Biogeochemical influences on the carbon isotope signatures of Lake Ontario biota

Biogeochemical influences on the carbonisotope signatures of Lake Ontario biota

M.F. Leggett, M.R. Servos, R. Hesslein, O. Johannsson, E.S. Millard, andD.G. Dixon

Abstract: Particulate organic matter (POM), zooplankton, and benthic invertebrates were sampled seasonally at amidlake and east basin site in Lake Ontario. The δ13C values of POM samples were compared with measurements ofchlorophyll a concentrations, areal rates of primary productivity, concentrations of dissolved free CO2 (CO2(aq)), and theδ13C of zooplankton and benthic invertebrates. The δ13C of POM was significantly correlated with the concentration ofCO2(aq) at the east basin site. No correlation was found between chlorophyll a concentrations, areal rates of primaryproductivity, and the δ13C of POM. The δ13C of zooplankton was not always similar to the δ13C of the POM fractioncollected, indicative of the complexity of food web interactions within the lower trophic levels. The δ13C of benthicinvertebrates feeding on the sediment surface was similar to that of POM produced prior to stratification, indicating theimportance of the spring bloom as a food source for benthic primary consumers.

Résumé : La matière organique particulaire, le zooplancton et les invertébrés benthiques ont fait l’objet deprélèvements saisonniers dans la partie centrale et le bassin est du lac Ontario. Les δ13C des échantillons de matièresorganiques particulaires (MOP) ont été comparés aux concentrations de chlorophylle a, aux taux surfaciques de laproductivité primaire, aux concentrations de CO2(aq) et aux δ13C du zooplancton et des invertébrés benthiques. Le δ13Cdes MOP présentait une corrélation significative avec la concentration de CO2(aq) au site du bassin est. Aucunecorrélation n’a été décelée entre les concentrations de chlorophylle a, les taux surfaciques de la productivité primaire etle δ13C des MOP. Le δ13C du zooplancton n’était pas toujours semblable à celui de la fraction des MOP prélevées, cequi dénote la complexité des interactions du réseau alimentaire des niveaux trophiques inférieurs. Le δ13C desinvertébrés benthiques s’alimentant à la surface des sédiments était semblable à celui des MOP produites avant lastratification, ce qui montre l’importance de la prolifération printanière comme source de nourriture pour lesconsommateurs primaires benthiques.

[Traduit par la Rédaction] Leggett et al. 2218

Introduction

Carbon isotopes have been used effectively as tracers offood sources in aquatic systems. It has also been suggestedthat the δ13C of sediment and particulates may be used as anindicator of lacustrine trophic status (Gu et al. 1996). Tem-poral changes in the productivity of a lake have beeninferred in paleolimnological investigations from the δ13C oforganic carbon and calcite in sediment cores (McKenzie 1985;

Schelske and Hodell 1991; Hodell and Schelske 1998). Thebasis for these inferences is that the 12C isotope of carbon isused preferentially by algal cells in photosynthesis, leaving adissolved inorganic carbon (DIC) pool enriched in 13C. There-fore, higher productivity is reflected in elevated δ13C in cal-cite and organic carbon produced in the epilimnion (Schelskeand Hodell 1991). It is assumed that the uptake of carbon byprimary producers is the predominant influence on the δ13Cof DIC and therefore the organic carbon produced using DICas a substrate for photosynthesis. A seasonal fluctuation inthe δ13C of DIC and organic carbon, reflecting seasonalchanges in the magnitude of primary production, is pre-dicted. A linear relationship between the concentration ofchlorophyll a (Chl a) and (or) the rate of productivity andthe δ13C of primary producers might also be expected.

