RACER: Sinking rates and vertical flux of phytoplankton pigments
RACER: Sinking rates and vertical flux of phytoplankton pigments JAMES P. SZYPER
Hawaii Institute of Marine Biology School of Ocean and Earth Science and Technology University of Hawaii P.O. Box 1346 Kaneohe, Hawaii 96744
DAVID M. KARL
School of Ocean and Earth Science and Technology University of Hawaii Honolulu, Hawaii 96822
Sinking is an important process in the dynamics of oceanic seston, particularly at high latitudes. Estimates of downward rates of particle flux contribute to analyses of nutrient sources supporting primary production and the fates of the material produced (Smith et al. 1986; Karl et al. 1988; Laws etal. 1988; Karl and Asper 1990; Karl et al. 1991; Nordhausen and Huntley 1990; Vernet and Karl 1990; Bienfang and Ziemann 1992). Sinking and material flux rates are estimated by two basic strategies. Particles are collected in traps deployed at selected depths for a period of one to several days, yielding flux rates in typical units (for pigments) of milligrams per square meter per day. Alternatively, sinking rates of particles in water samples (meters per day) may be determined by the SETCOL method (Bienfang 1981), and flux rates derived as products of sinking rates and ambient concentrations (milligrams per cubic meter). The trap method integrates processes over depth and time, while SETCOL analyses are closer to "point" estimates from discrete depths during short periods (2 to 6 hours). SETCOL analyses exclude relatively rare particles such as fecal pellets because they are not caught frequently (due either to abundance or to sampling efficiency) in the water samplers from which experimental water is taken. We employed both methods at a station in the northern Gerlache Strait during the Research on Antarctic Coastal Ecosystem Rates 3 (RACER3) cruise in December 1991. Sinking and flux rates are analyzed here in terms of chlorophyll a and phaeopigments that were determined fluorometrically aboard ship (Holm-Hansen and Riemann 1978). Other particulate materials (adenosine triphosphate, carbon, nitrogen, and silicon) were sampled during these experiments, but analyses were incomplete at this publication date. SETCOL incubations were performed in duplicate using an array of 12 clear acrylic columns 0.5 meters in height and 400 milliliters incapacity, contained in a clear water jacket filled with surface seawater suspended in shade on deck for periods of 3.5 to 5.5 hours. Columns were filled with seawater collected from various depths (0 to 75 meters) with a bucket or Niskin samplers. Sinking rates were calculated from the distribution of pigments among upper, middle, and bottom regions of the columns after incubation. Free-floating MULTITRAP arrays (Karl et al. 1991) were deployed at 20-meter depth intervals from 40 to 140 meters during each of three occupations of this station (station A) during
168
December 1991; the deployment periods were of 32-,27-, and 41'_ hour duration. Pigment analyses were performed on subsamples of high-density trap solutions (1.5 molar sodium chloride) lackting preservatives. SETCOL- derived sinking rates ranged from 0.19 to 0.72 meter per day for chlorophyll and from 0.18 to 0.96 meters per day for phaeopigments. The overall mean rates for the two materials were 0.51 and 0.55 meters per day, respectively, which did not differ significantly at a = 0.05. The vertical pattern in sinking rates (figure 1) was similar to the temperature profiles, which in general showed little or no mixed layer, approximately linear decrease in temperature to about 50 meters, and isothermal conditions at greater depth. Flux rates calculated independently from SETCOL and MULTITRAP experiments are shown in figure 2. Surface flux rates of chlorophyll a were relatively high, being products of reasonably high sinking rates (Bienfang 1984; Culver and Smith 1989) and high pigment concentrations (5 to 10 milligrams per cubic meter) in the upper 20 meters. Below 20 meters, both SETCOL and MULTITRAP-derived flux rates indicate an ap-
TEMPERATURE °C
20 ci 40
DEPTH 11 M 60 J.
80
NO
e
100
0.5 1.0
SINKING RATE m d1 Figure 1. SETCOL-determined sinking rates of particulate chlorophyll a (filled symbols) and phaeoplgments (open symbols) at station A during MULTITRAP deployments on 12 December (triangles), 19 December (squares), and 25 December (circles) 1991. Each point represents the mean rate derived from duplicate column incubations. Temperature profiles from the four hydrocasts providing experimental water are shown as dotted lines.
