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Distribution of microbial biomass and secondary production in a warm-core Gulf Stream ring
Deep-Sea Research, Vol. 32, No. I 1, pp. 1393 to 14113. 1985. Printed in Grca! Britain.
019S-1{~19/S5 $3,{1~1+ {I.11~| ~ 1985 Pergamon I'rcss lad.
Distribution of microbial biomass and secondary production in a warm-core Gulf Stream ring E. R. PEELE,* R. E. MURRAY,*R. B. HANSON,tL. R. POMEROY$and R. E. HODSON* (Received 16 September 1984; in final revised form 17 June 1985; uccQ~ted 18 June 1985) Abstract--Microbial biomass, bacterial abundance and secondary production were examined in relation to the changing physicochemical conditions within warm-core Gulf Stream ring 81-F. Highest densities of bacterioplankton (6.14 x ll)8 cells I L) occurred at the ring margin in continental shelf and slope water entrained by the ring. Likewise, both total bacterial secondary production (measured as incorporation of [3H]thymidine into DNA) and pcr-cell bacterial secondary production were highcst at thc ring margin, avcraging 291. l pmoles I ~ d i and 4.95 x 10 7 pmoles cell i d t respectively. In contrast, high concentrations of ATP (mean, 1.45 lag I ~) and chlorophyll a (mean, 2.29 lag I ~) were found both at the periphery and near the center of the ring. A similar distribution pattern was found for the incorporation of [3H]adenine into microbial RNA. The elevated values for microbial biomass and activity at the ring margin may reflect the response of microbial populations to new conditions resulting from the juxtaposition of water masses comprising and surrounding the ring. Our results indicate that the distribution of microbial populations and the rates of microbial processes occurring within warm-core ring 81-F were influenced by the age of the ring and the extent of its interaction with continental shelf water, surrounding slope water and Gulf Stream meanders.
INTRODUCTION
DURING the last decade it has been demonstrated that Gulf Stream rings are important mesoscale features in the Sargasso Sea and in continental slope water regions of the northwestern Atlantic. Warm anticyclonic rings form from northward meanders of the Gulf Stream which enclose cores of water appropriated from the Sargasso Sea (WIEBE, 1982). These warm-core eddies are generally 100 to 200 km in diameter, elliptical in shape and extend downward to a depth of approximately 1500 m (SAUNDERS,1971; LAI and RICtlARDSON, 1977). The initial physical, chemical and biological properties of the ring core are characteristic of Sargasso Sea water. However, as the ring ages, the core may gradually acquire properties of neighboring slope or shelf water through diffusion and entrainment. Nutrient concentrations and primary productivity are generally lower in Sargasso Sea water than in slope w a t e r ( J o Y c E and WIEBE, 1983), and so with dispersion and increasing turbulence, rings primarily undergo nutrient enrichment (LAI and RICItARDSON, 1977). Interactions with westward-extending Gulf Stream meanders may also alter the ring structure (JoYcE et al., 1984). It is estimated that 5 to 9 warm-core rings form yearly, some persisting for 200 to 300 days before decaying or coalescing with the Gulf Stream (FITZGERALDand CttAMBERLtN, * Department of Microbiology and Institute of Ecology, University of Georgia, Athens, GA 31~~02, U.S.A. 5 Skidaway Institute of Oceanography, Savannah, G A 31406, U.S.A. $ Institute of Ecology, University of Georgia, Athens. GA 30602, U.S.A. 1393
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1981; CN.()NJ.:and Ih~lo.:, 1985). Thc duration of such rcgular mcsoscalc fcaturcs makcs them ideal sites for correlative studies of the relationships between plankton distribution and physicochemical properties of the water masses comprising the ring. Moreover, if the integrity of the component water masses is maintained after ring formation, warm-core eddies would be useful systems for examining the effects of fronts or water mass boundaries on plankton distribution and activity. Based on the characteristics of the component water masses with respect to nutrient concentrations and primary productivity, one might expect that microbial biomass and rates of bacterioplankton secondary production would be lower in the ring core "than in the surrounding slope water. The results of some recent studies of bacterial distribution in warm-core ring 82-B suggest that bacterial numbers are, as expected, higher in the frontal zones surrounding the ring (DucKLOW, 1984). The principal aim of this study then was to ascertain if spatial variations in bacterial abundance and production reflected differences in the contrasting properties of the water masses comprising another warm-core ring (81-F). Variability in microbial biomass and secondary production is discussed in rehttion to thc agc and evolution of ring 81-F, and the influence of interactions between the ring and surrounding slope water on either the size of microbial populations or rates of microbial processes is examined. MATERIALS
AND
METIIODS
Seawater samples were collected from a depth of 10 m in clean 5-I Niskin ® bottles at 7 stations along a northeast-southwest transect across warm-core ring 81-F. The ring, centered at 38°24'N, 72°24'W, was located approximately 250 km northeast of Maryland, U.S.A. (Fig. 1) and was sampled 31 March to 1 April 1982, about 4 months after its formation. Ring 81-F formed late in 1981 and coalesced with the Gulf Stream off Cape Hatteras, NC on 27 May 1982 (CELONE and PRICE, 1985). Sampling sites included 4 locations within the core water of Sargasso Sea origin and 2 stations at the ring margin in cold shelf water entrained by the ring (Table 1). Samples were also collected from N
i
i
4'5° .
40 ° Ne.w J e r s e y if/~ Warm-Core .~ '~ ~Ring 81-F
35 °.75 ° / ' ~
~,,- , 70 =
65 °
Fig. 1. Location of warm-core ring 8I-F (31 March to 1 April 1982).
Microbial biomass and secondary production in a Gulf Strcam ring
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"Fable I. Stations sampled along a transect across warm-core ring 81-F, 31 March to I April 1982
Station 8 9 10 II 12 13 14
Location 38°53'N, 38°47'N, 38°34'N, 38°24'N, 38°14'N, 38°04'N, 37°51'N,
71°40'W 71°56'W 72°13'W 72°24'W 72°51'W 73°08'W 73°33'W
continental slope water south of the ring to provide a reference with which to compare the ring observations. All samples were processed within 1 h of collection. Surface water temperatures wcrc monitored continuously across thc ring, and expendable bathythermographs (XBTs) were used to determine the vertical temperature structure. Salinity was determined by precision salinometer measurements of samples from Niskin bottles. Measurements of in vivo fluorescence of Chl a were made by means of flowthrough pumping of surface seawater through a Turner Designs fluorometer.
Bacterial enumeration The procedure for acridine orange direct counts was adapted from HouutE et al. (1977). Seawater samples were preserved with formaldehyde (final concentration, 2% v/v) and refrigerated at 5°C until counted. Appropriate aliquots of preserved samples were incubated 4 min with acridine orange (final concentration, 0.01%) and filtered through 0.2 ~m Nuclepore filters which had been previously stained with irgalan black (acid-black no. 107, Ciba-Geigy Corp., Greensboro, NC). Filters were placed on microscope slides, covered with low fluorescence immersion oil and examined under epifluorescent illumination with an Olympus BHS microscope. A minimum of 10 randomly selected fields with />50 cells per field was counted on each filter.
