Particulate organic matter decomposition in the water column of Lake ...
perennially ice-covered lake in Antarctica. (Antarctic Research Series) Washington, D.C.: American Geophysical Union. 20:51-68. Lizotte, M. P. and J. C. Priscu. 1992. Photosynthesis-irradiance relationships in phytoplankton from the physically stable water column of a perennially ice-covered lake (Lake Bonney, Antarctica). Journal of Phycology, 28:179-185.
Lizotte, M. P. and J . C. Priscu. 1991. Natural fluorescence and photosynthetic quantum yields in vertically stable phytoplankton from perennially ice-covered lakes (dry valleys). Antarctic Journal of the U. S., in press. Neale, P. J. and J. C. Priscu. 1991. Variation of the fluorescence quantum yield in relation to photosynthesis by phytoplankton from perennially ice-covered Lake Bonney. Antarctic Journal of the U.S., 26(5):228-230. Parker, B. C., G. M. Simmons Jr., K. G. Seaburg, D. D. Cathey, and F.T.C.
Particulate organic matter decomposition in the water column of Lake Bonney, Taylor Valley, Antarctica
AlInut. 1982. Comparative ecology of plankton communities in seven antarctic oasis lakes. Journal of Plankton Research, 4:271-286. Priscu, J . C. 1992. Particulate organic matter decomposition in the water column of Lake Bonney, Taylor Valley. Antarctic Journal of the U.S., this issue. Sharp, T. R. and J. C. Priscu. 1992. Temporal variations of phytoplanktonspecific growth and loss rates in Lake Bonney, Antarctica. Antarctic Journal of the U.S., this issue. Spigel, R. H., I. Forne, I. Sheppard, and J . C. Priscu. 1992. Difference in temperature and conductivity between east and west lobes of Lake Bonney: Evidence for circulation within and between lobes. Antarctic Journal of the U.S., 26(5):221-222.
productivity and chlorophyll profiles, are presented in figure 1. Decomposition rates were always highest just beneath the permanent ice cap and declined with depth in the trophogenic zone (zone where primary productivity occurs; just beneath the ice to about 20 meters). Average decomposition rates within the
JOHN C. PRiscu
DECOMPOSITION PRODUCTIVITY; CHLOROPHYLL 0.04 0.08 0 1.0 2.0
Department of Biological Sciences Montana State University Bozeman, Montana 59717
Phytoplankton biomass within the dry valley lakes adjacent to McMurdo Sound is surprisingly high despite photosynthetic rates that are light-limited (Priscu et al. 1987; Priscu 1989; Lizotte and Priscu 1992). Presumably, the accumulation of phytoplankton biomass in these systems is the result of low loss rates. Losses to grazing are minimal owing to the virtual lack of crustaceous zooplankton and phytoplankton sinking is also assumed to be low because most of the species in the lakes are flagellated and thus capable of maintaining themselves at specific depths (Priscu et al. 1990b; Lizotte and Priscu 1992a,b). Because grazing and sinking losses are potentially low in these systems, I conducted experiments to determine if bacterial decomposition of phytoplankton may be a significant sink for phytoplankton organic matter. Potential decomposition rates of phytoplankton in the east lobe of Lake Bonney were determined by measuring the rate of 14CO2 released from phytoplankton labeled with carbon-14. Equilibrium labeling was obtained by incubating phytoplankton collected immediately under the ice cap with saturating light (approximately 100 micromoles of quanta per meter squared per second) for up to 4 days with NaH 14CO3. Equillibrium labeling of the major photosynthetic end-products has been shown to occur within 24 hours (Priscu et al. 1987). A known amount (in terms of activity and biomass) of labeled phytoplankton was concentrated onto Whatman CF/C glass-fiber filters, which were air-dried then suspended in gas-tight vials containing 10 milliliters of lake water from selected depths. 14 2 released via decomposition of phytoplankton was trapped on an ethanolamine-saturated glassfiber filter placed within each vial. Parallel samples treated with 5 percent formalin (final concentration) were used to correct for 4CO2 release unrelated to decomposition. Results from decomposition experiments conducted in 1990 and 1991, along with corresponding phytoplankton primary
260
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Figure 1. Profiles of decomposition rates (percent per day), primary productivity (micrograms carbon per liter per day), and chlorophyll (micrograms per liter) on 12 November 1990 and 10 October 1991 in the east lobe of Lake Bonney. The horizontal lines below the date denote the bottom of the ice.
