Sellner, Zingmark, Miller: The 14C Method of Measuring the Total Annual Production of Phytoplankton 119

Botanica MarinaVol. XIX, p. 119-125,1976

Interpretations of the 14C Method of Measuring the Total Annual Production of Phytoplankton in aSouth Carolina Estuary*)

Kevin G. Sellner

Department ofOceanography, Dalhousie University, Halifax, N. S., Canada B3H3J5

Richard G. Zingmark

Department of Biology and Belle W. Baruch Institute for Marine Biology and Coastal Research, University of SouthCarolinat Columbia, S. C, U. S. A. 29208

and

Thomas G. Miller

Belle W. Baruch Institute for Marine Biology and Coastal Research, University of South Carolina, Columbia, S. C,U. S. A. 29208

<Rec. 17. 3. 75)

The 14C primary production technique for the estimation of total phytoplanktonic primary production has beenapplied to an estuary in South Carolina. Total phytoplanktonic production generally followed the annual tempera-ture cycle and ranged from a low of 6.4 mgC/m2 · hi in November to a high of 234 mgC/m2 · h* in August. Totalannual production of phytoplankton was calculated to be 346 gC/m2. Over a year, the proportion of the release ofdissolved organic carbon (DOC) from estuarine phytoplankton ranged from 3 to 55 % of the total daily primary pro-duction. Inconsistencies in the amount of DOC measured are discussed relative to the experimental methods thatwere employed.

Introduction

The application of the 14C method (Steemann-Nielsen1952) for the measurement of phytoplanktonic primaryproduction rates is routine in laboratories and field stu-dies globally. However, criticisms of the method arenumerous (Fogg 1969, Morris et al 1971, Strickland1965). In recent years, measurements of the carboncontent of the medium in which the cells are suspendedhave enhanced the confusion already associated with the14C technique (Anderson and Zeutschel 1970, Arthurand Rigler 1967, Nalewajko and Lean 1972, Schindler1971, Schindler and Holmgren 1971, Thomas 1971,Williams et al 1972).

Large amounts of carbon have been observed in the fil-trates of 14C-labelled natural samples (Table i). Inshore,

*) This paper is contribution No. 128 of the Belle W. BaruchInstitute for Marine Biology and Coastal Research.

productive areas generally have high production rateswith low percentages of fixed carbon released to thesurrounding medium, while oligotrophic areas are charac-terized by low total fixation rates with high percentagesof extracellular carbon (Anderson and Zeutschel 1970,Fogg et al 1965, Thomas 1971, Watt 1966). Further,annual differences in the release of organic matter fromphytoplankton have also been found, with higher releaserates in post-bloom and senescent cells and lower ratesfound at most other times of the year (Hellebust 1965).

Productivity measurements in estuaries should furtherthe understanding of the production technique and ener-getics of the inshore environment. Production rates areusually high and one would expect considerabie concen-trations of organic matter to be released in these eutrophicregions. To determine the actual amounts of carbon fixedand released by phytoplankton, a year long biweeklysurvey was undertaken in a high salinity, weil-mixedestuary east of Georgetown, S. C. during 1972-73.

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1 20 Seilner, Zingmark, Miller; The 14C Method of Measuring the Total Annual Production of Phytoplankton

Tab. 1. Percentage of Fixed Carbon Released from Naturai Popula-tions of Phytoplankton

Location

North Sea

North AtlanticSargasso Sea

Sargasso Sea

Öligotrophicöffshore areaWashington

South IndianOcean

S,E. U.S. Coast

S.E. US. A,coastal

Upwelling areaoff Washington

Woods HoleGulf of MaineBritish Colum-

biaAntarctic Sea

Cochin, IndiaGeorgia Estu-

ariesWindermere

Tring Reser-voirs

Lake Ontario

Canadian ShieldLakes

Canadian ShieldLakes

Time of Year

June

AugustNovember

November

July

—

November

September

July

AprilMay-

annual

January-Maich

AugustApril

February-SeptemberMaich-April

year

yeai

% Release

5. 8-7.8 (LT)