Incorporation of [3H]thymidine Rates of [3H]thymidine incorporation were determined by the method of FUURMANand AZAM (1980, 1982). Triplicate 20 ml samples of seawater were incubated in the dark at approximate in situ temperature for 3 h with 3.2 nM [methyl-3H]thymidine (77.2 Ci mmol -z, New England Nuclear Corp., Boston, MA). After incubation, samples were chilled in ice water, extracted in an equal volume of ice-cold 10% trichloroacetic acid (TCA) and filtered through 0.22 lam Millipore filters. Filters were rinsed twice with 3 ml of cold 5% TCA and then transferred to vials containing 10 ml of Scintiverse ® (Fisher Scientific Co., Fair Lawn, N J). Radioactivity was assayed by liquid scintillation spectrometry. Formalin-killed controls were used to measure abiotic adsorption of [3H]thymidine. FUIIRMANand AZAM (1980, 1982) used 5 nM [3H]thymidine in their determinations of bacterial secondary production in various aquatic environments. In this study, however, seawater samples were incubated with 3.2 nM thymidine. Thus, the rates of [3H]thymidine incorporation into cold TCA-insoluble material (primarily DNA) were underestimated by about 10 to 15%.
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The rate of [3H]thymidine incorporation into the <0.6 jam size fraction was determined separately. Seawater samples were gently prefiltered through 0.6 jam Nuclepore filters and triplicate 20 ml subsamples incubated for 3 h with [3H]thymidine. After incubation, cells were extracted in cold trichloroacetic acid and the TCA-insoluble material collected on 0.22 jam Millipore filters. Filters were then processed in a manner identical to that described above. Bacterial production rates were estimated from [3H]thymidine incorporation rates using a conversion factor of 2.4 x 106 cells produced per pmol of exogenous thymidine incorporated (FuIIRMANand AZAM,1982). This empirical factor, suggested for offshore water, is based on a mean value of 2.6 x 10-5 g DNA per cell (FuHRMANand AZAM, 1982) and has been corrected for approximately 20% non-DNA activity in the TCA-insoluble material. Incorporation of [3H]adenine Rates of [3H]adenine incorporation were determined by the method of KARL(1979). A 250 ml sample of seawater was incubated in the dark at in situ temperature for 1 h with 0.1 jaCi ml -l [2-3H]adenine (15.5 Ci mmol -l, New England Nuclear Corp., Boston, MA). After incubation, 3 x 50 ml subsamples were filtered through 0.2 jam Nuclepore filters and treated with either cold 5% trichloroacetic acid (TCA), 0.3 M NaOH or 5% TCA at about 100°C. Extracts were chilled and then filtered through 0.45 jam Millipore filters. Filters were rinsed 3 times with cold 5% TCA, placed in scintillation vials and dissolved in 0.2 ml of Soluene-350 ® before adding 15 ml of scintillation cocktail. Radioactivity was assayed by liquid scintillation spectrometry. TCA-killed controls were used to measure chemical adsorption of [3H]adenine to particles. Rates of [3H]adenine uptake by different size fractions were determined as follows. Seawater samples were incubated with [3H]adenine, and after the incubation period, 20 ml aliquots were filtered through 0.2 and 0.6 jam pore-size Nuclepore filters. The filters were rinsed 3 times with 0.2 jam filtered seawater and then extracted and processed as described above. The percentage of adenine uptake attributable to 0.6 jam filterable organisms was calculated as [(dpm on 0.2 jam filter- dpm on 0.6 lam filter)/dpm on 0.2 jam filter] x 100. A TP determination Total microbial biomass was measured as the concentration of cellular (particulate) adenosine triphosphate (ATP). Seawater samples were filtered through 0.22 jam Millipore filters, and the filters extracted with 5 ml of boiling sodium bicarbonate buffer (0.1 M, pH 8.5) for 2 min. Samples were then cooled, placed in scintillation vials with 5 ml of Tris (tris[hydroxymethyl]aminomethane) buffer (0.1 M, pH 7.8) and frozen for later analysis. Particulate ATP concentrations were determined by the luciferin-luciferase method of HOLM-HANsENand BOOTIt (1966). The fraction of microbial ATP associated with attached bacteria and larger microheterotrophs was determined by filtering seawater samples through 0.6 jam pore-size filters. Filters were extracted and samples analyzed by the procedures described above for total particulate ATP. The ATP associated with free-living bacteria was calculated as: [ATP]f = [ATP]o.2 -[ATP]o.6.
E.R. PEELEetal.
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(Fig. 3). High salinity water (approximately 36%0 at 16.0°C) appropriated from the Sargasso Sea was found at the ring center (Stas 9 and 1 l); however, the warm water was not contiguous across the ring core. Cooler (.,? = 13.9°C) less saline (.f = 35.5%o) water was found at Stas 10 and 12; the discontinuity is attributed largely to spiral intermixing of Gulf Stream, slope and shelf water. Outward from the core (Stas 8 and 13), there was an abrupt decrease in surface temperature and salinity. The low T-S values in water associated with the ring edge most likely were caused by entrainment of cold, low salinity shelf water around the ring. Surface temperature and salinity of continental slope water southsouthwest of the ring were 12.0°C and 35.0%0, respectively. As the position and fate of Gulf Stream rings are usually inferred from the distribution of temperature or salinity below a depth of 100 to 200 m, expendable bathythermographs were used to determine the vertical temperature structure. Vertical sections through 81-F clearly show a subsurface core of warm water, presumably of Sargasso Sea origin (Fig. 3).
Bacterial numbers Highest densities of bacterioplankton (6.14 x 108 cells l-l), determined by acridine orange direct counts, occurred at Stas 8 and 13 in shelf water entrained by the ring (Fig. 4). Bacterial numbers were typically lower in the ring core (remnant Sargasso Sea water), ranging from 5.46 x 108 cells 1-1 at Sta. 9 to 3.27 x 108 cells 1-~ at the ring center. In continental slope waters south of warm-core ring 81-F, bacterial abundance averaged 4.09 x 108 cells 1-~.
Thymidine incorporation Rates of [3H]thymidine incorporation into cold TCA-insoluble material were highest at the outer edge of warm-core ring 81-F, averaging 291.1 pmoles 1-I d -~ at 10 m depth (Fig. 4). In the core water of Sargasso Sea origin, incorporation rates of exogenous thymidine were much lower, ranging from 57.0 to 135.8 pmoles I-~ d -~. Although there was a slight increase in the rate of [SH]thymidine incorporation at the ring center (Sta. 11), incorporation rates in the warm core of ring 81-F were generally about 2.8 times lower than rates at
400
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126
O'7 ZOO ~ - - J
4
m
"r:
~v 100
2
Z I O
I
I
I
I
I
I
I
14
13
12
n
IO
9
8
i
0
Station Fig. 4.
Spatial variations in bacterial abundance (0) and [3H]thymidine incorporation rates (O) across warm-core ring 8 I-F.
