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Organic carbon biogeochemistry of LakeSuperiorJames B. Cotner a , Bopaiah A. Biddanda b , Wataru Makino c &Edward Stets aa Department of Ecology Evolution and Behavior 1987 Upper BufordCircle University of Minnesota , St. Paul, MN, 55108b Annis Water Resources Institute Grand Valley State University , 740West Shorelinec Graduate School of Life Science Tohoko University Aramaki AzaAoba , Sendai, Japan , 980-8578Published online: 16 Aug 2010.

To cite this article: James B. Cotner , Bopaiah A. Biddanda , Wataru Makino & Edward Stets (2004)Organic carbon biogeochemistry of Lake Superior, Aquatic Ecosystem Health & Management, 7:4,451-464, DOI: 10.1080/14634980490513292

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Organic carbon biogeochemistry of Lake SuperiorJames B. Cotner,1∗ Bopaiah A. Biddanda,2 Wataru Makino,3

and Edward Stets11Department of Ecology, Evolution and Behavior, 1987 Upper Buford Circle, University of Minnesota, St. Paul, MN 55108

2Annis Water Resources Institute, Grand Valley State University, 740 West Shoreline Dr. Muskegon, MI 494413Graduate School of Life Science, Tohoko University, Aramaki Aza Aoba, Sendai, Miyagi 980-8578, Japan

∗Corresponding author: Tel: 612-625-1706; Fax: 612-624-6777; E-mail: cotne002@umn.edu

We examined the organic carbon budget for the Earth’s largest lake, Lake Superior, in the Laurentian GreatLakes. This is a unique, ultra-oligotrophic system with many features similar to the oligotrophic oceanic gyres,such as dominance of microbial biomass and dissolved organic carbon in biogeochemical processes. Photo-autotrophy is the dominant source of reduced organic matter in the lake. Areal rates of primary productionare among the lowest measured in any aquatic system, and are likely a result of cold water temperaturesand low nutrient concentrations in the lake. Allochthonous riverine organic carbon inputs were estimated atabout 10 percent of photo-autotrophic production. Atmospheric carbon deposition has not been measured to anysignificant extent but we estimate it at 0.16 to 0.41 Tg yr−1. All together, allochthonous carbon sources provide 13to 19 percent of photo-autotrophic production. The main loss of organic matter in the lake is through respirationin the water column. Respiration is double all estimated organic carbon sources combined and therefore sourcesare likely underestimated. Few measurements of photo-autotrophic carbon production have been made andnone recently. Nonetheless, most of the production and fluxes in this system pass through the large dissolvedorganic carbon pool (more than 10 times as large as the particulate organic carbon pool), which is mediatedby heterotrophic and autotrophic picoplanktonic microbial flora. Improved understanding of dissolved organiccarbon pools and dynamics is critical for constraining carbon flux in ultra-oligotrophic Lake Superior.

Keywords: respiration, heterotrophic bacteria, budget

Introduction

Lake Superior is the world’s largest lake by surfacearea (82,100 km2; Herdendorf, 1990) and is one of thedeepest in North America with a maximum depth ofover 400 m (Hecky, 2000). It contains approximately10% of the Earth’s surface freshwater (12,230 km3)and it is an important natural and economic resourceto the Great Lakes region, providing a clean, abundantwater source to the communities near the lake as well asa relatively inexpensive means of transportation. Also,the large size and thermal inertia associated with it haveimportant effects moderating the regional Great Lakesclimate (Booth et al., 2002).

Key to understanding the behavior of any lake is itsrelationship with its surrounding watershed. The ratioof the drainage area of the watershed to the Lake Su-perior surface area is ca. 1.55, an extremely low valuefor a lake. For comparison, Lake Michigan has a water-shed to lake surface area ratio of ca. 2 and Lakes Huron,Erie and Ontario are all greater than 3. Impoundmentstypically have watershed area to lake surface area ra-tios that are greater than 100 and often greater than200:1 (Wetzel, 2001). One implication from this lowratio in Lake Superior is that the lake is far less in-fluenced by the surrounding watershed than most lakesand there is a strong influence from the ‘airshed,’ whichencompasses a much larger area. This is particularly

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Aquatic Ecosystem Health & Management, 7(4):451–464, 2004. Copyright C© 2004 AEHMS. ISSN: 1463-4988 print / 1539-4077 onlineDOI: 10.1080/14634980490513292

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evident in that contaminants such as polychlorinatedbiphenyls and mercury are problematic in Lake Su-perior and the predominant source for these contami-nants is atmospheric deposition, often from extremelyremote regions (Jeremiason et al., 1994; Hornbuckleet al., 1995; Strandberg et al., 2001). Increased nitrateconcentrations in Lake Superior in the last one hundredyears are also likely a product of atmospheric deposi-tion into the lake (Ostrom et al., 1998). The increasedimportance of airshed dynamics and decreased signif-icance of riverine inputs in Lake Superior make it andother large lakes a reasonable model for allochthonousinputs into the ocean. With two-thirds of the Earth cov-ered with oceans, a similar calculation of the watershedto basin surface area yields a value of 0.42.

