Coral Reefs (2001) 20: 341±346 DOI 10.1007/s00338-001-0184-7
R EP O RT
M.J. Atkinson á J.L. Falter á C.J. Hearn
Nutrient dynamics in the Biosphere 2 coral reef mesocosm: water velocity controls NH4 and PO4 uptake
Received: 1 March 2001 / Accepted: 15 July 2001 / Published online: 25 October 2001 Ó Springer-Verlag 2001
Abstract The Biosphere 2 coral reef biome is a large, fully enclosed, self-sustaining mesocosm. Water is moved throughout the mesocosm by waves. Inorganic and organic nutrients were monitored weekly from 1995 to 2000. Eight nutrient-uptake experiments were conducted to measure uptake-rate constants (S, m s±1) for NH4, PO4, and NO3. Nutrient concentrations were low, except for DON, and typical of coral-reef ecosystems (means: NH4=0.63, NO3=0.62, PO4=0.05, SiO3=9.5, DON=41.2, DOP=0.26 mmol m±3). Nutrient uptakerate constants varied in the range 54±126´10±6 m s±1 (4.6±11 m day±1) and correlated with water velocity. These rates, however, are 2±3-fold higher than rates for equivalent water velocities in steady, non-wave ¯ows. Nutrients are recycled within the biome at rates sucient to support gross production and, even in this recycling system, nutrient-uptake rates are mass transfer-limited.
Introduction Rates of inorganic nutrient uptake (PO4, NO3, NH4) into communities of corals and macro-algae can be controlled by diusion through nutrient-depleted boundary layers, which are immediately adjacent to the surfaces of the organisms (Baird and Atkinson 1997). This control of uptake by diusion arises when uptake kinetics at the
M.J. Atkinson (&) á J.L. Falter Hawaii Institute of Marine Biology, PO Box 1346, Kanoehe, Hawaii 96744, USA E-mail:
[email protected] C.J. Hearn Oceanography, University College, University of New South Wales, Canberra, ACT 2600, Australia Supplementary address: M.J. Atkinson Biosphere 2 Center, Columbia University, Oracle, AZ, USA
surfaces of organisms far exceed rates of diusion through diusive boundary layers. This condition or response, termed mass-transfer limitation, has been studied in enclosed ¯umes with assemblages of experimental organisms, but has not yet been demonstrated for natural communities, in which nutrient recycling is commonly considered to dominate nutrient ¯ux. If mass-transfer limitation of nutrient uptake exists for natural ecosystems, then nutrient uptake is directly related to the concentration in the water and water velocity, and not strictly proportional to biomass. Our parameterization (Bilger and Atkinson 1992; Thomas and Atkinson 1997) denotes that benthic biomass can only in¯uence nutrient uptake by its control on the dissipation of energy from bottom friction. Thus, in tropical seas, where nutrient concentrations are relatively constant, nutrient uptake by benthic communities would be largely controlled by water velocity. For example, given the range of bottom friction and water velocities over typical fringing reefs, the estimated ®rstorder rate constants for nutrient uptake may vary 20fold. If mass-transfer limitation exists on natural reefs, then nutrient input into these systems must be primarily dependent on oceanic forcing and not strictly uniform, seasonally or spatially, as generally assumed by most ecologists. It is important to verify mass-transfer control of nutrient uptake into benthic systems which are dominated by nutrient recycling. We chose to study nutrientuptake kinetics in the Biosphere 2 coral reef mesocosm, a fully enclosed, self-sustaining mesocosm in which the water velocity is controlled by a wave machine. Nutrients must be completely recycled in this enclosed system to sustain new growth of plants. The question which is addressed here is that, if mass-transfer control occurs in the Biosphere 2 mesocosm, nutrient uptake should then be positively correlated with water velocity. Our ®rst eort was to describe the nutrient-turnover or recycling characteristics and long-term performance of the biome, then determine whether uptake rates are related to water velocity.