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Microbial biomass and secondary production in a Gulf Stream ring
Table 2. Size fractionation of microbial biomass (ATP concentrations), [3H]thymidine incorporation and [3H]adenine uptake
Station
% of total ATP in <0.6 lam fraction
% of total [3H]thymidine incorporation by 0.6 lam filterable organisms
% [3H]adenine uptake by 0.6 lain filterable organisms
8 9 10 11 12 13 14
18 40 20 15 0 52 26
88 70 74 93 73 98 89
84 41 54 43 62 83 88
the ring margin. Moreover, rates of bacterial production, estimated from [~H]thymidine incorporation rates, were generally lower at stations in the ring core (,t = 2.2 x l0 s cells 1-1 d -1) than at stations located at the ring margin (,f -- 7.0 x 109 cells !-1 d-l). Most (>70%) of the total incorporation of [3H]thymidine was by free-living bacterialsized organisms filterable through 0.6 I~m Nuclepore filters. Generally, the percent of activity due to free-living bacteria was higher in cold shelf water entrained at the ring edge (range = 87.8 to 98.5%) than in the core water of Sargasso Sea origin, with the exception of water at the ring center (Table 2). Size fractionation of thymidine uptake in continental slope water outside the ring showed that 88.7% of the total incorporation was attributable to 0.6 ~tm filterable organisms. Per-cell rates of [3H]thymidine incorporation were highest in continental slope water at a site southsouthwest of the ring system, averaging 5.84 x 10 -7 pmoles cell-t d-1. Inside the eddy, per-cell activity was highest at the ring margin, while lowest per-cell rates of [3H]thymidine uptake occurred in the warm core of water appropriated from the Sargasso Sea. The average rate of thymidine incorporation, on a per-cell basis, was 3.3 times higher at the ring margin than in the center of the ring.
6
"'7 5
o
.--I
I
14
13
12
11
10
9
8
o
Station
Fig. 5.
Spatial variations in total microbial ATP (Q) and [3H]adenine incorporation rates (O) across warm-core ring 81-F.
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Adenine incorporation
Rates of [3H]adenine incorporation into microbial RNA were highest (4.1 to 4.8 nmoles I-~ d-~) at Stas 8 and 13 in cold shelf water entrained at the ring edge (Fig. 5). Comparable rates were also observed at the center of the ring; however, at Stas 10 and 12 where the parent mass of Sargasso Sea water had been altered by the penetration of cooler and less saline shelf and slope water, the rates of adenine incorporation into RNA were much lower (0.15 to 1.8 nmoles I-I d-I). The percentage of [3H]adenine uptake attributable to different size fractions was spatially dependent. At the ring margin, 80 to 90% of the [3H]adenine uptake was by small (<0.6 lam) free-living picoplankton (Table 2). However, at the core of the ring the percentage of label in the size fraction smaller than 0.6 lam decreased to 40 to 60%, indicating that a large proportion of the total adenine incorporation was perhaps due to large picoplankton and nanoplankton. At Stas 9 and 11, where approximately 60% of the total uptake of [3H]adenine was due to plankton larger than 0.6 lam, Chl a concentrations were correspondingly high. Particulate A TP and Chl a
Concentrations of particulate ATP in the component water masses of ring 81-F varied between 0.61 and 1.73 lag I-~ and were highest at stations located at the ring margin (Fig. 5). High ATP concentrations (1.23 lag 1-j) were also found at the center of the ring. However, other sites located in the parent mass of warm Sargasso Sea water had much lower total microbial biomass (0.61 and 0.70 lag ATP 1-l at Stas 10 and 12, respectively). The distribution of Chl a was similar to that of total microbial ATP: maximum levels were typically observed at the outer edges of the ring and at the ring center (Table 3). The majority (48 to 100%) of microbial ATP was associated with organisms, presumably phytoplankton, retained on 0.6 lam pore-size Nuclepore filters (Table 2). Size fractionation of samples taken from the core of the ring showed that 63 to essentially 100% of the particulate ATP was associated with microorganisms retained on 0.6 lam filters. At the ring margin, approximately 50 to 80% of the total microbial biomass was associated with the size fraction larger than 0.6 lam. If we calculate the ratio of ATP to Chl a, it appears that most of the microbial biomass in surface waters of warm-core ring 81-F was, in fact, represented by autotrophic organisms (PoMEROYet al., 1983).
Table 3. Concentrations o f particulate A TP and Chl a in sea water samples collected from Gulf Stream ring 8 I-F Station
Total microbial ATP*
Chlorophyll a t
8 9 10 11 12 13 14
1.43 1.43 0.70 1.23 0.61 1.73 1.10
Not done 3.06 0.28 2.38 0.34 1.42 0.64)
* Concentrations of microbial A T P are given in lag 1-~. t Concentrations of Chl a are given in lag I i.
Microbial biomass and secondary production in a Gulf Stream ring
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DISCUSSION
Preliminary analyses of microbiological parameters show that substantial differences in microbial biomass and production occurred across warm-core ring 81-F. In general, higher densities of bacterioplankton and increased rates of [3H]thymidine and [3H]adenine incorporation were observed at stations located at the ring margin. The spatial pattern we observed in bacterial abundance is similar to the distribution of bacteria in other warmcore rings (DUCKLOW, 1984). Moreover, our values for bacterial abundance and production are comparable to values reported for warm-core ring 82-B (DucKLOW, 1984). However, it is difficult to directly compare our results with those from other anticyclonic Gulf Stream rings because of the significant differences in the evolution of rings and the extent of their interaction with Gulf Stream meanders, surrounding slope water and shelf water. Continuous monitoring along a southwestward transect across warm-core ring 81-F indicated that temperature anomalies, attributable largely to differences in original water masses comprising the ring, still remained at 10 m depth 4 months after ring formation. The persistence of such characteristic temperature and salinity profiles in the surface layer of ring 81-F indicated that vertical convection and horizontal mixing were relatively weak processes (GORDONet al., 1982). Penetration of surrounding slope water and continental shelf water into the ring center appeared to be gradual over a period of months, and thus the central core of Sargasso Sea water remained partially isolated. We considered the possibility that the observed distribution patterns for microbial biomass and production reflected plankton distribution within the component water masses at the time of eddy formation. Certainly, the composition and distribution of planktonic populations in the core water of Sargasso Sea origin had important effects on the evolution of spatial patterns within the ring. However, that does not account for the higher densities of bacterioplankton and the increased rates of bacterial production observed at the ring margin or the high concentrations of total microbial biomass and Chl a found at the ring center. A likely cause of the elevated values for bacterial abundance and rates of thymidine incorporation at the edge of warm-core ring 81-F was the characteristic entrainment of surrounding slope water and cold shelf water as the ring moved westward along the continental shelf break. The strong temperature and salinity gradients observed at the surface of the ring margin (Stas 8 and 13) indicate that cold, low salinity shelf water had been entrained by warm-core ring 81-F. Moreover, our shipboard observations of sharp temperature gradients in the frontal zone surrounding the ring were confirmed by satellite measurements of the ring's surface-temperature field (data courtesy of the National Weather Service and National Environmental Satellite Servicc). Thus, horizontal mixing of slope water and continental shelf water, which are characterized generally by greater nutrient concentrations and higher biomass values, with the Gulf Stream remnant surrounding the ring may have accounted, at least in part, for the higher levels of bacterial abundance and production at the ring margin. The spatial patterns we observed in warm-core ring 81-F presumably reflect the response of microbial populations to new conditions which resulted from the juxtaposition of component water masses comprising and surrounding the ring. A number of recent studies have shown close association between the presence of physicochemical discontinuities and enhanced bacterial activity and abundance. High plankton concentrations at
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frontal boundaries have bccn reported previously for cyclonic cddics near the British Isles (PINGREE et al., 1979), warm-core eddies formed from meanders of the East Australian Current (TRANTEket al., 1980) and other warm-core Gulf Stream rings (DucKLow, 1984). The accumulation of biomass in the frontal region surrounding a ring core may indicate that one or all of the adjacent water masses contribute some limiting nutrient (FLooDGATE et al., 1981) or chelate a toxic metal. In contrast to the distribution of bacterioplankton, the greatest concentrations of total microbial biomass (ATP) and Chl a were found both at the periphery and near the ccnter of the ring. A similar distribution pattern was found for the incorporation of [-~H]adenine into microbial RNA, since dissolved adenine can be utilized by both autotrophic and heterotrophic microorganisms which possess the appropriate membrane transport mechanisms. The observed patterns for phytoplankton abundance and particulate ATP were similar to patterns described previously for samples from warm-core ring 82-B (NEt,SON et al., 1982; GOULD and FRYXELL, 1982). High concentrations of biogenic particulate matter and large numbers of diatoms were found at the center of ring 82-B 4 months after its formation. Those patterns were attributed, in part, to the entrainment and penetration of surrounding slope water and continental shelf water into the ring core.