Despite the significance of the lake from both lim-nological and economic perspectives, it has been lit-tle studied, in part owing to its remote location andthe low human population around the lake (<1 mil-lion in the watershed). A dedicated issue of the Jour-nal of Great Lakes Research in 1978 provided basicdata on sedimentation (Kemp et al., 1978), climatol-ogy (Phillips, 1978), physical (Bennett, 1978), chemi-cal (Weiler, 1978) and biological limnology (Munawarand Munawar, 1978).

The purpose of this paper is to synthesize currentknowledge about organic carbon (OC) cycling in thislake. Given its large size and the ultra-oligotrophic con-ditions, it represents a ‘trophic end-member.’ The cur-rent effort has a distinctively ‘microbial’ flavor to it.This is because biomass and biogeochemical processesin Lake Superior, as well as other oligotrophic systems,are skewed toward the smallest, microbial organisms(Biddanda et al., 2001; Cotner and Biddanda, 2002).

Sources and fate of carbonin Lake Superior

Sources

Primary production is the main source of organicmatter to the Lake Superior water column and stableisotope studies support this observation (Keough et al.,1996; Ostrom et al., 1998). However, this importantflux is not well-constrained. The only available esti-mates were made decades ago (Vollenweider et al.,1974; El-Shaarawi and Munawar, 1978) before theadvent of ultra-clean techniques for making pro-ductivity measurements in oligotrophic systems. Thestudies that have been performed indicated produc-tivities varying from ca. 0.1 to 5 mg C m−3 hr−1

Table 1. Comparison of some large lakes ofthe world in terms of their annual primary pro-ductivity. Data are from Hecky (2000).

Annual productionLake (g C m−2 yr−1)

Erie (East) 160Ontario 170Huron 100Michigan 150Superior 65Malawi 240Tanganyika 290Victoria 1500

(Vollenweider et al., 1974; El-Shaarawi and Munawar,1978; Fee et al., 1992) and areal production of ca.65 g C m−2 yr−1 (Table 1, Hecky, 2000), but perhapsas high as 100 g m−2 yr−1 (Vollenweider et al., 1974).Extrapolating these values to the entire basin indicatethat ca. 5.3 to 8.2 × 1012 g C are produced by photo-autotrophic production in the lake.

These areal rates are among the lowest rates of pri-mary production measured in any aquatic systems. Pro-ductivity in Lake Superior is lower by nearly a factorof two relative to Lake Huron and nearly 3 times lessthan the eastern basin of Lake Erie and ca. 5 timesless than the western basin of Erie (Vollenweider et al.,1974). Even the oligotrophic oceanic gyres have muchhigher rates of productivity than those measured so farin Lake Superior. For example, at the Hawaii OceanicTime-Series site, productivity is approximately 150 to350 g C m−2 yr−1 (Karl et al., 1998).

Low mean temperatures and low light levels havea lot to do with the low rates of production observedin Lake Superior especially when rates are comparedwith the semi-tropical gyres of the ocean (Karl et al.,1998) or tropical lakes (Table 1). Lake Superior oc-curs at 46 to 49◦ latitude so light impinging on thelake is extremely variable seasonally and low in thewinter. Despite relatively high light levels in the sum-mer months, the lake water heats up little, providingan additional constraint to phytoplankton growth. Themean annual temperature in Lake Superior is a chilly3.64◦C and varies from less than 2◦C in March to nearly6◦C in September/October (Bennett, 1978). Maximumwater temperature observed by Bennett (1978) was16◦C but recent data indicate higher values than thisand suggest that the lake is heating up (E. Ralph,Univ. Minnesota, Duluth, MN; pers. comm.) whichis consistent with regional meteorological data and

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output from general circulation models (Sousounis andGrover, 2002). Nonetheless, such low temperatures inthe lake are due primarily to the high latitude and largevolume of the lake. The mean depth of Lake Superioris 150 m whereas the other Laurentian Great Lakes areall less than 100 m (Bennett, 1978).

Although much less important than in situ produc-tion, riverine systems generate another major flux oforganic matter into the basin. Again, this value is notvery well constrained, primarily because there are fewmeasurements of OC concentrations in rivers feed-ing Lake Superior. The values for OC loading intoLake Superior in Table 2 are based on mean river-ine flow into the lake and estimates of OC from themean OC load in rivers world-wide (Meybeck, 1982)or from OC measurements made in tributaries to south-ern Lake Michigan (Biddanda and Cotner, 2002) whichwere slightly higher than the world river average butsimilar. Scaling up from riverine OC concentrationsyielded an estimate of loading of 5.4–6.2 × 1011 g yr−1

(Table 2). Maier and Swain (1978) estimated riverineorganic C-loading to Lake Superior from rivers at 4.6to 6.3 × 1011 g yr−1, similar to the values proposedhere. Therefore, loading from tributary streams repre-sents about 10% of the annual total amount of photo-autotrophic production occurring in Lake Superior, anon-trivial value that could potentially ‘tip the scales’toward net heterotrophy (Cole et al., 1994) if it were allconsumed through respiration before being deposited

Table 2. Sources and sinks of organic carbon in Lake Superior.