The amount and composition of available DIC vary be-tween systems and are influenced by biological processes ofrespiration and photosynthesis as well as equilibrium kinet-ics and atmospheric gas exchange (Herczeg and Fairbanks1987; Aravena et al. 1992). The relative magnitudes of theforms of DIC and the processes influencing the equilibriumbetween components of the lake carbonate system influencethe carbon isotope signatures of particulate organic matter(POM) in two ways. First, the components of the lakecarbonate system, seeking to attain a state of equilibriumchemically, also move toward a state of isotopic equilibrium

Can. J. Fish. Aquat. Sci. 56: 2211–2218 (1999) © 1999 NRC Canada

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Received June 2, 1998. Accepted July 17, 1999.J14630

M.F. Leggett1 and D.G. Dixon. Department of Biology,University of Waterloo, Waterloo, ON N2L 3G1, Canada.M.R. Servos. Environment Canada, National Water ResearchInstitute, 867 Lakeshore Road, Burlington, ON L7R 4A6,Canada.R. Hesslein. Department of Fisheries and Oceans, FreshwaterInstitute, 501 University Crescent, Winnipeg, MB R3T 2N6,Canada.O. Johannsson and E.S. Millard. Department of Fisheriesand Oceans, Great Lakes Laboratory for Fisheries andAquatic Sciences, 867 Lakeshore Road, Burlington,ON L7R 4A6, Canada.

1Author to whom all correspondence should be addressed.e-mail: [email protected]

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(Weiler 1974). Many of the processes influencing the com-position of the DIC pool also serve to alter the δ13C of dis-solved free CO2 (CO2(aq)) and bicarbonate (HCO3

−). The δ13Cof fixed carbon will be determined to some degree by theδ13C of the inorganic carbon used in photosynthesis (Rau etal. 1989; Fogel et al. 1992). Second, the observed level ofisotope fractionation in primary producers is a function ofthe amount of carbon available at the site of activity of theenzyme binding the carbon substrate in carbon fixation (Far-quhar et al. 1982; Fogel and Cifuentes 1993). Isotope frac-tionation is also dependent on the level of isotopicdiscrimination characteristic of the particular enzyme systemused by the cell in carbon fixation (Goericke et al. 1994).

There may be species-specific differences in the δ13C ofprimary producers related to differences in DIC source andcarbon uptake kinetics. Because the isotope signature is afunction of the physical–chemical environment and intra-cellular carbon concentrations, differences in cell size andmorphology, or adaptation to different environments, arelikely to be expressed as variation in the δ13C of differentspecies. This variation would overlay a seasonal shift ofvarying magnitude depending on the system observed. Thezooplankton and benthic consumers feeding on primary pro-duction will have a δ13C that reflects their food source. Tem-poral changes in the carbon signature of primary producersshould be reflected in the signatures of these primary consum-ers. It is therefore important to characterize the baseline signa-ture of the system and the range of signatures in available foodsources in order to effectively use isotope data to make infer-ences on the relative trophic position of different organisms.

Given the number of areas where establishing a baselinehas relevance in the interpretation of isotope data, there arerelatively few studies where the isotope signature of POM ismeasured on a seasonal basis or in relation to system pro-ductivity (e.g., McCabe 1985; Bernasconi et al. 1997). Inthis study, we examined the relationship between seasonalconcentrations of Chl a, the level of photosynthetic produc-tion, and δ13C of POM to determine if the carbon isotopesignature of POM could be directly correlated with theproductivity of the system. Seasonal trends in the δ13C ofzooplankton and benthic invertebrates were measured to de-termine the extent to which the signature of POM was re-flected by primary consumers.

Materials and methods

Two sampling sites in Lake Ontario of the Laurentian GreatLakes were chosen for comparison and a 2-year seasonal study wasconducted. One site was located midlake, Station 41 (43°43′18′′ N,78°01′01′′ N), where the water column has a depth of about 130 m.The other site was in the eastern basin, Station 81 (44°01′00′′ N,76°40′18′′ N), where the water column is about 34 m deep(Johannsson et al. 1998). Terrestrial inputs to the POM were ex-pected to be negligible at both sites. Lake Ontario is a mesotrophiclake with an average pH of 7.8–8.6 and high ambient concentra-tions of DIC (about 1800 µM). The lake stratifies in mid-June andbiologically induced precipitation of CaCO3 occurs seasonally atthe end of July or early August (Lean et al. 1987; Hodell et al.1998). All of the sampling for this project was done in conjunctionwith the Lake Ontario Bioindex biomonitoring program(Johannsson et al. 1998). Samples were collected at Stations 41and 81 every 2 weeks from April 20 to September 27, 1994, andthen again from May 11 to October 31, 1995.