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Methods Biosphere 2 coral reef biome The Biosphere 2 Center is located 15 km north of Tucson, Arizona, in the foothills of the Catalina mountains (32°34¢N, 110°51¢W) and is described in Atkinson et al. (1999). Brie¯y, the coral reef biome has a volume of 2,650 m3, a water surface area of 711 m2 with 850 m2 of benthos, including benthos on the walls of the tank. The water volume to planar surface area of benthos is 3.1 m. The biome is divided into four distinct zones (Fig. 1) ± ocean, fore-reef, reef ¯at, and shallow lagoon. Water depths range from 6 m in the ocean to 0.1 m at the shallowest part of the reef ¯at. The fore-reef, reef ¯at, and shallow lagoon cover a projected area of approximately 590 m2. Waves (20±30 cm in height) are created by a vacuum-driven wave generator whose out¯ow is located 0.5 m below the water surface, along one half of the south wall of the biome. The waves impinge on the fore-reef, dissipate most of their energy on the reef ¯at, and help drive water exchange between the ocean and the lagoon. This water exchange is further enhanced by pumping water from intakes located on the lagoon ¯oor and underneath the dive platform to the bottom of the ocean. This forced ¯ow is sent through heat exchangers, which maintain constant water temperature within the biome at 26.50.5 °C. The mixing time of the ocean is roughly 1 h (Atkinson et al. 1999). Water lost by evaporation is re-added as low-nutrient freshwater de-ionized by reverse osmosis.
The benthic community within the B2 reef biome is dominated by calcareous and non-calcareous macro-algae belonging to the Chlorophyta, Rhodophyta, and Phaeophyta (Atkinson et al. 1999). The macro-algae include 11 genera of green algae, eight of red, two of brown, and some blue-greens, with a total of 50 species of algae. There are, however, only ®ve dominant species of algae, which vary in their relative abundances: Amphiroa fragillisima, Amphiroa rigida, Chondria dascyllus, Gelidiopsos intricata, and Haptilon cubense. There are approximately 55 species of invertebrates which live associated with the algae. The ®ve dominant species are taxonomically diverse. In order of relative abundance, these are a ®reworm (Amphinomidae, 44% total), an amphipod (Ceradocus rubromaculatus, 19% total), a white calcareous sponge (Leuconia sp, 12% total), an unidenti®ed snail (3% total), and a brittle star (Ophiolepis paucispina, 3% total). There are 25 genera of coral, two genera of sponges, 16 genera of ®sh, with seven genera of echinoids and three of large crustaceans. Community metabolism is similar to high-latitude coral reef lagoons (Kinsey 1985) ± P averages 17056 and R averages 17347 mmol O2 m±2 day±1 (Falter et al. 2001). Incident light levels to the biome are relatively low in comparison with low-latitude reefs. Typical daily maxima of measured PAR irradiance at the reef ¯at (0.5 m deep ) range between 1,200 and 1,400 lE m±2 s±1 or roughly three quarters the maximum PAR values found in a lower-latitude reef (1,500±2,000 lE m±2 s±1 in Moorea, French Polynesia, 17°29¢S; Gattuso et al. 1993, 1996). The B2 space frame window removes nearly all of the incident UV light. Total alkalinity and total dissolved inorganic C have been manipulated in the biome to control CO3 activities and CO2 partial pressure (DIC: 1,800±2,100 lM; pCO2: 200±700 latm; aragonite saturation state: 2.4±5.1; Langdon et al. 2000). Water sampling
Fig. 1 Planar view of the Biosphere 2 ocean. The depth contours are in meters; the volume-to-surface-area ratio is 3.1 m