Source or Sink References Estimate

Atmospheric deposition Eadie et al., 1984; Willey et al., 2000 1.6–4.1 × 1011 g yr−1

River carbon load Streamflow into lake basin (Hecky, 2000) 54 × 1012 l yr−1

Organic matter concentrations in rivers(Meybeck, 1982; Maier and Swain,1978; Biddanda and Cotner, 2002)

10–11.5 mg C l−1

Annual terrestrial organic carbonload

Phytoplankton primary production(Autochthonous carbon)

Annual area-specific phytoplanktonprimary production (Vollenweider et al.,1974; Hecky, 2000)

5.4–6.2 × 1011 g yr−1

65–100 g C m−2 yr−1

Lake area (Hecky, 2000) 82.1 × 1010 m2

Annual phytoplankton primaryproduction

5.3–8.2 × 1012 g C yr−1

Respiration Annual area-specific respiration(Biddanda et al., 2001; McManus et al.,2003)

163–476 g C m−2 yr−1

Annual respiration 1.3–3.9 × 1013 g C yr−1

Burial McManus et al., 2003 0.48–1.5 × 1012 g C yr−1

in the sediments or lost from the system via outflow(see discussion below).

Because of the small watershed to lake surface areain Lake Superior, the atmosphere plays a key role in theC budget of this system, unlike most small lakes. Or-ganic carbon deposition represented about 3% of pri-mary production (5 g C m−2 yr−1) in southern LakeMichigan (Eadie et al., 1984). If a similar quantity isdeposited on the surface of Lake Superior, this wouldgenerate similar amounts of OC import into the lake ascomes in via riverine transport. Willey et al. (2000) re-ported continental rain water dissolved organic carbon(DOC) concentrations that varied between 100 and 200µM C; an assumed average concentration of 150 µMwould deposit 1.2 × 1011 g, assuming precipitation of6.6 × 1010 m3 yr−1 (Maier and Swain, 1978). There-fore, we have constrained loading from between 2 to5 g C m−2 yr−1, providing 1.6–4.1 × 1011 g C yr−1 or26 to 76% of the riverine flux. This range is slightlyhigher than that estimated by Maier and Swain (1978)but they did not include dry deposition in their estimate.The range for both atmospheric and riverine inputs arefrom 7 to 10.3 × 1011 g C yr−1 or about 12 to 19% ofprimary production.

Pools of organic matter in Lake Superior

The organic matter pool in Lake Superior is domi-nated by the dissolved component. Estimates of DOC

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Figure 1. Whole lake water and<1µm pore-size fraction particulateorganic carbon profile for Lake Superior in July 2002. This profilewas taken at Station F (47◦00′N and 91◦30′W).

in the lake vary from 1 to 2.0 mg C l−1 (Baker andEisenreich, 1989; Biddanda and Cotner, 2003;Biddanda et al., 2001) and the ratio of dissolved to par-ticulate organic matter is greater than 10:1 (Biddandaet al., 2001). Therefore, organic carbon in the DOCpool represents from 1.5 to 1.9 × 1013 g C. The partic-ulate organic carbon (POC) values varied from 0.1 to0.5 mg C l−1 in surface waters and are usually less than0.1 mg l−1 in the hypolimnion (Figure 1). Therefore,the POC pool represents only 1.2 to 2.5 × 1012 g C.

A significant proportion of the POC is representedby bacterial carbon in this oligotrophic system. Ata deep station in Lake Superior, bacterial abundancevaried from ∼1.8 × 106 cells ml−1 near the surfaceto ca. 0.5 × 106 cells ml−1 below 50 m where mostof the volume of the lake is (Biddanda and Cotner,2003; Figure 2). However, there is considerable vari-ability in these values even over the course of the sum-mer (Figure 2). Our measurements of the less than1 µm size fraction carbon indicated that 46 to 59%of the POC was in this fraction, which we examined

Figure 2. Profiles of bacterial abundance (106 ml−1) measured atStation F (47◦00′N and 91◦30′W) in July and September 1998.

microscopically and found that it consisted primar-ily of heterotrophic bacteria. Particulate organic car-bon values in the hypolimnion typically vary between50 and 180 µg C l−1 but bacterial carbon only rep-resents about 10% or less of the POC in this regionof the lake. During the thermally stratified summermonths, most of the labile components of the par-ticulate organic matter (POM) produced in the sur-face waters are likely selectively consumed by het-erotrophs in the epilimnion. Consequently, the POMin the hypolimnion may be of reduced food qual-ity for bacteria. Such a nutritional change in sinkingPOM may explain the low bacterial organic carbon(BOC):POC ratio (<0.1) found within deeper wa-ters of the lake during the stratified period. Cho andAzam (1988) also observed similar large variabilityin BOC:POC ratios (0.20–0.60%) in the North Pacificgyre.

Sinks: Net autotrophic or netheterotrophic?