ANTARCTIC JOURNAL.
FLUX Mg M-2 day 0
1
0
Phaeopigments/Chlorophyll a
2 3 0
I • I
0
2
4
I •
p.
50
50 EDO
DEPTH
DEPTH M
M
100
CD D
100
a> Figure 2. Vertical flux rates of particulate chlorophyll aas determined by SETCOL experiments (filled symbols) and by MULTITRAP collections (open symbols). Dates are represented by different symbols (as In figure 1).
proximate order of magnitude decrease to relatively constant rates in the remainder of the depth range studied (40 to 140 meters). Phaeopigment flux rates (not shown) were lower than chlorophyll rates near the surface (due to lower concentrations), but greater below the photiczone. Downward flux rates of chlorophyll a and phaeopigments ranged from 0.04 to 2.88, and 0.03 to 2.83 milligrams per square meters per day, respectively, taking both methods together. These ranges, obtained after the peak of the 1991 bloom period, overlap with, but are generally lower than, those observed at station A in November 1989 during the spring bloom (Vernet and Karl 1990). Phaeopigment flux in relative importance with depth, gained as shown by the increasing ratio of phaeopigment flux/chlorophyll a flux rates (figure 3). This trend continued smoothly through the transition from SETCOL to MULTITRAP-derived flux rates at 30 to 40 meters. A similar depth-related increase was evident in the ratio of phaeopigment/chlorophyll a concentrations (P/C) in the suspended particulates collected by the Niskin samplers. Although traps make direct assessments of flux rates, these, like SETCOL-derived rates, may be considered products of sinking rates and concentrations. Pigment concentrations were relatively low below 50 meters (less than 0.4 milligrams per cubic meter) and did not increase withdepth. Thus, larger phaeopigment flux rates below 50 meters imply rapid sinking rates of tens of meters per day, which are characteristic of fecal pellets or large organic aggregates. Few pellets were seen on filters collecting trap material from 40 and 60 meters, but increasing numbers
1992 REVIEW
Figure 3. Ratios of particulate phaeopigments to chlorophyll sin the water column (dotted lines) and in vertical flux rates, as determined by SETCOL experiments (filled symbols) and by MULTITRAP collection (open symbols). Dates are represented by different symbols (as In figure 1). appeared with increasing depth. The influence of pellets on flux rates is illustrated by the discrepancy between the phaeopigment contribution to the SETCOL rate at 75 meters (which has no fecal pellet component) and to the MULTITRAP rate at 80 meters (open and closed circles in figure 3) on the same date. The two methods address the same natural process, but the characteristic exclusion of large particles from SETCOL experiments can be exploited to quantify the separate contribution of such particles to total vertical flux. We thank the RACER Project S-046 personnel (G. Tien, J. Burgett, J . Dore, R. Letelier, and G. Parrish) for their help in sample collection and analysis, A. Amos for providing the CTD data, and 0. Holm-Hansen for water column pigment measurements. This research was supported by National Science Foundation grant DPP 88-18899, awarded to D. Karl. SOEST Contribution No. 3127. References Bienfang, P. K. 1981. SETCOL—a technologically simple and reliable method for measuring phytoplankton sinking rates. Canadian Journal
of Fisheries and Aquatic Sciences, 38:1,289-1,294. Bienfang, P. K. 1984. Size structure and sedimentation of biogenic microparticulates in a subarctic ecosystem. Journal of Plankton Re-
search, 6:985-995.