The results of this study clearly demonstrate the relationship between microbial distribution and production and the changing physicochemical conditions within a mesoscale Gulf Stream ring. The distribution of plankton biomass and rates of microbial production were affected not only by the age of ring 81-F but also by the extent of its interactions with surrounding water masses. Elevated values for microbial biomass and activity were observed at the ring margin in continental shelf and slope water entrained by the ring as it moved westward along the shelf break. It might be expected that as a warm-core ring ages, there would be progressive replacement of Sargasso Sea water with neighboring slope water, and thus the ring would undergo nutrient enrichment. However, it should be noted that there is considerable variability in the evolution of warm-core rings with regard to horizontal exchange with the surrounding water, episodic interactions with Gulf Stream meanders and the time-scale of such processes. Moreover, biological activity in warm-core eddies may be affected by seasonal events such as the formation of a thermocline. Thus, sequential analyses over relatively short time scales would be critical in assessing changes in microbial biomass and activity. AcknowledgementsIWe thank P. J. Celone and the Atlantic Environmental Group (NMFS/NOAA) for information on the evolution and movement of warm-core ring 81 -F, S. Nishino and J. Sterns for expert technical assistance and thc officers and crew of R.V. Cape ttatteras for their assistance. This research was supported by National Science Foundation grants OCE-81107117 and OCE-8117834. Additional funding was prtwided from grant NA 8(IAA-D-IXX)91 from the National Sea Grant Program, U,S. Department of Commerce. REFERENCES ClOt.ONE P. J. and C. A. PRICE (19851 Anticyclonic warm-core Gull Strcam rings off the northcastcrn United States in 1982. Annales Biologiques, 39, in press. DUCKLOW H. W. 11984) Geographical ecology of marine bacteria: physical and biological variability at the mesoscale, in: Currentper~pectives in microbial ecology, M. J. KLU(Iand C. A. REI)DY, editors, American Society for Microbiology, pp. 22-31. FITZGI.]RAI,DJ. and J. L. CIIAMBERLIN(1981) Anticyclonic warm-core Gulf Stream eddies off the northeastern United States in 1979. Annales Biologiques, 36, 44-51. FI,OOI)GATE G. D., G. E. FOG(I, D. A. JONI-S, K. Lor,'lrrl-and C. M. TtJRI,I~Y (1981) Microbiological and zooplankton activity at a front in Liverpool Bay. Nature. London, 290, 133-136.
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FUIIRMAN J. A. and F. AZAM (1980) Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Applied and Environmental Microbiology, 39, 11185-1095. FHtRMAN J. A. and F. AZAM (1982) Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Marine Biology, 66, 109-120. GORDON H. R., D. K. CLARK, J. W. BROWN, O. B. BROWNand R. H. EVANS(1982) Satellite measurement of thc phytoplankton pigment concentration in the surface waters of a warm core Gulf Stream ring. Journal of Marine Research, 40, 491-502. GOULD R. W. and G. A. FRVXELL(1982) Abstracts, Winter Meeting of the American Society of Limnology and Oceanography. HOBBIF,J. E., R. J. DALEY and S. JASPER(1977) Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology, 33, 1225-1228. HOLM-HANSEN O. and C. R. BOOTH (1966) The measurement of adenosine triphosphate in the ocean and its ecological significance. Limnology and Oceanography, I l, 510-519. JACOBSEN T. R. (1978) A quantitative method for the separation of chlorophylls a and b from phytoplankton pigments by high pressure liquid chromatography. Marine Science Communications, 4, 33-47. JoV('E T. and P. WW.BE(1983) Warm-core rings of the Gulf Stream. Oceanus, 26, 34-44. JOYCE T. et al. (1984) Rapid evolution of a Gulf Stream warm-core ring. Nature, London, 308,837-8411. KARL D. M. (1979) Measurement of microbial activity and growth in the ocean by rates of stable ribonuclcic acid synthesis. Applied and Environmental Microbiology, 38, 850-8611. LAI D. Y. and P. L. R~CHARDSON(1977) Distribution and movement of Gulf Stream rings. Journal of Physical
Oceanography, 7,670-683. NELSON D. M., H. W. DUCKLOW and G. L. HLTCHCOCK(1982) Abstracts, Winter Meeting of the American Society of Limnology and Oceanography. PIN(IREE D. M., P. M. HOLHt';ANand G. T. MARDELL(1979) Phytoplankton growth and cyclonic eddies. Nature, London, 278, 245-247. POMEROY L. R., L. P. ATKINSON, J. O. BL,AN'rON,W. B. CAMPBELl,,T. R. JA('OBSI-N, K. tt. KERRI('Kand A. M. WOOD (19831 Microbial distribution and abundance in response to physical and biological processes on the continental shelf of southeastern U.S.A. Continental Shelf Research, 2, 1-20. SAUNDERS P. M. (1971) Anticyclonic eddies formed from shoreward meanders of the Gulf Stream. Deep-Sea Research, 18, 1207-1219. TRANTER D. J., R. R. PARKER and G. R. CRE'SSWELL(1980) Arc warm-core eddies unproductive'? Nature, London, 284, 540-542. WIEBE P. H. (1982) Rings of the Gulf Stream. Scientific American, 246, 60-711.
