nutrient-enhanced growth of Cladophora prolifera in Harrington Sound, Bermuda: eutrophication of a confined, phosphorus-limited marine ecosystem. Estuar. Coast. Shelf Sci. 28, 347–360.
Lapointe, B.E., Clark, M.W., 1992. Nutrient inputs from the watershed and coastal eutrophication in the Florida Keys. Estuaries 15, 465–576.
Lapointe, B.E., Matzie, W.R., 1996. Effects of stormwater nutrient discharges on eutrophication processes in nearshore waters of the Florida Keys. Estuaries 19, 422–435.
Lapointe, B.E., Littler, M.M., Littler, D.S., 1987. A comparison of nutrient-limited productivity in macroalgae from a Caribbean barrier reef and from a mangrove ecosystem. Aquat. Bot. 28, 243–255.
Lapointe, B.E., Littler, M.M., Littler, D.S., 1992. Nutrient availability to marine macroalgae in siliciclastic versus carbonate-rich castal waters. Estuaries 15, 75–82.
Larkum, A.W.D., Koop, K., 1997. ENCORE, algal productivity and possible paradigm shifts. Proc. 8th Int. Coral Reef Symp. 1, 881–884.
Larned, S.T., 1997. Nutrient limited growth and sources of nutrients for coral reef macroalgae. PhD dissertation, University of Hawaii, Honolulu, Hawaii, 178 pp.
Larned, S.T., 1998. Nitrogen- versus phosphorus-limited growth and sources of nutrients for coral reef macroalgae. Mar. Biol. 132, 409–421.
Larned, S., Stimson, J., 1996. Nitrogen-limited growth in the coral reef chlorophyte Dictyosphaeria cavernosa, and the effect of exposure to sediment-derived nitrogen on growth. Mar. Ecol. Prog. Ser. 145, 95–108. Lavery, P.S., McComb, A.J., 1991. Macroalgal sediment nutrient interactions and their importance to
macroalgal nutrition in a eutrophic estuary. Estuar. Coast. Shelf Sci. 32, 281–295.
Laws, E.A., Allen, C.B., 1996. Water quality in a subtropical embayment more than a decade after diversion of sewage discharges. Pac. Sci. 50, 194–210.
Lewis, J.B., 1987. Measurements of groundwater seepage flux onto a coral reef: spatial and temporal variations. Limnol. Oceanogr. 32, 1165–1169.
Littler, M.M., Littler, D.S., Titlyanov, E.A., 1991. Comparisons of N- and P-limited productivity between high granitic islands and low carbonate atolls in the Seychelles Archipelago: a test of the relative-dominance paradigm. Coral Reefs 10, 199–209.
Littler, M.M., Littler, D.S., Lapointe, B.E., 1992. Modification of tropical reef community structure due to cultural eutrophication: the southwest coast of Martinique. Proc. 7th Int. Coral Reef Symp. 1, 335–343. Maragos, J.E., Evans, C., Holthus, P., 1985. Reef corals in Kaneohe Bay six years before and after termination
of sewage discharges. Proc. 5th Int. Coral Reef Symp. 4, 189–194.
McGlathery, K.J., Howarth, R.W., Marino, R., 1992. Nutrient limitation of the macroalga, Pennicillus
capitatus, associated with subtropical seagrass meadows in Bermuda. Estuaries 15, 18–25.
Meyer, J.L., Schultz, E.T., 1985. Tissue condition and growth rate of corals associated with schooling fish. Limnol. Oceanogr. 30, 157–166.
O’Donohue, M.J., Moriarty, D.J.W., Mac Rae, I.C., 1991. Nitrogen fixation in sediments and the rhizosphere of the seagass Zostera capricorni. Microbiol. Ecol. 22, 53–64.
O’Neil, J.M., Capone, D.G., 1989. Nitrogenase activity in tropical carbonate marine sediments. Mar. Ecol. Prog. Ser. 56, 145–156.
Pigott, J.D., 1977. Early diagenesis of dissolved sulfur and nitrogen species in Jamaican reef sediments (determined by in situ sampling). Proc. 3rd Int. Coral Reef Symp. 2, 534–540.