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Figure 2. Profiles of bacterial activity (0.0001 nanomolar thymidine incorporation per hour) and bacterial biomass (micrograms carbon per liter) in the east lobe of Lake Bonney. The horizontal lines below the dates denote the bottom of the ice.
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0.05 z 0.04 0 F0.03 0 0 0.02 U UI o 0.01
0-04.5m (10 OCT 1991) 0-020m (26 SEP 1991)
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CHLOROPHYLL Figure 3. Decomposition rate (percent per day) as a function of chlorophyll a concentration (micrograms per liter) for water samples from the east lobe of Lake Bonney.
trophogenic zone were 0.056 and 0.008 percent per day for the 1990 and 1991 experimental dates, respectively (average 0.032). Data from phytoplankton photosynthesis measured over the spring and summer at Lake Bonney revealed an average increase in phytoplankton carbon of about three percent per day (J . C. Priscu, unpublished data). Hence, potential losses of phytoplank ton from bacterial decomposition are several orders of magnitude lower than phytoplankton growth, a result confirmed using models for phytoplankton growth and loss (Sharp and Priscu 1992; Sharp 1992). Decomposition was never measurable below the trophogenic zone (25 meters), which corresponds with a low or undetectable level of heterotrophic bacterial activity (tritium-thymidine incorporation) at 25 meters (figure 2). Interestingly, bacterial biomass was relatively high at 25 meters despite low thymidine incorporation. Collectively these results imply that bacteria below the trophogenic zone are inactive with respect to particulate organic matter decomposition and thymidine incorporation. Various inorganic nitrogen signatures below the trophogenic zone (Sharp and Priscu 1990; J. C. Priscu unpublished data) suggest that high bacterial biomass in this region may be due to chemoautotrophic nitrifying bacteria, which do not incorporate thymidine or oxidize organic carbon (Priscu et al. 1990a). The lack of phytoplankton decomposition below the trophogenic zone may explain the persistence of a chlorophyll peak in these aphotic waters (figure 1). To assess the kinetic response of decomposition in the upper and lower trophogenic zone, decomposition rates were measured over a range of phytoplankton concentrations (figure 3). These experiments showed that bacterial decomposition activity at 4.5 meters generally increased with increasing phytoplankton biomass, whereas bacterial decomposition activity at 20 meters did not respond to additional phytoplankton biomass. Perhaps
262
the exoenzymes required to hydrolyze particulate organic matter could not be induced in bacteria at 20 meters or perhaps deepwater bacteria in Lake Bonney are acclimated to using the large pool of dissolved organic carbon that exists at and below 20 meters U. C. Priscu unpublished data). Bacterial enzymes may have also been saturated below the lowest level of phytoplankton used in the experiment. Despite lack of clear biochemical explanations at this time, data obtained thus far support the following conclusions: • Phytoplankton decomposition rates (and loss rates in general) are extremely low relative to phytoplankton production rates. • Heterotrophic bacterial activity below the trophic zone is extremely low (and may be absent). • Bacteria below the chemocline may be dominated by chemoautotophs (e.g., nitrifying bacteria). I thank Tom Sharp, Michael Lizotte, Joseph Rudek, and Patrick Neale for their assistance in the field. This work was supported in part by National Science Foundation grant DPP 8820591.