Water samples for nutrient analysis and determination of boththe δ13C of DIC and the CO2(aq) concentration were obtained fromdiscrete 10-L water samples collected with Nisken bottles. Sampleswere taken at 10 m when the lake was thermally homogenous andfrom the midepilimnion once the lake had stratified. Subsamples ofwater from the Nisken bottles were collected in evacuated 250-mLbottles containing KCl as a preservative for carbon isotope andCO2(aq) analyses. Extraction and analyses of these samples wasconducted as per standard methods at the Department of Fisheriesand Oceans, Freshwater Research Institute. On August 2, 1995, du-plicate discrete samples were collected hourly from 3 m depthbetween 6:00 and 22:00 to determine if there was any diurnal fluc-tuation in the δ13C of DIC. DIC samples were also collected onAugust 2, 1995, at depths of 7.5, 12.5, 25.0, 75.0, and 120.0 m; themixing depth on August 2 was 6.5 m.

Samples of POM were obtained from 200 L of water pumpedfrom the midepilimnion through a 44-µm Nitex screen into storagecontainers. Most of these samples were then sequentially filteredthrough 20-µm-mesh Nitex screen and precombusted (500°C)0.7-µm nominal pore size Whatman GF/F glass fibre filters. Theexception was the sample collected on a GF/F filter on May 10,1995, at Station 81, which was not prefiltered through 20-µm-meshNitex screen. Filters and POM collected on 20-µm-mesh Nitexscreens (when available in sufficient mass) were dried at 60°C priorto analysis. In May and June of 1995, at both sites, additional sam-ples were obtained using a Westfalia continuous-flow centrifuge toseparate POM from 200-L samples, collected as described above.POM obtained from the centrifuge was dried at 60°C prior to analysis.

Zooplankton samples were collected from the surface to 1 mabove the start of the thermocline in vertical tows using 64-µm-mesh Nitex nets. Samples were screened to separate zooplanktoninto size categories >110, >210, and >250 µm. Screened sampleswere preserved in ethanol to facilitate speciation and removal ofparticulate and detrital material. Samples of individual specieswere obtained through separation under a microscope. Compositesamples of many hundreds of individuals were then rinsed withdistilled deionized water and dried prior to analysis. Samples ofDiporeia hoyi and oligocheates were obtained in benthic grab sam-ples. Benthic samples were also stored in ethanol rinsed with dis-tilled deionized water and dried prior to analysis. Ethanolpreservation was found to remove isotopically light lipids, increas-ing δ13C signatures by up to 1.5‰ (Leggett 1998).

The rates of areal primary productivity (PP, g C·m–2) reportedhere were determined utilizing 14C uptake in shipboard incubators,as described in Millard et al. (1996). Monthly average values forPP integrated through the epilimnion were used in comparisonswith the δ13C values of POM (Table 1). The relative concentrationsof CO2(aq) and HCO3

− were calculated as described in Leggett (1998).An Optima VG continuous-flow isotope ratio mass spectrometer

(CF-IRMS) was used to obtain the δ13C and δ15N values for all ofthe particulate, zooplankton, and benthic samples. Instrument accu-racy, precision, and range of linearity were monitored with sets ofNational Institute of Standards and Technology U.S.A. standards ofknown concentration and isotope composition including IAEA-CH6, IAEA-N1, and IAEA-N2. Duplicate standards of identicalmass, within the linear range of operation, consistently had mea-sured values within 0.25‰ of each other. All POM samples weretreated with 2 N HCl to remove traces of CaCO3. Subsamples ofcollected material had acid added to them; these samples wereredried at 60°C and analyzed. This procedure was repeated untilsuccessive analyses were identical, demonstrating that all residualCaCO3 had been removed.

Results

The δ13C of DIC was observed to increase about 2.0‰ be-tween April and October at both sites in each of the years

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investigated (Fig. 1). There was no discernible diurnal fluc-tuation in the δ13C of DIC. Duplicate samples, collected atincreasing depths, indicated that the δ13C of hypolimneticDIC was about 1.5‰ lower than that found in the epilimnion(Leggett 1998).