Rizzo, W.M., 1990. Nutrient exchanges between the water column and a subtidal benthic microalgal community. Estuaries 13, 219–226.
Rodgers, S.K., Cox, E.F., 1999. Rate of spread of the introduced rhodophytes Kappaphycus alvarezii,
Kappaphycus striatum and Gracilaria salicornia and their current distribution in Kaneohe Bay, Oahu,
Hawaii. Pac. Sci. 53, 232–241.
Russell, D.J., 1992. The ecological invasion of Hawaiian reefs by two marine red algae, Acanthophora
spicifera (Vahl) Boerg. and Hypnea musciformis (Wulfen) J. Ag., and their association with two native
species, Laurencia nidifica J. Ag. and Hypnea cervicornis J. Ag. ICES Mar. Sci. Symp. 194, 110–125. Sansone, F.J., Andrews, C.C., Buddemeier, R.W., Tribble, G.W., 1988. Well-point sampling of reef interstitial
water. Coral Reefs 7, 19–22.
Schaffelke, B., Klumpp, D.W., 1998. Short-term nutrient pulses enhance growth and photosynthesis of the coral reef macroalga Sargassum baccularia. Mar. Ecol. Prog. Ser. 170, 95–105.
Shashar, N., Kinane, S., Patterson, M.R., 1996. Hydromechanical boundary layers over a coral reef. J. Exp. Mar. Biol. Ecol. 199, 17–28.
Smith, S.V., Kimmerer, W.J., Laws, A.E., Brock, R.E., Walsh, T.W., 1981. Kaneohe Bay sewage diversion experiment: perspectives on ecosystem responses to nutritional perturbation. Pac. Sci. 35, 279–402. Stimson, J., Larned, S., McDermid, K., 1996. Seasonal growth of coral reef macroalga Dictyosphaeria
cavernosa (Forskal) Borgesen and the effects of nutrient availability, temperature and herbivory on growth
rate. J. Exp. Mar. Biol. Ecol. 196, 53–67.
Stimson, J., Larned, S.T., Conklin, E., 2000. Effects of herbivory, nutrient levels, and introduced algae on the distribution and abundance of the invasive macroalga Dictyosphaeria cavernosa in Kaneohe Bay, Hawaii. Coral Reefs (submitted).
¨ ´
Sundback, K., Graneli, W., 1988. Influence of microphytobenthos on the nutrient flux between sediment and water: a laboratory study. Mar. Ecol. Prog. Ser. 43, 63–69.
Szmant, A.M., Forrester, A., 1996. Water column and sediment nitrogen and phosphorus distribution patterns in the Florida Keys, USA. Coral Reefs 15, 21–41.
Taguchi, S., 1982. Sedimentation of newly produced particulate organic matter in a subtropical inlet, Kaneohe Bay, Hawaii. Estuar. Coast. Shelf Sci. 14, 533–544.
Taguchi, S., Laws, E.A., 1989. Biomass and compositional characteristics of Kaneohe Bay, Oahu, Hawaii, phytoplankton inferred from regression analysis. Pac. Sci. 43, 316–331.
Thybo-Christesen, M., Rasmussen, M.B., Blackburn, T.H., 1993. Nutrient fluxes and growth of Cladophora
sericea in a shallow Danish bay. Mar. Ecol. Prog. Ser. 100, 273–281.
Tribble, G.W., Sansone, F.J., Li, Y.-H., Smith, S.V., Buddemeier, R.W., 1988. Material fluxes from a reef framework. Proc. 6th Int. Coral Reef Symp. 2, 577–582.
Williams, S.L., Carpenter, R.C., 1988. Nitrogen-limited primary productivity of coral reef algal turfs: potential contribution of ammonium excreted by Diadema antillarum. Mar. Ecol. Prog. Ser. 47, 145–152. Williams, S.L., Gill, I.P., Yarish, S.M., 1985. Nitrogen cycling in backreef sediments (St. Croix, US Virgin