To describe nutrient concentrations, water samples were taken every week from 2-m depth near the dive platform (Fig. 1). The mixing time of the ocean is about 1 h based on a lithium and nutrient mixing experiment (Atkinson et al. 1999). Water samples taken from this location are representative of the bulk concentration. To measure the rate constant for nutrient uptake, NH4 (about 1,500 g of NH4Cl) and PO4 (about 350 g of KH2PO4) were mixed into a 20-l bucket and dumped in the ocean o the dive platform. Sucient NH4 and PO4 were added to raise concentrations to about 10 and 1 mmol m±3, respectively. The water mixes uniformly in the deep end of the biome within about 20 min. We waited about 1 h after addition of the nutrients, and then began sampling over the next 4±5 days, with half the samples taken in the ®rst 2 days and the remaining half taken over the next 2±3 days. This sampling protocol gives an even distribution of points across the full range of nutrient concentrations. Concentration data were ®tted to a ®rst-order decay equation having a constant nutrient release rate. The biome is completely enclosed, relying on recycled nutrients, so it is appropriate to add a release rate or excretion term, R/k, to the exponential decay equation: Y=(Yo±R/k) exp (±kt)+R/k. Y is the concentration of the added nutrient (NH4, NO3, PO4), R is the release rate in mmol m±2 min±1, k is the rate constant, and t is time in minutes for our results. R/k represents the steady concentration when t is large, after all of the added nutrients are removed from the water. k times the volume/surface area ratio of 3.1 m times minutes per day gives a rate constant (S) in units of m day±1. Because the amount of N and P removed from the water is only 1±2% of the estimated total nutrient in the benthos (30 mmol m±2 versus 2,000 mmol m±2), we assume the excretion rate, R, is constant for these ®ts. Water samples were frozen within 15 min, transported to Hawaii on dry-ice, and run for nutrients on a Technicon II Autoanalyzer in the SOEST Analytical Service. Initially we measured the rate constants over a 2-year period, August 1996 to February 1998, then we measured them with respect to water velocity during a summer period, July 1999, and a winter period, January 2000.
343 C/N/P ratios of algae C/N/P ratios of algae were determined as follows. Algae were harvested during 1996±1998. Algae were dried in an oven at 60 °C, and then subsampled 20 times. The bulk dried algae were ground to a ®ne powder. Subsets of the algae were analyzed for organic C by weight loss at 450 °C for 2 h and inorganic C by weight loss at 1,100 °C. Organic C and N were also analyzed in a CHN analyzer (Perkin-Elmer). The subset of the sample which was combusted at 450 °C was also extracted in 10% HCL and then analyzed colorimetrically (Technicon II molybdate complex, ascorbic acid reduction) for PO4. Measurements of water velocity Water velocities were measured at 20 dierent locations, evenly spaced (grid 5´4) during July 1999 and January 2000. A timedpulsed acoustic current meter (MAVS, made by NOBSCA, Woods Hole) was mounted at each location for 4 min, recording a 2-min record of the water velocity. Water velocities were averaged and reported as a mean. The resulting data showed a signi®cant positive correlation (p>0.05 mmol m±3). Tropical oceans usually have concentrations of NH4 and NO3 1)2 times that of PO4. Further, SiO3 was the only inorganic nutrient which increased throughout the 6-year period (Table 1). All inorganic nutrients, except SiO3, were high initially and dropped during 1996 (Fig. 2). Before October 1995, water which was evaporated from the ocean was added back using condensation water created from the groundwater of the wilderness biome, termed wilderness condensate water. This water was very high in nutrients, creating spikes of nutrients when added (Atkinson et al. 1999). Since 1996 nutrient concentrations steadily dropped, leveling o and oscillating near the present-day concentrations. It is not known why SiO3 increases in the biome, but it could be from a slow release from the underlying clays (Atkinson et al. 1999), particularly with increased remineralization of organic material within interstitial spaces reducing pH. Table 1 Means, 95% con®dence limits (in parenthesis) and regression slopes for Biosphere nutrient data from January 1995 to September 2000. NS Not signi®cantly dierent from zero. * Regression slope signi®cantly dierent than zero at p