12.7-34,335

0-22.9

26

5-3210

0-27.4

7

4.5^1617-3835-40

i-38

1-20

0.2-6,817,1

1-13 (LT)

23.1-76.1

1

2

Reference

Fogg et al. ,1965Choi, 1972Hobbie et al. ,1972Thomas,1971

Anderson &Zeutschel,1970

Jitts, 1967Hobbie et aL,1972

Thomas,1971Anderson &Zeutschel,1970Hellebust,

1965Antiae/ö/.,1963Hörne et <?/,,1969Samuel et al.,1971Thomas, 1971Foggetai,1965Watt, 1966

Nalewajko&Marin,1969Schindler &Holmgren,1971Schindler &Holmgren,1971

(LT) = ONLY RELEASE FROM LIGHT BOTTLE POPULATION

Methods

Three stations were established in the North Inletestuary, one in the main channel connecting the estuaryto the open ocean (Station 1), another in a small, sandy-bottomed tidal creek draining a large area of sandy saltmarsh and emptying into North Inlet (Station 2) and athird Station» approximately one kilometer inland fromStation l, representing a large volume tidal creek(Station 3). This last site drained extensive areas of finegrain sediment marsh and oyster bars (Fig. 1), Samples

were collected and analyzed bi-weekly beginning in July,1972.

Temperature, pH, alkalinity, salinity and Secchi discmeasurements were obtained for each Station. Watersamples collected from the surface and 50 % light inten-sity depth were inoculated with 1-20 //Ci/l30 ml bottleinto duplicate light and dark BOD botties and incubatedfrom 2—5 hours in the time-span 1000—1500 hrs in simu-lated in situ light intensity incubators at Station 3. Sub-samples (from 10—120 ml) were filtered at vacuum pres-sures less than 130 mm Hg. Filters were washed withdilute HC1 and placed in scintillation vials containing10 ml of Bray's scintillation Cocktail (Bray, 1960). Oneml aliquots of acidiiled, air-bubbled filtrate were pipet-ted into scintillation vials containing fluor. Counts/minute (CPM) were obtained from a PACKARD TR1-CARB #3320 Liquid Scintülation Counter at 75-80 %efficiency. CPM were adjusted for volume differences,and total production rates were determined from theformulae of Strickland and Parsons (1968), with totalproduction equalling particulate -14C fixed plus dissolvedorganic -14C(DOC) released. Percentages of releasedcarbon-14 were calculated äs:

DOC -14CTotal Production -14C

X 100

where DOC -14C is cpm/light filtrate minus background.

A series of measurements were made in the summerof 1974 at 100 %, 50 % and l % light levels to determineproduction rates below the 50 % light level. The relation-ship of production rates at 50 and l % light levels (50 %(l %) was determined, this correction factor (0.45) wasused for determining fixation rates at the l % light levelat each sampling date. Production/m2 was calculatedfrom planimeter Integration of production/m3 versusdepth for the three stations. Annual production rates/m2 were obtained by multiplying the mean fixation/m2/h r -12hr /d 365 d/yr.

100 ml water samples from each Station depth werefixed with Lugol's iodine in the field. Cells from uncon-centrated subsamples were counted on a Palmer-Maloneynannoplankton counting slide (Palmer and Maloney1954) at 450 x.

Results

Total production rates followed seasonal changes in thewater temperature (Fig. 2). Maximum rates observedwere 234 mgC/cm2/hr on 2 July 1972; lowest total pro-duction rates were noted on 17 November 1972, whenonly 6,44 mgC/m2/hr was incorporated into the phyto-plankton (Table II). However, total fixation duringFebruary 1973, was probably lower; the loss of thedissolved fraction prevented a comparison, but particu-late fixation was 0.7 mgC/m^hr, the lowest rate measuredduring the study.