Bienfang, P. K. and D. A. Ziemann. 1992. The role of coastal high latitude ecosystems in global export production. In P. G. Falkowski and
A. D. Woodhead (Eds.), Primary productivity and biogeochemical cycles in the sea. New York: Plenum Press, 285-297.
169
Culver, M. E. and W. 0. Smith. 1989. Effects of environmental variation on sinking rates of marine phytopl ankton. Journal of Phycology, 25:262-270. Karl, D. M., G. A. Knauer, and J . H. Martin. 1988. Downward flux of particulate organic matter in the ocean: A particle decomposition paradox. Nature, 332:438-441. Karl, D. M. and V. L. Asper. 1990. RACER: Particle flux measurements during the 1989-1990 austral summer. Antarctic Journal of the U.S., 25(5):167-169. Karl, D. M., B. D.Tilbrook, and G. Tien. 1991. Seasonal coupling of organic matter production and particle flux in the western Bransfield Strait, Antarctica. Deep-Sea Research, 38:1,097-1,126. Laws, E. A., P. K. Bienfang, D. A. Ziemann, and L. D. Conquest. 1988. Phytoplankton population dynamics and the fate of production du-
Exocellular enzyme activities in Gerlache Strait, Antarctica JAMES R. CHRISTIAN AND DAVID M. KARL
ring the spring bloom in Auke Bay, Alaska. Lim nology and Oceanogra-
phy, 33:57-65. Nordhausen, W. and M. E. Huntley. 1990. RACER: Carbon egestion rates of Euphausiasia superba. Antarctic Journal of the U.S., 25(5):161-162. Smith, S. V., W. J . Kimmerer, and T. W. Walsh. 1986. Vertical flux and biogeochemical turnover regulate nutrient limitation of net organic production in the North Pacific Gyre. Limnology and Oceanography, 31: 161-167. Smith, W. 0. 1987. Phytoplankton dynamics in marginal ice zones. In M. Barnes (Ed.), Oceanography and marine biology. 25(annual review): 11-38. Vernet, M. and D. M. Karl. 1990. RACER: Phytoplankton growth and zooplankton grazing in the northern Gerlache Strait estimated from chlorophyll budgets. Antarctic Journal of the U.S., 25(5):164-166.
points, see figure la, are removed r2 = 0.695). In fast grid C (27 to 30 December) there is no correlation at all (r 2= 0.156). Weak correlations beween BGase and LAPase suggest that enzyme activities are not a simple function of bacterial biomass. Our results from Hawaiian waters also show that while there is a positive correlation of enzyme activity with biomass, activity per unit biomass is highly variable.
School of Ocean and Earth Science and Technology University of Hawaii Honolulu, Hawaii 96822
Most dissolved organic matter (DOM) in seawater consists of polymeric substances that must be hydrolyzed by exocellular enzymes before being assimilated by microorganisms. Techniques for measuring enzyme activities using fluorescent substrate analogs have been in use for several decades but have only recently been applied to marine plankton, and never, to our knowledge, in Antarctica. During the 1991-1992 austral summer the Research on Antarctic Coastal Ecosystem Rates (RACER) cruise, activities of bacterial exocellular enzymes beta-glucosidase (BGase) and leucine aminopeptidase (LAPase) were measured in the Gerlache Strait. Two fast grids (30 to 40 stations sampled over approximately 72 hours) of surface water samples were taken, and four depth profiles (0 to 200 meters) at station A (64117S 61'19.5' W). Because these experiments are conducted at saturating substrate concentration (Hoppe 1983) and the concentration of substrate in situ is not known, these results must be considered indices of potential activity rather than estimates of actual activities in situ. Enzyme activities are expressed as nanomoles of substrate analog (methylumbelliferyl-beta-glucoside orL-leucylbeta-naphthylamine) hydrolyzed per liter per day at saturating substrate concentration. It has been suggested that such potential activity measurements are an index of bacterial biomass rather than growth or activity (Billen et al. 1990). If this is correct, then the potential activities of the two enzymes should be strongly positively correlated. However, an important result of this work is that the activities of these two enzymes are uncoupled in space or time, or both. Across two fast grids of surface samples there is little correlation between the activities of the two enzymes (figure 1). In fast grid B (22 to 25 December) there is only a weak positive correlation between the two (r2 = 0.264, but if the three outlier
170
6
.3) C,) CZ
(D co
2
1000
LAPase
2000
3000
Fast C/)
0
.
U •
•
•
U .. • U. • •. U 0 U. U
0
U U •U
1000
2000
LAPase Figure 1. Relationship between the activities of beta-glucosldase (BGase) and leucine aminopeptidase (LAPase) on (top) fast grid B (22 to 25 December 1991)and (bottom)fast grid C(27to 30 December 1991). Activities are in nanomoles per liter per day.