A seasonal shift was observed in the isotope signatures ofPOM in the 1–20 µm size fraction collected on GF/F filters(Figs. 2 and 3). In late May through mid-June, the δ13C ofPOM >20 µm in diameter was enriched in 13C relative to allother size-classes of POM at both sites (Tables 2 and 3). Theδ13C of POM collected on filters (1–20 µm size fraction) atstations 41 and 81 increased about 6‰ from spring mini-mum values. Over the period in the fall when thermal strati-fication breaks down, the δ13C of POM drops back down tounder –30.0‰ at both sites. No correlation between the δ13Cof POM, Chl a concentrations, or the areal rates of PP couldbe determined at either site. There was a negative correlation(r = –0.86, P = 0.002, α = 0.05, df = 10) between the δ13C ofPOM and the concentration of CO2(aq) at Station 81 and be-tween the δ13C of POM and temperature (r = 0.82, P =0.006). At Station 41, the δ13C of POM was not significantlycorrelated with the concentration of CO2(aq), Chl a, or PP.

Differences in carbon signatures were observed dependingon the size fraction of POM collected. Larger size fractionshad a higher δ13C. The discrepancy between size fractionsincreased during the summer months (Tables 2 and 3).

The 110–210 µm fraction of zooplankton collected wasmade up of nauplii, smaller copepodids, rotifers, and somebosminids in different proportions, depending on the time ofsampling. The 210–295 µm fraction contained bosminids,Daphnia spp., and calanoid and cyclopoid copepods includ-

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Leggett et al. 2213

Fig. 1. δ13C of DIC in surface water at (A) Station 41 in 1994(crosses) and 1995 (triangles) and (B) Station 81 in 1994(crosses) and 1995 (triangles).

Fig. 2. Seasonal trends at Station 41 in 1995: (A) δ13C of POM(1–20 µm size fraction) in relation to the δ13C of different sizefractions of zooplankton (crosses, >110 µm; circles, >210 µm;triangles, >295 µm, (B) surface water concentrations of Chl a andPOC, and (C) surface water concentrations of HCO3

− and CO2(aq).

Fig. 3. Seasonal trends at Station 81, 1995: (A) δ13C of POM(1–20 µm size fraction) in relation to the δ13C of different sizefractions of zooplankton (crosses, >110 µm; circles, >210 µm;triangles, >295 µm, (B) surface water concentrations of Chl a andPOC, and (C) surface water concentrations of HCO3

− and CO2(aq).



ing Diacyclops thomasi. All of the size fractions containedtrace amounts of phytoplankton that could not be removedby filtration (Figs. 2 and 3).

The δ13C of zooplankton samples collected in the springthrough early summer reflected the δ13C of the POM col-lected on GF/F filters (Figs. 2 and 3). In late summer at Sta-tion 41, there was a 4‰ difference in δ13C between thezooplankton samples collected and the 1–20 µm size fractionof POM (Fig. 2). The δ13C of Diporeia hoyi was similar tothe δ13C of POM and zooplankton collected from the epilim-nion in the spring (Table 4). Oligochaetes were enriched in13C relative to the Diporeia hoyi samples collected.

Discussion

The lack of correlation between PP and the δ13C of POMon a seasonal basis suggests that photosynthetic uptake isnot the sole determining factor of δ13C of DIC and POM inLake Ontario. The δ13C of the POM collected also likely de-pends on the mode of uptake and source of carbon availableto the algal cells present.

The observed 2.0‰ change in δ13C of DIC in Lake On-tario (Fig. 1) is hypothesized to be a function of a shrinkingpool of available CO2(aq), which is also becoming enrichedin 13C. The low level of seasonal change in the δ13C of DIC,relative to the fluctuation observed in POM, may be attrib-uted to the system’s alkalinity and the magnitude of the poolof DIC available in Lake Ontario.