The major loss of organic matter, whether pro-duced autochthonously or allochthonously is through

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Figure 3. Plots showing estimated respiration for whole lake water (plankton respiration in unfiltered water) and the bacterial size fraction(bacterial respiration in <1 µm filtered water). These samples were measured at Station F (47◦00′N and 91◦30′W) in September 1998.

respiration. We have measured surface water respira-tion rates that vary from 15 to 42 µg l−1O2 d−1, andshown that the bulk of the respiration is due to bac-teria in Lake Superior (Biddanda et al., 2001; Fig-ure 3). Surface water rates in summer are typicallymuch higher than the rates measured outside of themixed layer. A recent estimate for Lake Superior hy-polimnetic respiration based on changes in oxygenprofiles in the western arm of the lake during strati-fication indicated mean respiration rates of ca. 8 µgl−1 O2 d−1 (McManus et al., 2003), which is rea-sonable in the context of respiration in the surfacewaters. Their measurement, if relevant to the entirebasin, indicates respiration would consume 163 g Cm−2yr−1, and 1.3 × 1013 g yr−1 assuming a respira-tory quotient (RQ) of 1, but it should be noted thatlower RQs are often measured in aquatic systems, es-pecially if there is significant chemotrophy (Pakulskiet al., 1995). This is a bit of an underestimate rela-tive to the higher rates that we have measured in sur-face waters in summer, but likely overestimates rates inthe winter when photo-autotrophic production, organicmatter, and temperature are all minimized. Nonethe-less, the total organic matter sources to the lake, in-cluding primary production and allochthonous inputs,are only 6–9.2 × 1012 g yr−1, about 50 to 70% of totalrespiration.

The other important loss in the lake is throughburial. Organic carbon deposition is about 0.48 × 1012

(McManus et al., 2003) to 1.5 × 1012 g C yr−1 (Johnsonet al., 1982; Klump et al., 1989). These values are

similar in magnitude to terrigenous riverine inputsand represents about 10 to 30% of primary produc-tion (Table 2). If particulate matter burial is similar tothe amount exported from the euphotic zone, that is,there is little decomposition as it passes through the hy-polimnion, this export efficiency is comparable to thosethat have been measured in other oligotrophic systems(Baines et al., 1994). In their survey of lakes and oceans,Baines et al. (1994) found that oligotrophic lakes, withchlorophyll levels of 1 µg l−1 exported slightly higherpercentages of primary production (ca. 35%) than olig-otrophic oceans at a the same chlorophyll level (ca.15–20%). Due in a large part to the huge pool of or-ganic matter that is dissolved compared to particulateorganic matter, most of the respiration in Lake Supe-rior is supported by DOC. McManus et al. (2003) foundthat the particulate carbon settling into the hypolimnionwas six times less than the total respiration rate andconcluded that dissolved organic matter supported thebulk of organic matter decomposition in this system,unlike other oligotrophic lakes where particulate mat-ter fluxes to deep water are of a sufficient magnitude tosupport deep water respiration (Dymond et al., 1996).In another Lake Superior study, organic carbon fluxesfrom surface waters ranged from 60 to 90 mg C m2 d−1,with only ∼5% of OC settling from surface waters ac-cumulating in bottom sediments (Baker et al., 1991). Asimilar phenomenon has been observed in the SargassoSea, where export of DOC into deep water was compa-rable to the particulate C export in this system (Carlsonet al., 1994).

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The discrepancy between respiratory demands andorganic matter production obviously needs to be ad-dressed in order to balance the C budget for this lake.Numerous studies in the oligotrophic ocean and in lakeshave shown that primary production and respiration donot balance, suggesting that there must be other OCsubsidies to balance the C budget in oligotrophic sys-tems (del Giorgio et al., 1997; Duarte and Agusti, 1998;del Giorgio and Duarte, 2002). However, even includ-ing allochthonous inputs into the C budget of LakeSuperior does not fully balance the budget.

There are a number of reasons for this. An impor-tant reason is that few of the measurements are well-constrained and, therefore, many more synoptic mea-surements need to be made. Another reason for theimbalance in production/allochthonous inputs and res-piration is that most of the respiratory measurementshave been made in the western arm of Lake Superiorwhere there is higher primary production and higherallochthonous carbon inputs relative to the rest of thelake (McManus et al., 2003). Perhaps more impor-tantly, no measurements of respiration have been madein the winter when rates are likely to be lower due tocolder temperatures (Pomeroy et al., 1991; Rivkin andLegendre, 2001; Biddanda and Cotner, 2002). Mea-surements of bacterial respiration in Lake Michiganshowed a positive relationship with temperature, butthis relationship was also dependent on OC availability.

Even doubling DOC loading in both atmosphericand riverine pools would not balance the budget. Theworld average DOC concentration for rivers is ca.10 mg C l−1 (Meybeck, 1982) and many of the riversflowing into Lake Superior have concentrations higherthan this. Average DOC values for the St. Louis Riverwere 22 mg C l−1 and the Baptism River averaged11 mg C l−1, but varied between 6 and 18 mg C l−1

(Maier and Swain, 1978). However, the mean organicmatter concentration coming into the lake would haveto be off by more than a factor of 10 to balance thebudget. It is not likely that atmospheric deposition andallochthonous carbon input by rivers is likely to be un-derestimated by that much.