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Sellner, Zingmark, MiBetr The *̂ C Method of Meaturing the Total Annual Production of Phytoplankton 121

84· 80· 76*

ClambankCreek

EASTERNU.S.A

.·""*··*%**' »***·*·**.'·. S.C.

getcwn

Town Creek

NorthIn/et

oO

c:O

36«

32«

Fig. 1. Map of North Inlet Estuary, east of Georgetown, S. C.

250 -

1972M 0 N T H S 1973

Fig. 2. Total phytoplanktonic primary production ( ) and water temperature (—) in the North Inlet Estuary

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122 Seltner, Zingmark, Miller: The I4C Method of Measuring the Total Annual Production of Phytoptankton

Tab. 2. Total Production Rate for the North Inlet, S. C. Estuary1972-73.

Date

2 J u l 7216Jul 7229 Jul 7212 Äug 7225 Äug 729Sep 72

23Sep 7270ct 72

21 Oet 724Nov 72

17Nov 722 Dec 72

16 Dec 7214 Jan 7328 Jan 7318 Feb 733 Mai 73

17 Mai 732Apr 73

17Apr 7328Apr 7312 May 7330 May 7314Jun 7328Jun 73

ParticulatemgC/m2/hr

14998.854.345.459.167.588.8

157100

12.95.7

14.88.44.07.70.76.9

19.443.754.4

14239.874.9

113109

ReleasedmgC/m2/hr

84,553.254.341.956.882.538.141.8—1.40.7

—1.33.74.0

——3.12.62.44.14.37.64.24.3

TotalmgC/m2/hr

234152109

87.3116150127199—14.3

6.4—

9.77.7

11.7—

—22.546.356.8

14644.182.5

117113

%DOC

3635504849553021—1011—

134834—

—14643

10944

The amounts of carbon found in the filtrates variedfrom 3-55 % of the total carbon fixed/m2/hr (Tab. 2,Fig. 3). The maximum percentages of released carbon(30-55%) were observed in the summer months of 1972and January 1973 (34-48 %). The highest concentrationof carbon lost to the environment was 84.5 mgC/m2/hrand occurred on 2 July 1972.

The difference between total production estimates andparticulate rates are large. If one ignores the carbonreleased, production rates from 3—55% lower daüy arecalculated.

Standing crop varied seasonally, with higher cell concen-trations observed in September-October 1972, Januaryand April 1973. The cell concentrations ranged from0.54 X 106 cells/1 on 17 November 1972 to 3.40 106

ceDs/1 on 17 April 1973 (Fig. 4).

Discussion

The seasonal trend in annual production and water tem-perature in the North Inlet estuary agrees with data col-lected from the estuaries of Beaufort, N. C. (Thayer1971, Williams 1966) and the Patuxent River estuary ofthe Chesapeake Bay (Stross and Stottlemeyer 1965).Comparing particulate production data from other easternseaboard areas with the observed particulate fixationrates in the present study (Tab. 3), we find the NorthInlet estuary intermediate in production between theestuaries of N.C. and Georgia.

However, Computing primary production rates solelyfrom the amount of 14C-particulate material caught on asmall pore filter is unjustified. From 3-55 % of the totalproduction would be ignored, if we consider only theparticulate fixed -14C in the present study. The amountof carbon lost was considerable (up to 84.5 mgC/m2/hr)in July 1972, even when relatively small volumes werefiltered (50-120 ml). Fogg et al (1965) reported 7-50%of the carbon fixed was released when 25—50 ml samples

250-

200 -

c\JEv,O

»E

f ,

N D l J F

M O N T H S

M M

Fig. 3. Total (-

1972-) paiticulate ( ) and released organic caibon ( ) for phytoplankton in North Inlet Estuary

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Seilner, Zingmark, Miller: The 14C Method of Measuring the Total Annual Pioduction of Phytoplankton 123

(O

LÜO

A S

1972

N D l J FM 0 N T H S

M A

1973

M

Fig. 4. Cell counts for North Inlet Estuary, 1972-1973.