References Lizotte, M. P. and J. C. Priscu. 1992a. Photosynthesis-irradiance relation ships in phytoplankton from the physically stable water column of a perennially ice-covered lake. Journal of Phycology, 28:179-185. Lizotte, M. P. and J . C. Priscu. 1992b. Algal pigments as markers for stratified phytoplankton populations in Lake Bonney (dry valleys). Antarctic Journal of the U.S., this issue. Priscu,J. C., L. R. Priscu, V. F. Warwick, and C. Howard-Williams. 1987. A photosynthate distribution by microphytoplankton in permanently ice-covered antarctic desert lakes. Limnology and Oceanography, 23(1):260-270. Priscu,J. C. 1989. Photon dependence of inorganic nitrogen transport by phytoplankton in antarctic lakes. In W. F. Vincent and E. Ellis-Evans (Eds.), High Latitude Limnology. Hydrobiologia, 172. Klewer Press. 173-182. Priscu, J . C., M. T. Downes, L. R. Priscu, A. C. Palmisano, and C. W. Sullivan. 1990a. Dynamics of ammonium oxidizer activity and nitrous oxide (N20) within and beneath antarctic sea ice. Marine Ecology Progress Series, 62:37-46. Priscu, J . C., T. R. Sharp, M. P. Lizotte, and P. J . Neale. 1990b. Photoadaptation by phytoplankton in permanently ice-covered antarctic lakes: Response to a nonturbulent environment. Antarctic Journal of the U.S., 25:221-222. Sharp, T. R. and J. C. Priscu. 1991. Ambient nutrient levels and the effects of nutrient enrichment on primary productivity in Lake Bonney. Antarctic Journal of the U.S., 25(5):226-227. Sharp, T. R. 1992. Phytoplankton ecology in Lake Bonney, Antarctica: Emphasizing temporal variation of growth and loss rates. M.S. Thesis, Montana State University. Sharp, T. R. and J . C. Priscu. 1991. Rates of production and growth for phytoplankton in Lake Bonney. Antarctic Journal of the U.S., 26(5):225. Sharp, T. R. and J. C. Priscu. 1992. Temporal variation of phytoplanktonspecific growth and loss rates in Lake Bonney, Antarctica. Antarctic Journal of the U.S., this issue.
ANTARCTIC JOURNAL
Lizotte, M. P. and J . C. Priscu. 1991. Natural fluorescence and photosynthetic quantum yields in vertically stable phytoplankton from perennially ice-covered lakes (dry valleys). Antarctic Journal of the U. S., in press. Neale, P. J. and J. C. Priscu. 1991. Variation of the fluorescence quantum yield in relation to photosynthesis by phytoplankton from perennially ice-covered Lake Bonney. Antarctic Journal of the U.S., 26(5):228-230. Parker, B. C., G. M. Simmons Jr., K. G. Seaburg, D. D. Cathey, and F.T.C.
Particulate organic matter decomposition in the water column of Lake Bonney, Taylor Valley, Antarctica
AlInut. 1982. Comparative ecology of plankton communities in seven antarctic oasis lakes. Journal of Plankton Research, 4:271-286. Priscu, J . C. 1992. Particulate organic matter decomposition in the water column of Lake Bonney, Taylor Valley. Antarctic Journal of the U.S., this issue. Sharp, T. R. and J. C. Priscu. 1992. Temporal variations of phytoplanktonspecific growth and loss rates in Lake Bonney, Antarctica. Antarctic Journal of the U.S., this issue. Spigel, R. H., I. Forne, I. Sheppard, and J . C. Priscu. 1992. Difference in temperature and conductivity between east and west lobes of Lake Bonney: Evidence for circulation within and between lobes. Antarctic Journal of the U.S., 26(5):221-222.