It seems probable that estimates of primary pro-duction for Lake Superior are underestimated. Hecky(2000) used data from Vollenweider et al. (1974) in es-timating primary production at 65 g m−2 yr−1; how-ever, Vollenweider et al. (1974) suggested that pro-duction could be as high as 100 g m−2 yr−1, whichwould bring the budget closer to being in balance.Indeed, a recent study in Lake Michigan has foundthat the use of standard Niskin and Van Dorn bot-tles to collect water samples inhibits photosynthesis

(Fahnenstiel et al., 2002), suggesting that previous es-timates of primary production in the oligotrophic wa-ters of the Great Lakes may have been systematicallyunderestimated. Another problem is that primary pro-duction measurements have been performed with 14Cincorporation into particulate matter which underesti-mates gross primary production due to algal respira-tion of recently produced organic matter (del Giorgioand Duarte, 2002). In addition, this method does notaccount for organic matter produced and released asDOC (Carlson et al., 1998; Karl et al., 1998). In thesub-tropical Pacific, DOC production was a large partof the total productivity, nearly 50% (Karl et al., 1998).Therefore, it is probable that a large proportion ofprimary production is excreted by extremely nutri-ent limited phytoplankton in high-light environmentssuch as in the mixed layer of sub-tropical gyres andLake Superior, especially in summer. There is a largebody of evidence indicating that healthy phytoplank-ton are capable of excreting recently fixed photosyn-thate but the process is still poorly understood (Fogg,1983; Karl et al., 1998). The process is most likelya passive diffusion of low molecular weight organiccompounds that would be accentuated by cells with ahigh surface to volume ratio, such as the small cellsabundant in oligotrophic systems. In a literature sur-vey, excreted OC represented an average of 13% ofprimary production and did not indicate that this per-centage increased consistently in oligotrophic oceans(Baines and Pace, 1991). However, in eutrophic lakes,excreted OC was relatively constant suggesting thatproportionately more OC was excreted in oligotrophicsystems.

Another possible reason for an imbalance in produc-tion and respiration estimates is that there is a temporaldisequilibrium between production and decompositionin Lake Superior. This was first suggested as a possi-ble explanation for excess bacterial C-demand season-ally in Lake Michigan relative to primary production(Scavia and Laird, 1987) and was recently re-examinedin that system (Biddanda et al., 2001; Biddanda andCotner, 2002). In the latter work it was shown thatDOC accumulated in the system in winter/spring dueto intense primary production and increased springrunoff, and is subsequently drawn down in the summerto satisfy increased decomposition and bacterial car-bon/respiratory demand at that time. We have recentlyobserved similar seasonal changes in DOC in Lake Su-perior (Figure 4). At three of four sites and especially inopen water, there was a decrease in integrated epilim-netic DOC from July to September. This idea of tem-poral disequilibrium in DOC concentrations could also

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Figure 4. Dissolved organic carbon (DOC) drawdown in Lake Su-perior. The drawdown was estimated from two cruises in 2002 (Julyand September) and the drawdown is the mean difference in inte-grated epilimnetic DOC between these two dates. Sites were on atransect from a site near Duluth Harbor (46◦43′N, 91◦59′W) out intothe western arm of the lake (furthest point from harbor: 46◦52′N;91◦44′W).

apply to long-term processes, decades to centuries. Forinstance, if primary production exceeded respirationfor a long period of time, DOC concentrations couldbuild up in the lake and subsequently be drawn down inlatter years if respiration exceeded production for a longperiod of time (del Giorgio and Duarte, 2002). The firsthalf of the 20th Century was cooler than the latter halfin the Great Lakes region (Bolsenga and Norton, 1993)and photosynthesis is less temperature dependent thanrespiration (Pomeroy and Wiebe, 1988), perhaps pro-viding a mechanism for DOC to accumulate.

What happens to organic matterin Lake Superior?

Hedges et al. (1997) addressed the question of thefate of terrestrial organic matter in the ocean and wehave paraphrased their title here. Our focus is on thefate of DOM in the world’s largest lake, including bothterrigenous and autochthonous organic matter.

We can estimate the mean residence time of organicmatter in Lake Superior using the rates of primary pro-ductivity and river and atmospheric deposition rates.If we assume that the organic carbon pools are not in-creasing or decreasing, we estimate a residence time fororganic matter in the water column of 26 to 36 years.Because most of the organic matter is in the DOM pool,it would be valuable to have an estimate of the meanage of this pool in the lake. However, there are no such

estimates for this lake or any of the Laurentian Greatlakes (B. Eadie, NOAA-Great Lakes EnvironmentalResearch Laboratory, Ann Arboar, MI; pers. comm.).Similar measurements in the ocean have shown thatdissolved organic matter has a much older 14C-age (ca.4000 years; Williams and Druffel, 1987) than the res-idence time of the ocean (ca. 1000 years), suggestingeither that some pool of the dissolved organic mat-ter is extremely recalcitrant to decomposition or thata pool of very old organic matter is deposited into theocean from terrestrial sources. Recent measurementsof the 14C-age of organic matter in rivers discharg-ing into the Western Atlantic Ocean demonstrated thatDOM in these rivers was extremely variable, with agesestimated at anywhere from modern to >1300 years(Raymond and Bauer, 2001). This provides evidencethat some very old organic matter can be delivered tolentic systems.

Alternatively, relatively old organic matter ages maybe due to selective preservation of organic matter in thewater column. The main vector for DOC decomposi-tion in lakes and the ocean is through bacterial res-piration, as discussed above. This loss increases theturnover rate of DOM, but recent work has shown thatbacterial degradation of organic matter can also gen-erate relatively recalcitrant organic matter that couldincrease the mean age of organic matter in the oceanand presumably in lakes as well (Ogawa et al., 2001).Refractory DOM produced by bacteria in cultures per-sisted for over a year and other work in marine systemshas shown that bacterial D-amino acids are more resis-tant to degradation than bulk DOM (McCarthy et al.,1997).