Tab. 3. A comparison of estuarine primary production rates forthe Eastern Seaboard of the U.S.

Location

Narragansett BayL. 1. SoundRatuxent River Est.

Beaufort Est, N. C.Beaufort Est, N. C.North Inlet EstAtlamaha Rivermouth

Method

02O, (net)14C

14C

O, (net)14C14C

ProductionRategC/m2/yr

84170193-330

6753

259 (346)1)546

Reference

Smayda, 1957Riley, 1956Stross & Stottle-meyer, 1966Thayer, 1971Williams, 1966present studyThomas, 1966

Particulate = 259; total (particulate + released) = 346.

were filtered. Cell lysis during filtration resulted in higherrelease of organic carbon. Aurthur and Rigler (1967),Schindler (1971) and Schindler and Holmgren (1971)found large errors in filtering 5—50 ml samples, thelatter authors found increased release in samples abun-dant in nannoplankton. Schindler and Holmgren reportedthat from 24-77% of the total production was lost iffiltration problems were not taken into account.

The release of large percentages of the fixed carbon inr

the summer and winter could be etfpected, but for diffe-rent reasons. The large summer percentages hsave severalexplanations. The first is the lysis of cells in filtering50-120 ml of sample. The total amount of carbon fixed

includes both particulate carbon and that found outsidethe cells. If in routine fütration, considerable carbon islost from breaking cells, primary production rates will bedrastically underestimated, if the particulate fixed carbonis the only 14C-labelled material counted. In the summerof 1972, the particulate phytoplanktonic production/hrwas only 50-60% of the total productivity. Collectionand measurement of the released carbon was thus^cricialto estimate total fixation rates. The second reason is thatthe summer is the season of maximum radiant energyand total production. High light intensities can cause in-creased release of phytoplanktonic carbon through photo-oxidation damage to cells and photoinhibition of thephotosynthetic apparatus (Fogg et al. 1965, Hellebust1965, Watt 1966). Hörne et ai (1969) reported from1-38% of the carbon fixed was released when naturalsamples were incubated at high light intensities.

The abundance of nannoplankton in North Inlet estuaryis probably cnicial to understanding the release figurespresented. Malone (1971) found nannoplankton thedominant phytoplankton in both Standing crop and pro-duction in inshore and oceanic waters. Further, nanno-plankton production is most important in the summermonths in the New York Bight (Malone, pers. comm.). Ifthis was the case in the North Inlet estuary, the largerelease noted in the summer of 1972 was probably a func-tion of nannoplankton lysis on filtration. Unialgal cul-tures of Skeletonema costatum have a constant fixationrate/ml filtered when 5-100 ml of between 105 and l O8

cells/1 are filtered. Further, there is no increased release

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124 14,Seilner, Zingmark, Miller: The 14C Method of Measuring the Total Annual Production of Phytoplankton

due to filter clogging or cell lysis when larger volumes arefiltered (Seilner, unpubl. data). Therefore the high per-centage of release noted in the estuary in summer 1972could have been due to nannoplankton lysis during fil-tration.

There were two relatively large and one small phyto-plankton blooms in the study period, with the largepeaks falling in mid-January and April 1973, and thesmaller peak in September-October 1972. The latesummer bloom of 9 September 1972 was concomitantwith the relatively large DOC percentage (55%) thatwas calculated. Similarly, following the other twoblooms, there is an increase in the release of dissolvedmaterials to 34-4S% in January 1973 and to 10% inearly May 1973.

The increased release of material following blooms haspreviously been reported from natural populations in theGulf of Maine and Woods Hole (Hellebust 1965), 4-16 %of the fixed carbon was released from apparently healthypopulations and increased to 17.38 % in post-bloom cells.A similar phenomenon could partially explain the highrelease rates we have noted.