productivity and chlorophyll profiles, are presented in figure 1. Decomposition rates were always highest just beneath the permanent ice cap and declined with depth in the trophogenic zone (zone where primary productivity occurs; just beneath the ice to about 20 meters). Average decomposition rates within the
JOHN C. PRiscu
DECOMPOSITION PRODUCTIVITY; CHLOROPHYLL 0.04 0.08 0 1.0 2.0
Department of Biological Sciences Montana State University Bozeman, Montana 59717
Phytoplankton biomass within the dry valley lakes adjacent to McMurdo Sound is surprisingly high despite photosynthetic rates that are light-limited (Priscu et al. 1987; Priscu 1989; Lizotte and Priscu 1992). Presumably, the accumulation of phytoplankton biomass in these systems is the result of low loss rates. Losses to grazing are minimal owing to the virtual lack of crustaceous zooplankton and phytoplankton sinking is also assumed to be low because most of the species in the lakes are flagellated and thus capable of maintaining themselves at specific depths (Priscu et al. 1990b; Lizotte and Priscu 1992a,b). Because grazing and sinking losses are potentially low in these systems, I conducted experiments to determine if bacterial decomposition of phytoplankton may be a significant sink for phytoplankton organic matter. Potential decomposition rates of phytoplankton in the east lobe of Lake Bonney were determined by measuring the rate of 14CO2 released from phytoplankton labeled with carbon-14. Equilibrium labeling was obtained by incubating phytoplankton collected immediately under the ice cap with saturating light (approximately 100 micromoles of quanta per meter squared per second) for up to 4 days with NaH 14CO3. Equillibrium labeling of the major photosynthetic end-products has been shown to occur within 24 hours (Priscu et al. 1987). A known amount (in terms of activity and biomass) of labeled phytoplankton was concentrated onto Whatman CF/C glass-fiber filters, which were air-dried then suspended in gas-tight vials containing 10 milliliters of lake water from selected depths. 14 2 released via decomposition of phytoplankton was trapped on an ethanolamine-saturated glassfiber filter placed within each vial. Parallel samples treated with 5 percent formalin (final concentration) were used to correct for 4CO2 release unrelated to decomposition. Results from decomposition experiments conducted in 1990 and 1991, along with corresponding phytoplankton primary
260
I I0 IJ
E I I.0 LiJ
Figure 1. Profiles of decomposition rates (percent per day), primary productivity (micrograms carbon per liter per day), and chlorophyll (micrograms per liter) on 12 November 1990 and 10 October 1991 in the east lobe of Lake Bonney. The horizontal lines below the date denote the bottom of the ice.
ANTARCTIC JOURNAL
THYMIDINE INCORPORATION 2 4 0 2 4 0 2 4 6
ILI
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50 100 150 200
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Figure 2. Profiles of bacterial activity (0.0001 nanomolar thymidine incorporation per hour) and bacterial biomass (micrograms carbon per liter) in the east lobe of Lake Bonney. The horizontal lines below the dates denote the bottom of the ice.
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261
0.05 z 0.04 0 F0.03 0 0 0.02 U UI o 0.01
0-04.5m (10 OCT 1991) 0-020m (26 SEP 1991)
0.00
0
0
20 40 60 80 100 120
CHLOROPHYLL Figure 3. Decomposition rate (percent per day) as a function of chlorophyll a concentration (micrograms per liter) for water samples from the east lobe of Lake Bonney.