The measured carbon isotope signature of DIC is an inte-gration of all of the carbon molecules making up the totalpool of available DIC. As most of the DIC is HCO3

−, theδ13C of DIC is dominated by the δ13C of HCO3

−. This par-tially explains the observed seasonal stability of the δ13C ofDIC in relation to the δ13C of POM. While the δ13C ofCO2(aq) and the δ13C of HCO3

− are both likely to shift on aseasonal basis, the δ13C of HCO3

− will be fairly stable, sinceconcentrations of HCO3

− remain relatively high. Therefore, alarge amount of carbon has to be exchanged in order to get ashift in the δ13C of the entire pool of DIC. In addition, theequilibrium between CO2(aq) and HCO3

− is the predominantmechanism for exchange of carbon isotopes in the HCO3

−

pool. Therefore, changes in the signature of HCO3− have to

be produced as a result of changes in the δ13C of CO2(aq) and(or) changes in the fractionation associated with the equili-

bration of CO2(aq) and HCO3− (Mook et al. 1974; Marlier and

O’Leary 1984). The δ13C of CO2(aq) in the system is moresusceptible to change because the concentration is smallerand there are a number of physical, chemical, and biologicalprocesses influencing both the concentration and the δ13C ofCO2(aq). It is predominantly CO2(aq) that is used as a sub-strate for photosynthesis, and therefore, shifts in the concen-tration and the δ13C of CO2(aq) are reflected in the δ13C ofPOM.

The temperature of the lake in April or early May is usu-ally between 2 and 4°C, which is near the seasonal mini-mum (Johannsson et al. 1998). Colder winter temperaturesenhance CO2(aq) solubility so that CO2(aq) contributes moresubstantially (5.3% as opposed to 0.3% midsummer) to aslightly larger DIC pool (about 1900 µmol C·L–1 as opposedto 1500 µmol C·L–1). The elevated concentration of CO2(aq)results in a DIC pool with a lower δ13C, since CO2(aq) is de-pleted in 13C relative to HCO3

−. The –2.2‰ signature forDIC measured in the spring represents a seasonal low.

The lake does not freeze over the winter and CO2(aq) isfree to exchange with atmospheric CO2. In the winter andearly spring, Lake Ontario is supersaturated with CO2 andacts as a source of CO2 to the atmosphere, losing between 2and 3 g C·m–2·day–1 (Weiler 1974). CO2 exchange across theair–water interface will act to push the δ13C of CO2(aq) to-ward –8.0‰, the value for the δ13C of atmospheric CO2(Keeling et al. 1979). Given the net flux of CO2 from thewater column, it is unlikely that isotopic equilibrium existsbetween CO2(aq) and atmospheric CO2.

The onset of spring and subsequent warmer temperaturescoincides with elevated levels of primary production. TheCO2(aq) pool is used preferentially as a source of carbon forprimary producers, and concentrations of CO2(aq) start to fall.Isotopically light carbon is drawn out of the CO2(aq) pool asthe heavier isotope of carbon is discriminated against by theenzyme systems active in carbon fixation. With rising tem-peratures and an increase in primary production, there is anincrease in the pH of the system and a resulting decrease inthe solubility of CO2(aq). By the time the lake is thermallystratified in mid-June, the concentration of CO2(aq) hasdropped from >70 to <10 µM. Continued removal of CO2(aq)leads to a reversal in the exchange of CO2 with the atmo-sphere as the system becomes a sink for atmospheric CO2.The combination of these processes is at least partially re-

© 1999 NRC Canada


Station 41 Station 81

Time period Empirical solar Cloudless solar Empirical solar Cloudless solar

Season 132.8 181.3 151.1 193.9Stratified period 84.0 115.9 107.6 136.5May 27.1 35.7 21.6 27.3June 24.7 33.0 20.7 25.3July 17.9 25.8 25.1 31.7Aug. 24.4 32.3 39.5 48.8Sept. 24.6 33.2 25.6 33.1Oct. 14.1 21.3 18.6 27.8

Note: The monthly PP rates were calculated for both empirical and theoretical cloudless (maximum) levels of solarirradiance. The stratified period for Station 41 was June 19 – October 16 and for Station 81 was June 24 – October 20.

Table 1. Areal rates of photosynthesis (g C·m–2·month–1) at Stations 41 and 81 determined from the results ofshipboard incubation of water samples with 14C addition.