019S-1{~19/S5 $3,{1~1+ {I.11~| ~ 1985 Pergamon I'rcss lad.
Distribution of microbial biomass and secondary production in a warm-core Gulf Stream ring E. R. PEELE,* R. E. MURRAY,*R. B. HANSON,tL. R. POMEROY$and R. E. HODSON* (Received 16 September 1984; in final revised form 17 June 1985; uccQ~ted 18 June 1985) Abstract--Microbial biomass, bacterial abundance and secondary production were examined in relation to the changing physicochemical conditions within warm-core Gulf Stream ring 81-F. Highest densities of bacterioplankton (6.14 x ll)8 cells I L) occurred at the ring margin in continental shelf and slope water entrained by the ring. Likewise, both total bacterial secondary production (measured as incorporation of [3H]thymidine into DNA) and pcr-cell bacterial secondary production were highcst at thc ring margin, avcraging 291. l pmoles I ~ d i and 4.95 x 10 7 pmoles cell i d t respectively. In contrast, high concentrations of ATP (mean, 1.45 lag I ~) and chlorophyll a (mean, 2.29 lag I ~) were found both at the periphery and near the center of the ring. A similar distribution pattern was found for the incorporation of [3H]adenine into microbial RNA. The elevated values for microbial biomass and activity at the ring margin may reflect the response of microbial populations to new conditions resulting from the juxtaposition of water masses comprising and surrounding the ring. Our results indicate that the distribution of microbial populations and the rates of microbial processes occurring within warm-core ring 81-F were influenced by the age of the ring and the extent of its interaction with continental shelf water, surrounding slope water and Gulf Stream meanders.
INTRODUCTION
DURING the last decade it has been demonstrated that Gulf Stream rings are important mesoscale features in the Sargasso Sea and in continental slope water regions of the northwestern Atlantic. Warm anticyclonic rings form from northward meanders of the Gulf Stream which enclose cores of water appropriated from the Sargasso Sea (WIEBE, 1982). These warm-core eddies are generally 100 to 200 km in diameter, elliptical in shape and extend downward to a depth of approximately 1500 m (SAUNDERS,1971; LAI and RICtlARDSON, 1977). The initial physical, chemical and biological properties of the ring core are characteristic of Sargasso Sea water. However, as the ring ages, the core may gradually acquire properties of neighboring slope or shelf water through diffusion and entrainment. Nutrient concentrations and primary productivity are generally lower in Sargasso Sea water than in slope w a t e r ( J o Y c E and WIEBE, 1983), and so with dispersion and increasing turbulence, rings primarily undergo nutrient enrichment (LAI and RICItARDSON, 1977). Interactions with westward-extending Gulf Stream meanders may also alter the ring structure (JoYcE et al., 1984). It is estimated that 5 to 9 warm-core rings form yearly, some persisting for 200 to 300 days before decaying or coalescing with the Gulf Stream (FITZGERALDand CttAMBERLtN, * Department of Microbiology and Institute of Ecology, University of Georgia, Athens, GA 31~~02, U.S.A. 5 Skidaway Institute of Oceanography, Savannah, G A 31406, U.S.A. $ Institute of Ecology, University of Georgia, Athens. GA 30602, U.S.A. 1393
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1981; CN.()NJ.:and Ih~lo.:, 1985). Thc duration of such rcgular mcsoscalc fcaturcs makcs them ideal sites for correlative studies of the relationships between plankton distribution and physicochemical properties of the water masses comprising the ring. Moreover, if the integrity of the component water masses is maintained after ring formation, warm-core eddies would be useful systems for examining the effects of fronts or water mass boundaries on plankton distribution and activity. Based on the characteristics of the component water masses with respect to nutrient concentrations and primary productivity, one might expect that microbial biomass and rates of bacterioplankton secondary production would be lower in the ring core "than in the surrounding slope water. The results of some recent studies of bacterial distribution in warm-core ring 82-B suggest that bacterial numbers are, as expected, higher in the frontal zones surrounding the ring (DucKLOW, 1984). The principal aim of this study then was to ascertain if spatial variations in bacterial abundance and production reflected differences in the contrasting properties of the water masses comprising another warm-core ring (81-F). Variability in microbial biomass and secondary production is discussed in rehttion to thc agc and evolution of ring 81-F, and the influence of interactions between the ring and surrounding slope water on either the size of microbial populations or rates of microbial processes is examined. MATERIALS
AND
METIIODS
Seawater samples were collected from a depth of 10 m in clean 5-I Niskin ® bottles at 7 stations along a northeast-southwest transect across warm-core ring 81-F. The ring, centered at 38°24'N, 72°24'W, was located approximately 250 km northeast of Maryland, U.S.A. (Fig. 1) and was sampled 31 March to 1 April 1982, about 4 months after its formation. Ring 81-F formed late in 1981 and coalesced with the Gulf Stream off Cape Hatteras, NC on 27 May 1982 (CELONE and PRICE, 1985). Sampling sites included 4 locations within the core water of Sargasso Sea origin and 2 stations at the ring margin in cold shelf water entrained by the ring (Table 1). Samples were also collected from N
i
i
4'5° .
40 ° Ne.w J e r s e y if/~ Warm-Core .~ '~ ~Ring 81-F
35 °.75 ° / ' ~
~,,- , 70 =
65 °
Fig. 1. Location of warm-core ring 8I-F (31 March to 1 April 1982).
Microbial biomass and secondary production in a Gulf Strcam ring
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"Fable I. Stations sampled along a transect across warm-core ring 81-F, 31 March to I April 1982
Station 8 9 10 II 12 13 14
Location 38°53'N, 38°47'N, 38°34'N, 38°24'N, 38°14'N, 38°04'N, 37°51'N,
71°40'W 71°56'W 72°13'W 72°24'W 72°51'W 73°08'W 73°33'W
continental slope water south of the ring to provide a reference with which to compare the ring observations. All samples were processed within 1 h of collection. Surface water temperatures wcrc monitored continuously across thc ring, and expendable bathythermographs (XBTs) were used to determine the vertical temperature structure. Salinity was determined by precision salinometer measurements of samples from Niskin bottles. Measurements of in vivo fluorescence of Chl a were made by means of flowthrough pumping of surface seawater through a Turner Designs fluorometer.
Bacterial enumeration The procedure for acridine orange direct counts was adapted from HouutE et al. (1977). Seawater samples were preserved with formaldehyde (final concentration, 2% v/v) and refrigerated at 5°C until counted. Appropriate aliquots of preserved samples were incubated 4 min with acridine orange (final concentration, 0.01%) and filtered through 0.2 ~m Nuclepore filters which had been previously stained with irgalan black (acid-black no. 107, Ciba-Geigy Corp., Greensboro, NC). Filters were placed on microscope slides, covered with low fluorescence immersion oil and examined under epifluorescent illumination with an Olympus BHS microscope. A minimum of 10 randomly selected fields with />50 cells per field was counted on each filter.