trophogenic zone were 0.056 and 0.008 percent per day for the 1990 and 1991 experimental dates, respectively (average 0.032). Data from phytoplankton photosynthesis measured over the spring and summer at Lake Bonney revealed an average increase in phytoplankton carbon of about three percent per day (J . C. Priscu, unpublished data). Hence, potential losses of phytoplank ton from bacterial decomposition are several orders of magnitude lower than phytoplankton growth, a result confirmed using models for phytoplankton growth and loss (Sharp and Priscu 1992; Sharp 1992). Decomposition was never measurable below the trophogenic zone (25 meters), which corresponds with a low or undetectable level of heterotrophic bacterial activity (tritium-thymidine incorporation) at 25 meters (figure 2). Interestingly, bacterial biomass was relatively high at 25 meters despite low thymidine incorporation. Collectively these results imply that bacteria below the trophogenic zone are inactive with respect to particulate organic matter decomposition and thymidine incorporation. Various inorganic nitrogen signatures below the trophogenic zone (Sharp and Priscu 1990; J. C. Priscu unpublished data) suggest that high bacterial biomass in this region may be due to chemoautotrophic nitrifying bacteria, which do not incorporate thymidine or oxidize organic carbon (Priscu et al. 1990a). The lack of phytoplankton decomposition below the trophogenic zone may explain the persistence of a chlorophyll peak in these aphotic waters (figure 1). To assess the kinetic response of decomposition in the upper and lower trophogenic zone, decomposition rates were measured over a range of phytoplankton concentrations (figure 3). These experiments showed that bacterial decomposition activity at 4.5 meters generally increased with increasing phytoplankton biomass, whereas bacterial decomposition activity at 20 meters did not respond to additional phytoplankton biomass. Perhaps
262
the exoenzymes required to hydrolyze particulate organic matter could not be induced in bacteria at 20 meters or perhaps deepwater bacteria in Lake Bonney are acclimated to using the large pool of dissolved organic carbon that exists at and below 20 meters U. C. Priscu unpublished data). Bacterial enzymes may have also been saturated below the lowest level of phytoplankton used in the experiment. Despite lack of clear biochemical explanations at this time, data obtained thus far support the following conclusions: • Phytoplankton decomposition rates (and loss rates in general) are extremely low relative to phytoplankton production rates. • Heterotrophic bacterial activity below the trophic zone is extremely low (and may be absent). • Bacteria below the chemocline may be dominated by chemoautotophs (e.g., nitrifying bacteria). I thank Tom Sharp, Michael Lizotte, Joseph Rudek, and Patrick Neale for their assistance in the field. This work was supported in part by National Science Foundation grant DPP 8820591.
References Lizotte, M. P. and J. C. Priscu. 1992a. Photosynthesis-irradiance relation ships in phytoplankton from the physically stable water column of a perennially ice-covered lake. Journal of Phycology, 28:179-185. Lizotte, M. P. and J . C. Priscu. 1992b. Algal pigments as markers for stratified phytoplankton populations in Lake Bonney (dry valleys). Antarctic Journal of the U.S., this issue. Priscu,J. C., L. R. Priscu, V. F. Warwick, and C. Howard-Williams. 1987. A photosynthate distribution by microphytoplankton in permanently ice-covered antarctic desert lakes. Limnology and Oceanography, 23(1):260-270. Priscu,J. C. 1989. Photon dependence of inorganic nitrogen transport by phytoplankton in antarctic lakes. In W. F. Vincent and E. Ellis-Evans (Eds.), High Latitude Limnology. Hydrobiologia, 172. Klewer Press. 173-182. Priscu, J . C., M. T. Downes, L. R. Priscu, A. C. Palmisano, and C. W. Sullivan. 1990a. Dynamics of ammonium oxidizer activity and nitrous oxide (N20) within and beneath antarctic sea ice. Marine Ecology Progress Series, 62:37-46. Priscu, J . C., T. R. Sharp, M. P. Lizotte, and P. J . Neale. 1990b. Photoadaptation by phytoplankton in permanently ice-covered antarctic lakes: Response to a nonturbulent environment. Antarctic Journal of the U.S., 25:221-222. Sharp, T. R. and J. C. Priscu. 1991. Ambient nutrient levels and the effects of nutrient enrichment on primary productivity in Lake Bonney. Antarctic Journal of the U.S., 25(5):226-227. Sharp, T. R. 1992. Phytoplankton ecology in Lake Bonney, Antarctica: Emphasizing temporal variation of growth and loss rates. M.S. Thesis, Montana State University. Sharp, T. R. and J . C. Priscu. 1991. Rates of production and growth for phytoplankton in Lake Bonney. Antarctic Journal of the U.S., 26(5):225. Sharp, T. R. and J. C. Priscu. 1992. Temporal variation of phytoplanktonspecific growth and loss rates in Lake Bonney, Antarctica. Antarctic Journal of the U.S., this issue.
ANTARCTIC JOURNAL