Another potential source of refractory DOM in lakesis through photo-chemical alteration of organic mat-ter, primarily by UV-A and UV-B near the surface.DOM is responsible for most of the absorption ofsunlight in natural waters (Miller, 1998), especiallythe most oligotrophic ones. Because DOM absorbsUV radiation, it is susceptible to photochemical re-actions. Photochemical degradation of DOC is a sig-nificant flux globally, equivalent to ca. 0.6 to 3% ofthe total DOC pool in the ocean and 20 to 100 timesthe amount of C buried annually (Moran and Zepp,1997; Mopper and Kieber, 2000). Irradiation of river-ine, estuarine and marine waters with simulated naturalsunlight generated dissolved inorganic carbon (DIC)at an average rate of 0.75 µmol C l−1h−1 in sur-face waters (Miller and Zepp, 1995). This observa-tion suggests that photochemical oxidation may animportant sink for DOM in clear, oligotrophic, sur-face waters. However, over an entire water column,

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bacterial respiration remains the dominant oxidationprocess.

Photochemical processes may affect microbial OCconsumption in other, perhaps more complex, waysas well. Interactions between the products of photo-chemical reactions, such as oxygen radicals (Milesand Brezonik, 1981), can also make remaining or-ganic matter more (Lindell et al., 1995; Wetzel et al.,1995; Kieber et al., 1989; Benner and Biddanda, 1998;Moran et al., 2000), or less (Benner and Biddanda,1998; Tranvik and Kokalj, 1998; Anesio et al., 1999;Obernosterer et al., 2001) ‘available’ to bacterial degra-dation. These processes are complex and not verywell understood. Photo-oxidation processes can re-lease inorganic nutrients (Cotner and Heath, 1990;Bushaw-Newton and Moran, 1999), which are likelyto stimulate biological decomposition but other photo-products may directly inhibit bacterial production.Thus sunlight-driven photochemical transformationshave the potential to facilitate or retard decomposi-tion of DOM in natural waters. Nevertheless, only afew studies have attempted to make direct comparisonsbetween photochemical versus microbial utilization ofDOM (Amon and Benner, 1996; Graneli et al., 1996;Opsahl and Benner, 1998).

There are few published studies on photochemi-cal processes in the Laurentian Great Lakes. How-ever, we recently completed several experiments inlakes Michigan and Superior that suggest that photo-oxidation may be an important sink for DOM in thesesystems. Photo-oxidation measurements in Lake Su-perior were ca. an order of magnitude less than thosemeasured by Miller and Zepp (1995; 0.06 µmol Cl−1h−1 in August 2000). One Lake Michigan exper-iment conducted on a transect from the St. JosephRiver in May 2000 showed that riverine water ex-posed to ambient light stimulated higher rates of bac-terial production than the same water incubated in thedark (Biddanda and Cotner, 2003). Nearshore waterwas stimulated less and in offshore water, bacterialproduction was inhibited relative to the dark control.These experiments suggest that terrigenous materialscoming into the lake are highly photo-reactive. It hasbeen argued that more recently produced organic com-pounds, such as algal photosynthate, which is high incarbohydrates, are unavailable to heterotrophic bacte-ria when exposed to sunlight. Older, more humifiedDOM, such as that coming from terrigenous soils, be-comes more available to bacteria upon exposure to sun-light (Benner and Biddanda, 1998; Obernosterer et al.,2001).

In the marine literature, many researchers have con-cluded that surface water DOM is dominated by a rela-tively fresh and labile component, whereas subsurface(aphotic) waters are dominated by relatively old and re-fractory DOM (Williams and Druffel, 1987). Althoughsuch vertical differences in chemical composition ofDOM may be attenuated somewhat in lakes due to theirshallow depth and annual mixing, we demonstrated thatLake Michigan and Lake Superior are characterizedby substantial river to lake, surface to depth, and sea-sonal gradients in DOC reactivity as well as quantity(Biddanda and Cotner, 2003).

Comparisons to other Great Lakes

DOM concentrations do not vary greatly in theGreat Lakes, probably because all of the lakes liewithin a similar climatological and geological wa-tershed (Fahnenstiel et al., 1998). Our measurements(Biddanda et al., 2001; Biddanda and Cotner, 2003)and those of others indicate that mean DOC concen-trations in Superior are ca. 1 to 1.5 mg l−1. SouthernLake Michigan had a slightly higher mean DOC of ca.1.5 mg l−1 (Biddanda and Cotner, 2002). Mean DOC ina survey performed in Lake Erie was 2.7 mg l−1 (Smithet al., 1999a) and 2.2 mg l−1 in Lake Ontario (Jeromeand Bukata, 1998), nearly double that of Lake Superiorand Lake Michigan.

One can get an estimate for the length of time thatorganic matter in a given system is exposed to solar ra-diation by examining the euphotic zone depth and theresidence time of water in a lake. We performed theseanalyses for the Great Lakes and present the results inTable 3. Lake Superior is deepest and the most photo-exposed of all the Great Lakes with an average expo-sure time of lake water at >50 years (Table 3). LakesMichigan and Huron have intermediate levels of lightexposure at tens of years followed by Erie and Ontariowith only 1 to 2 years of exposure. Consequently thereis a gradient in light exposure of DOM from the upperlakes to the lower lakes, which could have significantimpacts on the quantity and quality of organic matterin each lake.