Incorporation of [3H]thymidine Rates of [3H]thymidine incorporation were determined by the method of FUURMANand AZAM (1980, 1982). Triplicate 20 ml samples of seawater were incubated in the dark at approximate in situ temperature for 3 h with 3.2 nM [methyl-3H]thymidine (77.2 Ci mmol -z, New England Nuclear Corp., Boston, MA). After incubation, samples were chilled in ice water, extracted in an equal volume of ice-cold 10% trichloroacetic acid (TCA) and filtered through 0.22 lam Millipore filters. Filters were rinsed twice with 3 ml of cold 5% TCA and then transferred to vials containing 10 ml of Scintiverse ® (Fisher Scientific Co., Fair Lawn, N J). Radioactivity was assayed by liquid scintillation spectrometry. Formalin-killed controls were used to measure abiotic adsorption of [3H]thymidine. FUIIRMANand AZAM (1980, 1982) used 5 nM [3H]thymidine in their determinations of bacterial secondary production in various aquatic environments. In this study, however, seawater samples were incubated with 3.2 nM thymidine. Thus, the rates of [3H]thymidine incorporation into cold TCA-insoluble material (primarily DNA) were underestimated by about 10 to 15%.
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The rate of [3H]thymidine incorporation into the <0.6 jam size fraction was determined separately. Seawater samples were gently prefiltered through 0.6 jam Nuclepore filters and triplicate 20 ml subsamples incubated for 3 h with [3H]thymidine. After incubation, cells were extracted in cold trichloroacetic acid and the TCA-insoluble material collected on 0.22 jam Millipore filters. Filters were then processed in a manner identical to that described above. Bacterial production rates were estimated from [3H]thymidine incorporation rates using a conversion factor of 2.4 x 106 cells produced per pmol of exogenous thymidine incorporated (FuIIRMANand AZAM,1982). This empirical factor, suggested for offshore water, is based on a mean value of 2.6 x 10-5 g DNA per cell (FuHRMANand AZAM, 1982) and has been corrected for approximately 20% non-DNA activity in the TCA-insoluble material. Incorporation of [3H]adenine Rates of [3H]adenine incorporation were determined by the method of KARL(1979). A 250 ml sample of seawater was incubated in the dark at in situ temperature for 1 h with 0.1 jaCi ml -l [2-3H]adenine (15.5 Ci mmol -l, New England Nuclear Corp., Boston, MA). After incubation, 3 x 50 ml subsamples were filtered through 0.2 jam Nuclepore filters and treated with either cold 5% trichloroacetic acid (TCA), 0.3 M NaOH or 5% TCA at about 100°C. Extracts were chilled and then filtered through 0.45 jam Millipore filters. Filters were rinsed 3 times with cold 5% TCA, placed in scintillation vials and dissolved in 0.2 ml of Soluene-350 ® before adding 15 ml of scintillation cocktail. Radioactivity was assayed by liquid scintillation spectrometry. TCA-killed controls were used to measure chemical adsorption of [3H]adenine to particles. Rates of [3H]adenine uptake by different size fractions were determined as follows. Seawater samples were incubated with [3H]adenine, and after the incubation period, 20 ml aliquots were filtered through 0.2 and 0.6 jam pore-size Nuclepore filters. The filters were rinsed 3 times with 0.2 jam filtered seawater and then extracted and processed as described above. The percentage of adenine uptake attributable to 0.6 jam filterable organisms was calculated as [(dpm on 0.2 jam filter- dpm on 0.6 lam filter)/dpm on 0.2 jam filter] x 100. A TP determination Total microbial biomass was measured as the concentration of cellular (particulate) adenosine triphosphate (ATP). Seawater samples were filtered through 0.22 jam Millipore filters, and the filters extracted with 5 ml of boiling sodium bicarbonate buffer (0.1 M, pH 8.5) for 2 min. Samples were then cooled, placed in scintillation vials with 5 ml of Tris (tris[hydroxymethyl]aminomethane) buffer (0.1 M, pH 7.8) and frozen for later analysis. Particulate ATP concentrations were determined by the luciferin-luciferase method of HOLM-HANsENand BOOTIt (1966). The fraction of microbial ATP associated with attached bacteria and larger microheterotrophs was determined by filtering seawater samples through 0.6 jam pore-size filters. Filters were extracted and samples analyzed by the procedures described above for total particulate ATP. The ATP associated with free-living bacteria was calculated as: [ATP]f = [ATP]o.2 -[ATP]o.6.
E.R. PEELEetal.
1398
(Fig. 3). High salinity water (approximately 36%0 at 16.0°C) appropriated from the Sargasso Sea was found at the ring center (Stas 9 and 1 l); however, the warm water was not contiguous across the ring core. Cooler (.,? = 13.9°C) less saline (.f = 35.5%o) water was found at Stas 10 and 12; the discontinuity is attributed largely to spiral intermixing of Gulf Stream, slope and shelf water. Outward from the core (Stas 8 and 13), there was an abrupt decrease in surface temperature and salinity. The low T-S values in water associated with the ring edge most likely were caused by entrainment of cold, low salinity shelf water around the ring. Surface temperature and salinity of continental slope water southsouthwest of the ring were 12.0°C and 35.0%0, respectively. As the position and fate of Gulf Stream rings are usually inferred from the distribution of temperature or salinity below a depth of 100 to 200 m, expendable bathythermographs were used to determine the vertical temperature structure. Vertical sections through 81-F clearly show a subsurface core of warm water, presumably of Sargasso Sea origin (Fig. 3).
Bacterial numbers Highest densities of bacterioplankton (6.14 x 108 cells l-l), determined by acridine orange direct counts, occurred at Stas 8 and 13 in shelf water entrained by the ring (Fig. 4). Bacterial numbers were typically lower in the ring core (remnant Sargasso Sea water), ranging from 5.46 x 108 cells 1-1 at Sta. 9 to 3.27 x 108 cells 1-~ at the ring center. In continental slope waters south of warm-core ring 81-F, bacterial abundance averaged 4.09 x 108 cells 1-~.
Thymidine incorporation Rates of [3H]thymidine incorporation into cold TCA-insoluble material were highest at the outer edge of warm-core ring 81-F, averaging 291.1 pmoles 1-I d -~ at 10 m depth (Fig. 4). In the core water of Sargasso Sea origin, incorporation rates of exogenous thymidine were much lower, ranging from 57.0 to 135.8 pmoles I-~ d -~. Although there was a slight increase in the rate of [SH]thymidine incorporation at the ring center (Sta. 11), incorporation rates in the warm core of ring 81-F were generally about 2.8 times lower than rates at
400
aoo ~,_,
126
O'7 ZOO ~ - - J
4
m
"r:
~v 100
2
Z I O
I
I
I
I
I
I
I
14
13
12
n
IO
9
8
i
0
Station Fig. 4.
Spatial variations in bacterial abundance (0) and [3H]thymidine incorporation rates (O) across warm-core ring 8 I-F.