ANTARCTIC JOURNAL
Hawaii Institute of Marine Biology School of Ocean and Earth Science and Technology University of Hawaii P.O. Box 1346 Kaneohe, Hawaii 96744
DAVID M. KARL
School of Ocean and Earth Science and Technology University of Hawaii Honolulu, Hawaii 96822
Sinking is an important process in the dynamics of oceanic seston, particularly at high latitudes. Estimates of downward rates of particle flux contribute to analyses of nutrient sources supporting primary production and the fates of the material produced (Smith et al. 1986; Karl et al. 1988; Laws etal. 1988; Karl and Asper 1990; Karl et al. 1991; Nordhausen and Huntley 1990; Vernet and Karl 1990; Bienfang and Ziemann 1992). Sinking and material flux rates are estimated by two basic strategies. Particles are collected in traps deployed at selected depths for a period of one to several days, yielding flux rates in typical units (for pigments) of milligrams per square meter per day. Alternatively, sinking rates of particles in water samples (meters per day) may be determined by the SETCOL method (Bienfang 1981), and flux rates derived as products of sinking rates and ambient concentrations (milligrams per cubic meter). The trap method integrates processes over depth and time, while SETCOL analyses are closer to "point" estimates from discrete depths during short periods (2 to 6 hours). SETCOL analyses exclude relatively rare particles such as fecal pellets because they are not caught frequently (due either to abundance or to sampling efficiency) in the water samplers from which experimental water is taken. We employed both methods at a station in the northern Gerlache Strait during the Research on Antarctic Coastal Ecosystem Rates 3 (RACER3) cruise in December 1991. Sinking and flux rates are analyzed here in terms of chlorophyll a and phaeopigments that were determined fluorometrically aboard ship (Holm-Hansen and Riemann 1978). Other particulate materials (adenosine triphosphate, carbon, nitrogen, and silicon) were sampled during these experiments, but analyses were incomplete at this publication date. SETCOL incubations were performed in duplicate using an array of 12 clear acrylic columns 0.5 meters in height and 400 milliliters incapacity, contained in a clear water jacket filled with surface seawater suspended in shade on deck for periods of 3.5 to 5.5 hours. Columns were filled with seawater collected from various depths (0 to 75 meters) with a bucket or Niskin samplers. Sinking rates were calculated from the distribution of pigments among upper, middle, and bottom regions of the columns after incubation. Free-floating MULTITRAP arrays (Karl et al. 1991) were deployed at 20-meter depth intervals from 40 to 140 meters during each of three occupations of this station (station A) during
168
December 1991; the deployment periods were of 32-,27-, and 41'_ hour duration. Pigment analyses were performed on subsamples of high-density trap solutions (1.5 molar sodium chloride) lackting preservatives. SETCOL- derived sinking rates ranged from 0.19 to 0.72 meter per day for chlorophyll and from 0.18 to 0.96 meters per day for phaeopigments. The overall mean rates for the two materials were 0.51 and 0.55 meters per day, respectively, which did not differ significantly at a = 0.05. The vertical pattern in sinking rates (figure 1) was similar to the temperature profiles, which in general showed little or no mixed layer, approximately linear decrease in temperature to about 50 meters, and isothermal conditions at greater depth. Flux rates calculated independently from SETCOL and MULTITRAP experiments are shown in figure 2. Surface flux rates of chlorophyll a were relatively high, being products of reasonably high sinking rates (Bienfang 1984; Culver and Smith 1989) and high pigment concentrations (5 to 10 milligrams per cubic meter) in the upper 20 meters. Below 20 meters, both SETCOL and MULTITRAP-derived flux rates indicate an ap-
TEMPERATURE °C
20 ci 40
DEPTH 11 M 60 J.
80
NO
e
100
0.5 1.0
SINKING RATE m d1 Figure 1. SETCOL-determined sinking rates of particulate chlorophyll a (filled symbols) and phaeoplgments (open symbols) at station A during MULTITRAP deployments on 12 December (triangles), 19 December (squares), and 25 December (circles) 1991. Each point represents the mean rate derived from duplicate column incubations. Temperature profiles from the four hydrocasts providing experimental water are shown as dotted lines.