Dissolved organic matterand global change

Several global change issues are relevant to carbondynamics in Lake Superior. Because of its long resi-dence time, any changes due to anthropogenic influence

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Table 3. Index of the potential for photochemical degradation in the Great Lakes relative to each other and the ocean. The indexof photo-exposure was determined as the maximum euphotic zone depth divided by the mean depth times the residence time.

LakeSuperior

LakeHuron

LakeMichigan

LakeErie

LakeOntario Ocean

Max. Euphotic zone (m) 43 31 19 20 27 150Mean depth (m) 147 59 85 19 86 3500Residence time (yr) 191 22 62 2 6 34,000Index of photo-exposure (years) 55.9 11.6 13.8 2.1 1.9 1457

are likely to be manifested for a long time. Given theultra-oligotrophic nature of this lake, it is particularlysensitive to human influence. Human alteration of theearth is substantial and growing (Vitousek et al., 1997).All natural water bodies receive significant inputs oforganic matter and inorganic nutrients from the land(Wetzel, 2001)—and may be considerably influencedby human land use (Daily et al., 2000). For example,runoff of sediments and nutrients from transformedlandscapes are known to cause major changes in down-stream aquatic ecosystems, such as eutrophication andloss of biodiversity (Hecky and Kilham, 1988).

Nutrients

Increased nutrient loading and eutrophication isprobably the greatest threat to the relatively pristinequalities of the Lake Superior ecosystem and its C-cycle. Eutrophication is a global threat to aquaticecosystems (Smith et al., 1999b) and Lake Superior iscertainly one of the most vulnerable ecosystems, due ina large part to the low ambient nutrient concentrations.Small increases in the concentrations of potentially lim-iting nutrients, especially P, which typically limits pro-duction in Lake Superior (Schelske et al., 1972; Sterneret al., 2004) could have large impacts on the whole lakeecosystem.

The most likely cause of increased P input in mostlakes is increased loading due to human populationand especially sewage inputs. Sewage has a relativelylow N:P ratio (Caraco, 1995). This threat, although al-ways a concern, is ameliorated somewhat because ofthe small human population and low human growthrate in the Lake Superior watershed. It is the largestGreat Lake but has the smallest human population atless than 1 million compared to Lake Michigan withnearly 15 million and Lake Erie with over 12 millionhumans in their respective watersheds. The largest mu-nicipality in the Lake Superior watershed is Duluth atca. 250,000 in the metropolitan area and therefore the

greatest potential for P-derived eutrophication is in thewestern arm of the lake. This region is also character-ized by large clay deposits that also contribute signif-icantly to P-loading into the lake (Robertson, 1997).The St. Louis and Nemadji rivers combined contributeca. 10% of the P-load to the entire lake (Robertson,1997).

An unexplored, but perhaps significant flux of P intoLake Superior is atmospheric deposition into the lake.Some earlier estimates have even suggested that up to athird of the total input of P to Lake Superior may comevia atmospheric precipitation (Matheson and Munawar,1978). Phosphorus deposition in dust from the Saharais known to increase P concentrations in the NorthAtlantic gyre (Duce, 1986) and the Mediterranean Sea(Herut et al., 2002; Ridame and Guieu, 2002), but littlework has examined the importance of atmospheric de-position of P in lakes. Non-point sources can be impor-tant sources of both N and P pollution in lakes and thecoastal ocean (Carpenter et al., 1998; Jickells, 1998),providing a mechanism for long-range transport of nu-trients into the lake from remote regions of the up-per Mid-West. Increased P-deposition has been impli-cated as a cause of eutrophication in Sierra Nevadalakes (Sickman et al., 2003). The >25 µmol l−1 in-crease in nitrate concentrations in Lake Superior overthe past century (Bennett, 1986) is a manifestation oflong-range transport and atmospheric deposition in thelake (Ostrom et al., 1998). Similar deposition of P overlong periods of time would have more detrimental ef-fects because of P-limitation in the lake. Decreasedprecipitation and increased dust generation in theUpper Mid-West may exacerbate this problem in thefuture.

Global warming

There are numerous studies showing increasedglobal and regional air temperatures in the past cen-tury and especially in the past several decades. The

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Great Lakes region has not escaped this phenomenonand there is evidence that the Great Lakes are heatingup as well (Assel and Robertson, 1995; McCormickand Fahnenstiel, 1999; Nicholls, 1999; Sousounis andGrover, 2002). Furthermore, Lake Superior has demon-strated increased duration of stratification and in-creased maximum summer time temperatures in thepast decade (E. Ralph, Univ. Minnesota, Duluth, MN;pers. comm.).