1399
Microbial biomass and secondary production in a Gulf Stream ring
Table 2. Size fractionation of microbial biomass (ATP concentrations), [3H]thymidine incorporation and [3H]adenine uptake
Station
% of total ATP in <0.6 lam fraction
% of total [3H]thymidine incorporation by 0.6 lam filterable organisms
% [3H]adenine uptake by 0.6 lain filterable organisms
8 9 10 11 12 13 14
18 40 20 15 0 52 26
88 70 74 93 73 98 89
84 41 54 43 62 83 88
the ring margin. Moreover, rates of bacterial production, estimated from [~H]thymidine incorporation rates, were generally lower at stations in the ring core (,t = 2.2 x l0 s cells 1-1 d -1) than at stations located at the ring margin (,f -- 7.0 x 109 cells !-1 d-l). Most (>70%) of the total incorporation of [3H]thymidine was by free-living bacterialsized organisms filterable through 0.6 I~m Nuclepore filters. Generally, the percent of activity due to free-living bacteria was higher in cold shelf water entrained at the ring edge (range = 87.8 to 98.5%) than in the core water of Sargasso Sea origin, with the exception of water at the ring center (Table 2). Size fractionation of thymidine uptake in continental slope water outside the ring showed that 88.7% of the total incorporation was attributable to 0.6 ~tm filterable organisms. Per-cell rates of [3H]thymidine incorporation were highest in continental slope water at a site southsouthwest of the ring system, averaging 5.84 x 10 -7 pmoles cell-t d-1. Inside the eddy, per-cell activity was highest at the ring margin, while lowest per-cell rates of [3H]thymidine uptake occurred in the warm core of water appropriated from the Sargasso Sea. The average rate of thymidine incorporation, on a per-cell basis, was 3.3 times higher at the ring margin than in the center of the ring.
6
"'7 5
o
.--I
I
14
13
12
11
10
9
8
o
Station
Fig. 5.
Spatial variations in total microbial ATP (Q) and [3H]adenine incorporation rates (O) across warm-core ring 81-F.
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E . R . PEELEet al. k.,
Adenine incorporation
Rates of [3H]adenine incorporation into microbial RNA were highest (4.1 to 4.8 nmoles I-~ d-~) at Stas 8 and 13 in cold shelf water entrained at the ring edge (Fig. 5). Comparable rates were also observed at the center of the ring; however, at Stas 10 and 12 where the parent mass of Sargasso Sea water had been altered by the penetration of cooler and less saline shelf and slope water, the rates of adenine incorporation into RNA were much lower (0.15 to 1.8 nmoles I-I d-I). The percentage of [3H]adenine uptake attributable to different size fractions was spatially dependent. At the ring margin, 80 to 90% of the [3H]adenine uptake was by small (<0.6 lam) free-living picoplankton (Table 2). However, at the core of the ring the percentage of label in the size fraction smaller than 0.6 lam decreased to 40 to 60%, indicating that a large proportion of the total adenine incorporation was perhaps due to large picoplankton and nanoplankton. At Stas 9 and 11, where approximately 60% of the total uptake of [3H]adenine was due to plankton larger than 0.6 lam, Chl a concentrations were correspondingly high. Particulate A TP and Chl a
Concentrations of particulate ATP in the component water masses of ring 81-F varied between 0.61 and 1.73 lag I-~ and were highest at stations located at the ring margin (Fig. 5). High ATP concentrations (1.23 lag 1-j) were also found at the center of the ring. However, other sites located in the parent mass of warm Sargasso Sea water had much lower total microbial biomass (0.61 and 0.70 lag ATP 1-l at Stas 10 and 12, respectively). The distribution of Chl a was similar to that of total microbial ATP: maximum levels were typically observed at the outer edges of the ring and at the ring center (Table 3). The majority (48 to 100%) of microbial ATP was associated with organisms, presumably phytoplankton, retained on 0.6 lam pore-size Nuclepore filters (Table 2). Size fractionation of samples taken from the core of the ring showed that 63 to essentially 100% of the particulate ATP was associated with microorganisms retained on 0.6 lam filters. At the ring margin, approximately 50 to 80% of the total microbial biomass was associated with the size fraction larger than 0.6 lam. If we calculate the ratio of ATP to Chl a, it appears that most of the microbial biomass in surface waters of warm-core ring 81-F was, in fact, represented by autotrophic organisms (PoMEROYet al., 1983).
Table 3. Concentrations o f particulate A TP and Chl a in sea water samples collected from Gulf Stream ring 8 I-F Station
Total microbial ATP*
Chlorophyll a t
8 9 10 11 12 13 14
1.43 1.43 0.70 1.23 0.61 1.73 1.10
Not done 3.06 0.28 2.38 0.34 1.42 0.64)
* Concentrations of microbial A T P are given in lag 1-~. t Concentrations of Chl a are given in lag I i.
Microbial biomass and secondary production in a Gulf Stream ring
1401
DISCUSSION
Preliminary analyses of microbiological parameters show that substantial differences in microbial biomass and production occurred across warm-core ring 81-F. In general, higher densities of bacterioplankton and increased rates of [3H]thymidine and [3H]adenine incorporation were observed at stations located at the ring margin. The spatial pattern we observed in bacterial abundance is similar to the distribution of bacteria in other warmcore rings (DUCKLOW, 1984). Moreover, our values for bacterial abundance and production are comparable to values reported for warm-core ring 82-B (DucKLOW, 1984). However, it is difficult to directly compare our results with those from other anticyclonic Gulf Stream rings because of the significant differences in the evolution of rings and the extent of their interaction with Gulf Stream meanders, surrounding slope water and shelf water. Continuous monitoring along a southwestward transect across warm-core ring 81-F indicated that temperature anomalies, attributable largely to differences in original water masses comprising the ring, still remained at 10 m depth 4 months after ring formation. The persistence of such characteristic temperature and salinity profiles in the surface layer of ring 81-F indicated that vertical convection and horizontal mixing were relatively weak processes (GORDONet al., 1982). Penetration of surrounding slope water and continental shelf water into the ring center appeared to be gradual over a period of months, and thus the central core of Sargasso Sea water remained partially isolated. We considered the possibility that the observed distribution patterns for microbial biomass and production reflected plankton distribution within the component water masses at the time of eddy formation. Certainly, the composition and distribution of planktonic populations in the core water of Sargasso Sea origin had important effects on the evolution of spatial patterns within the ring. However, that does not account for the higher densities of bacterioplankton and the increased rates of bacterial production observed at the ring margin or the high concentrations of total microbial biomass and Chl a found at the ring center. A likely cause of the elevated values for bacterial abundance and rates of thymidine incorporation at the edge of warm-core ring 81-F was the characteristic entrainment of surrounding slope water and cold shelf water as the ring moved westward along the continental shelf break. The strong temperature and salinity gradients observed at the surface of the ring margin (Stas 8 and 13) indicate that cold, low salinity shelf water had been entrained by warm-core ring 81-F. Moreover, our shipboard observations of sharp temperature gradients in the frontal zone surrounding the ring were confirmed by satellite measurements of the ring's surface-temperature field (data courtesy of the National Weather Service and National Environmental Satellite Servicc). Thus, horizontal mixing of slope water and continental shelf water, which are characterized generally by greater nutrient concentrations and higher biomass values, with the Gulf Stream remnant surrounding the ring may have accounted, at least in part, for the higher levels of bacterial abundance and production at the ring margin. The spatial patterns we observed in warm-core ring 81-F presumably reflect the response of microbial populations to new conditions which resulted from the juxtaposition of component water masses comprising and surrounding the ring. A number of recent studies have shown close association between the presence of physicochemical discontinuities and enhanced bacterial activity and abundance. High plankton concentrations at
14112
E . R . I'i!l!H~et al.