ANTARCTIC JOURNAL.
FLUX Mg M-2 day 0
1
0
Phaeopigments/Chlorophyll a
2 3 0
I • I
0
2
4
I •
p.
50
50 EDO
DEPTH
DEPTH M
M
100
CD D
100
a> Figure 2. Vertical flux rates of particulate chlorophyll aas determined by SETCOL experiments (filled symbols) and by MULTITRAP collections (open symbols). Dates are represented by different symbols (as In figure 1).
proximate order of magnitude decrease to relatively constant rates in the remainder of the depth range studied (40 to 140 meters). Phaeopigment flux rates (not shown) were lower than chlorophyll rates near the surface (due to lower concentrations), but greater below the photiczone. Downward flux rates of chlorophyll a and phaeopigments ranged from 0.04 to 2.88, and 0.03 to 2.83 milligrams per square meters per day, respectively, taking both methods together. These ranges, obtained after the peak of the 1991 bloom period, overlap with, but are generally lower than, those observed at station A in November 1989 during the spring bloom (Vernet and Karl 1990). Phaeopigment flux in relative importance with depth, gained as shown by the increasing ratio of phaeopigment flux/chlorophyll a flux rates (figure 3). This trend continued smoothly through the transition from SETCOL to MULTITRAP-derived flux rates at 30 to 40 meters. A similar depth-related increase was evident in the ratio of phaeopigment/chlorophyll a concentrations (P/C) in the suspended particulates collected by the Niskin samplers. Although traps make direct assessments of flux rates, these, like SETCOL-derived rates, may be considered products of sinking rates and concentrations. Pigment concentrations were relatively low below 50 meters (less than 0.4 milligrams per cubic meter) and did not increase withdepth. Thus, larger phaeopigment flux rates below 50 meters imply rapid sinking rates of tens of meters per day, which are characteristic of fecal pellets or large organic aggregates. Few pellets were seen on filters collecting trap material from 40 and 60 meters, but increasing numbers
1992 REVIEW
Figure 3. Ratios of particulate phaeopigments to chlorophyll sin the water column (dotted lines) and in vertical flux rates, as determined by SETCOL experiments (filled symbols) and by MULTITRAP collection (open symbols). Dates are represented by different symbols (as In figure 1). appeared with increasing depth. The influence of pellets on flux rates is illustrated by the discrepancy between the phaeopigment contribution to the SETCOL rate at 75 meters (which has no fecal pellet component) and to the MULTITRAP rate at 80 meters (open and closed circles in figure 3) on the same date. The two methods address the same natural process, but the characteristic exclusion of large particles from SETCOL experiments can be exploited to quantify the separate contribution of such particles to total vertical flux. We thank the RACER Project S-046 personnel (G. Tien, J. Burgett, J . Dore, R. Letelier, and G. Parrish) for their help in sample collection and analysis, A. Amos for providing the CTD data, and 0. Holm-Hansen for water column pigment measurements. This research was supported by National Science Foundation grant DPP 88-18899, awarded to D. Karl. SOEST Contribution No. 3127. References Bienfang, P. K. 1981. SETCOL—a technologically simple and reliable method for measuring phytoplankton sinking rates. Canadian Journal
of Fisheries and Aquatic Sciences, 38:1,289-1,294. Bienfang, P. K. 1984. Size structure and sedimentation of biogenic microparticulates in a subarctic ecosystem. Journal of Plankton Re-
search, 6:985-995.
Bienfang, P. K. and D. A. Ziemann. 1992. The role of coastal high latitude ecosystems in global export production. In P. G. Falkowski and