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20–44 µm 0.45–44 µm 1–20 µm

Date δ13C δ15N n C/N δ13C δ15N n C/N δ13C n δ15N n C/N

May 11 10.01 –28.4±2.38 7.18±0.83 9 5.51 –30.46±0.90 5 11.44±0.49 6 6.08June 7 –23.11 3.39 2 9.67 –26.36±0.93 4 7.58±0.35 7 6.91June 16 –26.25±0.09 3 4.18±0.57 3 8.77June 19 –26.51±0.74 1.90±2.39 6 7.50 –29.4±0.95 3.70±0.66 7 6.62 –28.92±1.11 3 4.28 1 7.02June 21 –26.90 0.71 1 7.72 –27.8±0.47 2.53±0.20 8 9.35 –27.57±0.97 3 3.51±0.19 3 7.97June 29 –22.43 7.54 2 5.93 –24.49±0.65 4 4.59±0.59 7 7.17July 15 –18.70 7.08 2 –23.86 2 5.55±0.26 4 9.85Aug. 1 –21.85±2.22 8.49±1.66 3 8.73 –26.83 2 4.22±0.42 5 9.49Aug. 30 –26.93±0.89 3 5.68 1 6.41Sept. 21 –27.36 2 7.57±0.64 3 6.72Oct. 5 –27.08±0.54 3 7.96±0.36 4 6.85Oct. 23 –25.05 9.08 2Oct. 30 –30.26±0.78 4 10.02±0.63 5 7.95

Note: The samples were collected as follows: 20–44 µm, on Nitex screens; 0.45–44 µm, with a Westfalia centrifuge; 1–20 µm, on glass fibre filters after prefiltering through 44- and 20-µm-meshscreens.

Table 2. δ13C, δ15N (±SD), and the C/N ratio of POM samples collected at Station 41 in 1995.

20–44 µm 0.45–44 µm 1–20 µm

Date δ13C δ15N n C/N δ13C δ15N n C/N δ13C n δ15N n C/N

May 10 –29.3±0.76 4.41±0.59 9 7.16 –29.01±0.28 5 4.73±0.26 5 9.13June 6 –28.73±0.66 3 8.53±0.63 3 7.68June 15 –28.18±1.02 4 5.01±0.30 3 8.98June 20 –27.40 4.77 2 10 –29.4±0.77 4.01±0.46 11 7.98 –28.67±0.62 3 3.54±0.32 3 6.62June 28 –27.38±0.54 3 4.52±0.30 3 7.55July 14 –25.83±0.33 3 4.29±0.81 6 8.21Aug. 2 –19.03 6.36 2 11 –26.50±0.71 3 5.23±0.75 6 8.26Aug. 15 –24.28 2Aug. 29 –25.71±0.42 3 7.26±0.42 4 7.49Sept. 11 –25.83±0.88 3Oct. 4 –27.79±1.24 3 7.81±0.28 3 6.38Oct. 20 –25.17±0.73 8.31 3 5Oct. 30 –31.72 2 11.84 1 8.23

Note: The samples were collected as follows: 20–44 µm, on Nitex screens; 0.45–44 µm, with a Westfalia centrifuge; 1–20 µm, on glass fibre filters after prefiltering through 44- and 20-µm-meshscreens.

Table 3. δ13C, δ15N (±SD), and the C/N ratio of POM samples collected at Station 81 in 1995.

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sponsible for the observed increase in the δ13C of DIC in theepilimnion, from –2.2 to –0.5‰, where it remains for muchof the summer. As the CO2(aq) pool shrinks and becomesmore enriched in 13C, the process of equilibration betweenCO2(aq) and HCO3

− becomes faster, as there is less carbon inthe CO2(aq) pool to turnover and less total DIC in the system.The isotopic equilibrium, such that it exists, is shifted andsubsequently, both CO2(aq) and HCO3

− become more isotopi-cally enriched. At higher temperatures, the carbon isotopefractionation of CO2(aq), with respect to dissolved HCO3