The release percentage of 34-48% in January 1973may have been in part a function of the low totalfixation peculiar to the month. Any activity found inthe filtrate would have formed a considerable fractionof the total fixed carbon. Therefore release percentageswould be high. Chapman and Rae (1969) state, ". . . partof the explanation for very high excretion in naturalmixed communities.. . is undoubtedly that these wereobtained when total fixation was low." Further, Helle-bust (1965) and Fogg (1958) have observed increasein excretion rates at lower light intensities. The winterminima of light and temperature could result in a similarSituation in the North Inlet estuarine phytoplankton,increasing the percentages released.

The low percentages noted from 17 Mär 73 through June1973 (4-14 %) are similar to data collected in August inGeorgia estuaries (Thomas 1971) and in the Spring inWoods Hole and the Gulf of Maine (Hellebust 1965)where 0.2-6.8 and 4.5-16% was released in healthypopulations, respectively. At these later sampling dates,small volumes of 10-20 ml were filtered, decreasing theamount of carbon released during cell lysis in filtration.This percentage ränge better reflects natural release ratesthan do the percentages from the previous sampling dates,where larger volumes were filtered.

The dark bottle in the 14C method is a dilemma; whatshould be done with it? Should it even be used? Foggand co-workers (1965), Morris et al (1971) and Tolbert(1974) discussed two distinct mechanisms for the fixationof CO2, one mediated and one inhibited by light. Thesetwo processes appear to be independent of each other.If this is so, we cannot substract the values, for each

process adds fixed carbon to the population. In thepresent study, only light fixation and subsequent releasewas accounted for in extracellular carbon and percentagerelease data. Dark release was not included. The annualfluctuation in release finds low light and dark filtrateradioactwity in the winter months with summer lightrelease values increasing to approximately twice summerdark release activity. Future work regarding the darkbottle in the 14C-technique is crucial for interpretingcorrectly the mechanisms of primary production.

Summary

1. Total production was followed in an estuary east ofGeorgetown, S. C. for one year.2. Total production rates followed seasonal changes inwater temperature. Particulate production is 259 gC/m2/yr, falling between North Carolina and Georgia estuarineproduction data. If the carbon released is included, thetotal production is 346 gC/m2/yr. If the released carbonis neglected, the rate of carbon is underestimated by25%.3. High release rates were observed in summer 1972,where up to 55% of the carbon fixed/hr was released.Discussions of these large release rates centers on celllysis during filtration. During the winter months of 1973,less than 48% of the fixed carbon was released. This largerelease is attributed to low total fixation rates of theseason. Spring to summer 1973 release data reveal only3—14 % extracellular carbon and these data are moreacceptable due to the minimization of the cell lysisproblem and the increase in total production rates.4. The 14C method should be used with caution in evenvery productive areas (e.g. estuaries). Special attentionshould be made to volume filtration errors (cell lysis)producing high released carbon percentages, and incorpo-ration of the dark bottle in primary production estimates.

Acknowledgements

Portions of this study were sponsered by grants AT(38-1)-777 from the Atomic Energy Commission and R 80 2928-01-l from the Environmental Protection Agency, awardedto R. G. Zingmark.

We would like to thank the faculty, staff and students ofthe Belle W. Bamch Institute for Marine Biology andCoastal Research for financial and vocal support andfor the many discussions that enhanced the understan-ding of estuarine processes. Special thanks go to Mr.ehester Sansbury for logistic aids he eagerly supplied.The staff and students of the Department of Oceano-graphy, Dalhousie University, also deserve our applausein the preparation of the manuscript. Dr. Peter Wangers-ky is thanked for criticisms of the final copy.

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Seilner, Zingmark, Miller: The I4C Method of Measuring the Total Annual Production of Phytoplankton 125

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