A. D. Woodhead (Eds.), Primary productivity and biogeochemical cycles in the sea. New York: Plenum Press, 285-297.
169
Culver, M. E. and W. 0. Smith. 1989. Effects of environmental variation on sinking rates of marine phytopl ankton. Journal of Phycology, 25:262-270. Karl, D. M., G. A. Knauer, and J . H. Martin. 1988. Downward flux of particulate organic matter in the ocean: A particle decomposition paradox. Nature, 332:438-441. Karl, D. M. and V. L. Asper. 1990. RACER: Particle flux measurements during the 1989-1990 austral summer. Antarctic Journal of the U.S., 25(5):167-169. Karl, D. M., B. D.Tilbrook, and G. Tien. 1991. Seasonal coupling of organic matter production and particle flux in the western Bransfield Strait, Antarctica. Deep-Sea Research, 38:1,097-1,126. Laws, E. A., P. K. Bienfang, D. A. Ziemann, and L. D. Conquest. 1988. Phytoplankton population dynamics and the fate of production du-
Exocellular enzyme activities in Gerlache Strait, Antarctica JAMES R. CHRISTIAN AND DAVID M. KARL
ring the spring bloom in Auke Bay, Alaska. Lim nology and Oceanogra-
phy, 33:57-65. Nordhausen, W. and M. E. Huntley. 1990. RACER: Carbon egestion rates of Euphausiasia superba. Antarctic Journal of the U.S., 25(5):161-162. Smith, S. V., W. J . Kimmerer, and T. W. Walsh. 1986. Vertical flux and biogeochemical turnover regulate nutrient limitation of net organic production in the North Pacific Gyre. Limnology and Oceanography, 31: 161-167. Smith, W. 0. 1987. Phytoplankton dynamics in marginal ice zones. In M. Barnes (Ed.), Oceanography and marine biology. 25(annual review): 11-38. Vernet, M. and D. M. Karl. 1990. RACER: Phytoplankton growth and zooplankton grazing in the northern Gerlache Strait estimated from chlorophyll budgets. Antarctic Journal of the U.S., 25(5):164-166.
points, see figure la, are removed r2 = 0.695). In fast grid C (27 to 30 December) there is no correlation at all (r 2= 0.156). Weak correlations beween BGase and LAPase suggest that enzyme activities are not a simple function of bacterial biomass. Our results from Hawaiian waters also show that while there is a positive correlation of enzyme activity with biomass, activity per unit biomass is highly variable.
School of Ocean and Earth Science and Technology University of Hawaii Honolulu, Hawaii 96822
Most dissolved organic matter (DOM) in seawater consists of polymeric substances that must be hydrolyzed by exocellular enzymes before being assimilated by microorganisms. Techniques for measuring enzyme activities using fluorescent substrate analogs have been in use for several decades but have only recently been applied to marine plankton, and never, to our knowledge, in Antarctica. During the 1991-1992 austral summer the Research on Antarctic Coastal Ecosystem Rates (RACER) cruise, activities of bacterial exocellular enzymes beta-glucosidase (BGase) and leucine aminopeptidase (LAPase) were measured in the Gerlache Strait. Two fast grids (30 to 40 stations sampled over approximately 72 hours) of surface water samples were taken, and four depth profiles (0 to 200 meters) at station A (64117S 61'19.5' W). Because these experiments are conducted at saturating substrate concentration (Hoppe 1983) and the concentration of substrate in situ is not known, these results must be considered indices of potential activity rather than estimates of actual activities in situ. Enzyme activities are expressed as nanomoles of substrate analog (methylumbelliferyl-beta-glucoside orL-leucylbeta-naphthylamine) hydrolyzed per liter per day at saturating substrate concentration. It has been suggested that such potential activity measurements are an index of bacterial biomass rather than growth or activity (Billen et al. 1990). If this is correct, then the potential activities of the two enzymes should be strongly positively correlated. However, an important result of this work is that the activities of these two enzymes are uncoupled in space or time, or both. Across two fast grids of surface samples there is little correlation between the activities of the two enzymes (figure 1). In fast grid B (22 to 25 December) there is only a weak positive correlation between the two (r2 = 0.264, but if the three outlier
170
6
.3) C,) CZ
(D co
2
1000
LAPase
2000
3000
Fast C/)
0
.
U •
•
•
U .. • U. • •. U 0 U. U
0
U U •U
1000
2000
LAPase Figure 1. Relationship between the activities of beta-glucosldase (BGase) and leucine aminopeptidase (LAPase) on (top) fast grid B (22 to 25 December 1991)and (bottom)fast grid C(27to 30 December 1991). Activities are in nanomoles per liter per day.
ANTARCTIC JOURNAL