−, isless pronounced (–8.97‰ at 25°C) (Mook et al. 1974). Inaddition to the biological and chemical kinetic influences,the influx of atmospheric CO2 maintains the low levels ofCO2(aq) at near-equilibrium concentrations (Boston et al.1989). The concentration of CO2 added from the atmosphereis larger than that from epilimnetic respiration and the entirepool is circulated very rapidly. Therefore, this source mayalso serve to stabilize the δ13C of CO2 (aq) at about –8.0‰,the air–water equilibrium value. Under conditions wherethere is an influx of atmospheric CO2, the δ13C of POM isnot as susceptible to enrichment by primary producers, sincethe concentration of CO2(aq) is maintained by a source ofcarbon that is isotopically light relative to HCO3

−.In the hypolimnion, where primary production is not a

significant factor influencing the DIC pool, respired CO2from sediment/fauna and colder temperatures maintain aDIC pool that is depleted in 13C relative to epilimnetic DIC.There is little or no mixing of hypolimnetic and epilimneticCO2(aq) so that atmospheric CO2 is not a mitigating factor.When the lake turns over in the fall, there is mixing ofepilimnetic and hypolimnetic DIC. This addition of 13C-

depleted DIC, along with cooler fall temperatures andCaCO3 precipitation, boosts the concentration of CO2(aq)available to primary producers and results in a decline in thecarbon isotopic signatures of DIC and POM. The observeddecline would be expected to continue into the winter untilthe lake again reaches a point where the it attains a balanceand a resulting δ13C signature of about –2.2‰ for DIC.

The high δ13C of POM while the lake is stratified canmost easily be attributed to an increase in the δ13C of CO2(aq)and (or) a reduction in the level of isotope fractionation byprimary producers due to reduced concentrations of avail-able CO2(aq). Alternatively, the elevated signatures may bedue to the active uptake of DIC or the facilitated conversionof HCO3

− to CO2(aq) by primary producers (Kaplan 1985).These mechanisms are most likely to be active under condi-tions of CO2(aq) limitation, since the active uptake of HCO3

−,or the facilitated conversion of HCO3

− to CO2(aq), has an at-tached energetic cost that must be overcome before any netbenefit is derived (Raven and Lucas 1985). The concentra-tions of CO2(aq) in Lake Ontario are probably sufficient fordiffusive uptake of CO2 to meet the carbon requirements fora majority of the primary producers (Leggett 1998). How-ever, it is possible that some species may find it advanta-geous to use HCO3

− to meet their photosynthetic demands.For lakes of high alkalinity (1.5–3.0 mequiv.·L–1), such asLake Ontario, the pH range 8.1–8.3 also represents an air-equilibrium state. As a result, these lakes may be more sus-ceptible to pH elevation and CO2 depletion (Talling 1985).

The direct assimilation of HCO3− by Lake Ontario pico-

plankton has previously been observed in 14C addition ex-periments (Caron et al. 1985). Boundary layer effects,

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Diacyclopsthomasi

Calanoidcopepods Bosmina spp. Daphnia spp. Diporeia hoyi Oligocheates

Date δ13C n δ13C n δ13C n δ13C n δ13C n δ13C n

1994Apr. 20 –28.45 8 –23.68 2May 12 –27.63 2 –26.28 1May 26 –28.01 2 –26.39 1June 6 –27.60 1 –26.58 2 –26.61 3 –24.54 2June 30 –25.15 5 –26.48 1 –24.43 2July 14 –24.23 1 –22.89 2 –26.95 7July 28 –21.67 1 –22.93 1Aug. 11 –22.69 2 –22.42 2 –23.49 1 –27.21 2 –22.58 4Aug. 29 –21.78 3 –24.36 2 –23.18 4Sept. 27 –23.64 2Oct. 6 –21.60 1 –22.85 1 –22.76 2 –24.40 1Oct. 13 –23.01 3 –22.99 1 –27.15 6 –24.18 3

1995May 11 –28.52 2 –29.07 2June 16 –25.34 6 –25.15 1 –25.47 2June 21 –25.05 1 –24.91 1 –26.04 2June 29 –25.38 1Aug. 1 –23.58 2 –24.95 1 –24.44 3 –25.17 1Aug. 30 –21.11 1Sept. 26 –22.81 1 –29.00 1 –24.49 1 –24.01 1Oct. 23 –27.11 1 –24.48 1 –25.93 1

Note: All samples are composites. Zooplankton was sampled from 20 m to the surface when the lake was mixed and from the midepilimnion to thesurface when the lake was thermally stratified.