A number of papers have been published recentlythat examine the Great Lakes under various climatechange models. Maximum air temperatures in the LakeSuperior basin are predicted to increase by 3 to 5◦C withlittle or no change in precipitation (Mortsch and Quinn,1996). However, most models predict less runoff intothe lakes due to increased evaporation (Argyilan andForman, 2003). Recent analysis of potential changes inmixing and stratification processes in the Great Lakesusing two different general circulation models indi-cated that Lake Superior is likely to be the most stronglyimpacted by global warming (Lehman, 2002). The du-ration of stratification was predicted to increase fromless than 100 days currently to more than 200 days in 90years (Lehman, 2002). The mean mixed layer tempera-ture was also predicted to increase from 5◦C currentlyto 10 to 14◦C in the future (Lehman, 2002). Bottomtemperatures were also predicted to increase from 1 to2◦C. All of these changes will have large impacts onC-cycling in the lake. Climate change and increasedduration of stratification was predicted to decrease pri-mary production in Lake Michigan by as much as 13%in the future. This change was largely attributed to de-creased duration of spring mixing and increased cloudcover (Brooks and Zastrow, 2002).

There are many impacts of increased temperatureon planktonic food web structure (Rhee and Gotham,1981; Fiala and Delille, 1992; Lefevre et al., 1994).We have recently observed a potential interaction be-tween temperature and biomass stoichiometry of bac-teria and plankton (Cotner et al.; unpubl. data). Specifi-cally, we have noted increased C:P and N:P seston ratiosin plankton of both marine and freshwater ecosystemswith increased water temperatures. In chemostats wehave observed that these changes in stoichiometry maybe related to decreased cell-specific rRNA content aswater temperatures increase. Because RNA is relativelyP-rich (ca. 10% P by weight), and rRNA represents alarge part of the P content in most microbes (up to80%), small changes in RNA could have important im-pacts on the P-content and stoichiometry of organisms(Elser et al., 1996). We observed ca. a 25% reductionin RNA content in Escherichia coli K-12 with increas-

Figure 5. Profiles of bacterial abundance (BA) and nucleic acidsin the bacterial size fraction (<1 µm) at Station F (47◦00′N and91◦30′W) in Lake Superior in August 2000. Nucleic acids weremeasured with a fluorescent RiboGreen (Molecular Probes) and amicroplate reader (Makino et al., 2003).

ing temperature (from 20–38◦C), which caused a 33%increase in the C:P ratio.

Our measurements in Lake Superior indicate thatRNA and DNA in bacteria are two of the main nucleicacid pools in the water column (Figure 5) and P inmicrobial nucleic acids is a significant component ofthe total P pool (Figure 6) and therefore, changes intemperature could have important impacts on P cyclingin this system. RNA and DNA in microbial biomass

Figure 6. (A) Estimates of the amount of P associated with RNA,DNA and total nucleic acids in a profile in August 2000 at stationF(47◦00′N and 91◦30′W). (B) We did not measure total P on thiscruise but other measurements at this site have indicated values ofca. 2 µg P l−1 and this value was used to estimate the contributionof the nucleic acids in bacteria to total P in the water column.

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Figure 7. The organic carbon budget for the Lake Superior. Pools are in Tg and fluxes are in Tg yr−1. P is photoautotrophic production andR is respiration.

(<1 µm size fraction) was ca. 4 and 2 fg cell−1 on asummer cruise in the surface waters. Assuming nucleicacids are 10% P by weight and comparing to previousmeasurements of total P in the water (ca. 2 µg l−1), wesee that bacterial nucleic acids represent ca. 20 to 50%of the total and particulate P in the water column. Thebulk of remaining P likely also resides in nucleic acidsbut in particles greater than 1 µm in size.

Lake Superior biomass is already relatively P-deficient with a mean C:P and N:P of 320 and 31, re-spectively (Guildford and Hecky, 2000); increased tem-peratures in the basin in the future are likely to furtherdecrease the food quality in this system, contributing todecreased food web production. However, this impactis fairly speculative because of other potential changesin biogeochemical cycles that accompany changes intemperature. For instance, increased temperatures innearshore regions may contribute to increased P-fluxesfrom the sediments (Nicholls, 1999), perhaps offset-ting increases in biomass stoichiometry with increasedtemperatures.

Recent observations of earlier and increased ampli-tude of water level fluctuations may also have a climatesignature (Lenters, 2001; Argyilan and Forman, 2003).Snowmelt is occurring earlier in the year in most ofthe Great Lakes, including Superior, increasing the po-tential for seasonal sediment resuspension events thathave considerable impact on biogeochemical processesin the nearshore region (Eadie et al., 1996; Cotner et al.,2000).

Conclusions

We summarize the main pools and OC fluxes inLake Superior in Figure 7. The OC budget of Lake

Superior suggests that this lake is ultra-oligotrophic,microbially dominated, and has a large proportionof photo-autotrophic production passing directly intothe DOC pool. Phytoplankton production is the mainsource of organic matter for the lake. AllochthonousOC inputs are a significant portion of the budget inthis large lake ecosystem, representing 12 to 19% ofphoto-autotrophic production. The main sink for or-ganic matter is water column respiration, most of whichis mediated by heterotrophic bacteria. Current esti-mates suggest that losses of organic matter are aboutdouble the inputs, suggesting either that inputs are un-derestimated, losses are overestimated, or the systemis in non-steady state. The most probable explanationis that primary production is underestimated, perhapsdue to an underestimate of synthesized organic matterthat passes directly into the DOC pool.

Acknowledgments

This work was partially supported by US NOAASea Grant (#NA16RG1046), and the US NSF(DEB9977047) and NOAA through their jointly spon-sored program EEGLE (Episodic events Great LakesExperiment #46290000).

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