frontal boundaries have bccn reported previously for cyclonic cddics near the British Isles (PINGREE et al., 1979), warm-core eddies formed from meanders of the East Australian Current (TRANTEket al., 1980) and other warm-core Gulf Stream rings (DucKLow, 1984). The accumulation of biomass in the frontal region surrounding a ring core may indicate that one or all of the adjacent water masses contribute some limiting nutrient (FLooDGATE et al., 1981) or chelate a toxic metal. In contrast to the distribution of bacterioplankton, the greatest concentrations of total microbial biomass (ATP) and Chl a were found both at the periphery and near the ccnter of the ring. A similar distribution pattern was found for the incorporation of [-~H]adenine into microbial RNA, since dissolved adenine can be utilized by both autotrophic and heterotrophic microorganisms which possess the appropriate membrane transport mechanisms. The observed patterns for phytoplankton abundance and particulate ATP were similar to patterns described previously for samples from warm-core ring 82-B (NEt,SON et al., 1982; GOULD and FRYXELL, 1982). High concentrations of biogenic particulate matter and large numbers of diatoms were found at the center of ring 82-B 4 months after its formation. Those patterns were attributed, in part, to the entrainment and penetration of surrounding slope water and continental shelf water into the ring core.
The results of this study clearly demonstrate the relationship between microbial distribution and production and the changing physicochemical conditions within a mesoscale Gulf Stream ring. The distribution of plankton biomass and rates of microbial production were affected not only by the age of ring 81-F but also by the extent of its interactions with surrounding water masses. Elevated values for microbial biomass and activity were observed at the ring margin in continental shelf and slope water entrained by the ring as it moved westward along the shelf break. It might be expected that as a warm-core ring ages, there would be progressive replacement of Sargasso Sea water with neighboring slope water, and thus the ring would undergo nutrient enrichment. However, it should be noted that there is considerable variability in the evolution of warm-core rings with regard to horizontal exchange with the surrounding water, episodic interactions with Gulf Stream meanders and the time-scale of such processes. Moreover, biological activity in warm-core eddies may be affected by seasonal events such as the formation of a thermocline. Thus, sequential analyses over relatively short time scales would be critical in assessing changes in microbial biomass and activity. AcknowledgementsIWe thank P. J. Celone and the Atlantic Environmental Group (NMFS/NOAA) for information on the evolution and movement of warm-core ring 81 -F, S. Nishino and J. Sterns for expert technical assistance and thc officers and crew of R.V. Cape ttatteras for their assistance. This research was supported by National Science Foundation grants OCE-81107117 and OCE-8117834. Additional funding was prtwided from grant NA 8(IAA-D-IXX)91 from the National Sea Grant Program, U,S. Department of Commerce. REFERENCES ClOt.ONE P. J. and C. A. PRICE (19851 Anticyclonic warm-core Gull Strcam rings off the northcastcrn United States in 1982. Annales Biologiques, 39, in press. DUCKLOW H. W. 11984) Geographical ecology of marine bacteria: physical and biological variability at the mesoscale, in: Currentper~pectives in microbial ecology, M. J. KLU(Iand C. A. REI)DY, editors, American Society for Microbiology, pp. 22-31. FITZGI.]RAI,DJ. and J. L. CIIAMBERLIN(1981) Anticyclonic warm-core Gulf Stream eddies off the northeastern United States in 1979. Annales Biologiques, 36, 44-51. FI,OOI)GATE G. D., G. E. FOG(I, D. A. JONI-S, K. Lor,'lrrl-and C. M. TtJRI,I~Y (1981) Microbiological and zooplankton activity at a front in Liverpool Bay. Nature. London, 290, 133-136.
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FUIIRMAN J. A. and F. AZAM (1980) Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Applied and Environmental Microbiology, 39, 11185-1095. FHtRMAN J. A. and F. AZAM (1982) Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Marine Biology, 66, 109-120. GORDON H. R., D. K. CLARK, J. W. BROWN, O. B. BROWNand R. H. EVANS(1982) Satellite measurement of thc phytoplankton pigment concentration in the surface waters of a warm core Gulf Stream ring. Journal of Marine Research, 40, 491-502. GOULD R. W. and G. A. FRVXELL(1982) Abstracts, Winter Meeting of the American Society of Limnology and Oceanography. HOBBIF,J. E., R. J. DALEY and S. JASPER(1977) Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology, 33, 1225-1228. HOLM-HANSEN O. and C. R. BOOTH (1966) The measurement of adenosine triphosphate in the ocean and its ecological significance. Limnology and Oceanography, I l, 510-519. JACOBSEN T. R. (1978) A quantitative method for the separation of chlorophylls a and b from phytoplankton pigments by high pressure liquid chromatography. Marine Science Communications, 4, 33-47. JoV('E T. and P. WW.BE(1983) Warm-core rings of the Gulf Stream. Oceanus, 26, 34-44. JOYCE T. et al. (1984) Rapid evolution of a Gulf Stream warm-core ring. Nature, London, 308,837-8411. KARL D. M. (1979) Measurement of microbial activity and growth in the ocean by rates of stable ribonuclcic acid synthesis. Applied and Environmental Microbiology, 38, 850-8611. LAI D. Y. and P. L. R~CHARDSON(1977) Distribution and movement of Gulf Stream rings. Journal of Physical
Oceanography, 7,670-683. NELSON D. M., H. W. DUCKLOW and G. L. HLTCHCOCK(1982) Abstracts, Winter Meeting of the American Society of Limnology and Oceanography. PIN(IREE D. M., P. M. HOLHt';ANand G. T. MARDELL(1979) Phytoplankton growth and cyclonic eddies. Nature, London, 278, 245-247. POMEROY L. R., L. P. ATKINSON, J. O. BL,AN'rON,W. B. CAMPBELl,,T. R. JA('OBSI-N, K. tt. KERRI('Kand A. M. WOOD (19831 Microbial distribution and abundance in response to physical and biological processes on the continental shelf of southeastern U.S.A. Continental Shelf Research, 2, 1-20. SAUNDERS P. M. (1971) Anticyclonic eddies formed from shoreward meanders of the Gulf Stream. Deep-Sea Research, 18, 1207-1219. TRANTER D. J., R. R. PARKER and G. R. CRE'SSWELL(1980) Arc warm-core eddies unproductive'? Nature, London, 284, 540-542. WIEBE P. H. (1982) Rings of the Gulf Stream. Scientific American, 246, 60-711.