Table 4. δ13C of individual species of zooplankton and benthic invertebrates collected at Station 41.



limiting CO2(aq) at the cell surface, or low CO2 to O2 ratiosin the cell may also induce some species of primary produc-ers to use compensating mechanisms for carbon uptake(Prins and Elzenga 1989; Tsuzuki and Miyachi 1989). Thismay explain some of the variability in the δ13C of differentsize fractions of POM collected. The observed differencesare possibly a function of species-specific differences in up-take and fractionation of carbon isotopes. The sample mayinclude algae using HCO3

− as a carbon source. Hodell andSchelske (1998) noted the high concentrations ofchoococcoid cyanobacteria in Lake Ontario in late summeras potentially having a role in calcite formation. Synecho-coccus can use HCO3

− as a source of carbon-producinghydroxyl ions, which could induce calcite formation.

The enriched δ13C of the zooplankton collected in latesummer at Station 41 suggests a food source other than thePOM collected on the filters. This could reflect feeding onalgae that are using an enriched source of carbon such asHCO3

−. Alternatively, the elevated zooplankton signatures inlate summer may be a lag from the elevated signatures ofPOM generated earlier in the season. The carbon from POMrecycled through bacteria and mesotrophic algae feeding onbacteria may remain in the system for a longer period oftime. Sources of organic carbon (particulate organic carbon(POC)) other than photosynthetic algae, indicated by theconcentration of Chl a, are elevated in late summer and mayplay a significant role in sustaining secondary production inthe system (Fig. 2).

The δ13C signatures of the Diporeia hoyi collected atStation 41 indicate the importance of production early in theseasonal cycle in sustaining benthic primary consumers (Ta-ble 4). Diporeia hoyi will feed on POM at the sediment sur-face, and their δ13C will reflect the δ13C of the bulk of thePOM available. Signatures of Diporeia hoyi increase slightlyas the season progresses but remain consistently below val-ues for epilimnetic POM, produced after the lake has strati-fied. In contrast, the oligochaetes collected had a higher δ13Cthan most of the POM samples measured in this study. Oli-gochaetes feed on bacteria and organic detritus below thesediment surface: the original source of organic carbon isprobably identical to that consumed by Diporeia hoyi.Therefore, the difference between the Diporeia hoyi andoligochaete signatures may be attributed to diagenesis ofsurficial sediment. Alternatively, the discrepancy may be anindication of different dietary sources of carbon.

ConclusionsThe results of this study suggest that a seasonal fluctua-

tion in the δ13C of POM is largely influenced by the algal re-sponse to the ambient concentration of CO2(aq) and also thatthe δ13C of POM may not necessarily be an effective indica-tor of productivity in all circumstances. There are a numberof processes influencing the δ13C of DIC and POM at anypoint in the season. The δ13C observed depends on whichprocess is dominant at any given time. Any relationship be-tween the δ13C of POM, levels of productivity, Chl a, or theδ13C of DIC is likely to be system and season specific de-pending on the processes controlling CO2(aq). The range inδ13C of different size-classes of POM at different times alsosuggests a species-specific relationship between the δ13C,availability of CO2(aq), and the δ13C of the organic carbon

produced. Therefore, using the δ13C of organic carbon insediment may not always be a robust means of inferring pastproductivity in lacustrine systems.

An understanding of system biogeochemistry and poten-tial for change and variability in the δ13C of primary produc-ers should be an intrinsic part of any study where carbonisotopes are used to make inferences regarding carbonsource in aquatic systems. In this study, the δ13C of primaryconsumers reflected the source of carbon available to themat any particular point in time. Characterization of the sea-sonal pattern in POM therefore provided some insight intothe relative importance of primary production at differenttimes during the season to benthic and pelagic primary con-sumers. Since a number of factors influence the carbon sig-nature of POM on a temporal basis, and are not likely to beconsistent between systems, it is difficult to make inferencesas to the food source of organisms without characterizing thevariability in potential food sources.

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Biogeochemical influences on the carbon isotope signatures of Lake Ontario biota

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