Stable Isotope (D13c and D15n) Values of Sediment Organic Matter in Subtropical Lakes of Different Trophic Status

J Paleolimnol (2012) 47:693–706 DOI 10.1007/s10933-012-9593-6

ORIGINAL PAPER

Stable isotope (d13C and d15N) values of sediment organic matter in subtropical lakes of different trophic status

Isabela C. Torres • Patrick W. Inglett • Mark Brenner • William F. Kenney • K. Ramesh Reddy

Received: 22 April 2011 / Accepted: 22 February 2012 / Published online: 13 March 2012 Ó Springer Science+Business Media B.V. 2012

Abstract Lake sediments contain archives of past variables yield information about shifts in trophic environmental conditions in and around water bodies status through time, or alternatively, diagenetic and stable isotope analyses (d13C and d15N) of changes in sediment OM. Three Florida (USA) lakes sediment cores have been used to infer past environ- of very different trophic status were selected for this mental changes in aquatic ecosystems. In this study, study. Results showed that both d13C and d15N values we analyzed organic matter (OM), carbon (C), nitro- in surface sediments of the oligo-mesotrophic lake gen (N), phosphorus (P), and d13C and d15N values in were relatively low compared to values in surface sediment cores from three subtropical lakes that span a sediments of the other lakes, and were progressively broad range of trophic state. Our principal objectives lower with depth in the sediment core. Sediments of were to: (1) evaluate whether nutrient concentrations the eutrophic lake had d13C values that declined and stable isotope values in surface deposits reflect upcore, whereas d15N values increased toward the modern trophic state conditions in the lakes, and (2) sediment surface. The eutrophic lake displayed d13C assess whether stratigraphic changes in the measured values intermediate between those in the oligo-mesotrophic and hypereutrophic lakes. Sediments of the hypereutrophic lake had relatively higher d13C and I. C. Torres P. W. Inglett (&) K. Ramesh Reddy d15N values. In general, we found greater d13C and Wetland Biogeochemistry Laboratory, Soil and Water d15N values with increasing lake trophic state. Science Department, University of Florida, 106 Newell Hall, Gainesville, FL 32611-0510, USA e-mail: pinglett@ufl.edu Keywords Eutrophication Nutrients Nitrogen I. C. Torres Microbial processes Stable isotopes e-mail: [email protected] K. Ramesh Reddy e-mail: krr@ufl.edu Introduction

M. Brenner Some of the organic matter (OM) that enters a lake from Department of Geological Sciences, University of Florida, Gainesville, FL 32611-2120, USA the watershed (allochthonous) or is produced within the e-mail: brenner@ufl.edu lake itself (autochthonous) is ultimately deposited on the lake bottom and becomes incorporated permanently into M. Brenner W. F. Kenney the lake sediments. Lakes thus function as sinks for OM Land Use and Environmental Change Institute, University of Florida, Gainesville, FL 32611-2120, USA and associated macro-elements such as carbon (C), e-mail: kenney@ufl.edu nitrogen (N), and phosphorus (P). As a result, lake 123 694 J Paleolimnol (2012) 47:693–706 sediments contain an archive of past environmental Stable isotope signatures of bulk lake sediment OM conditions and biogeochemical processes in and around can sometimes be used to identify impacts of anthro- the water body and lake sediment cores can be used to pogenic activities including wastewater and agricul- document ecosystem changes through time (Smeltzer tural runoff that yield autochthonous OM with low and Swain 1985). Macro-element and OM accumula- d13C and high d15N (Burnett and Schaffer 1980; tion rates in sediments have been studied in conjunction Savage et al. 2004). A stable isotope approach using with stable isotope analyses (d13Candd15N) toinfer past d15N was also used to assess sources of N in Lake environmental changes in marine (Savage et al. Lugano (Terranes and Bernasconi 2000). In that study, 2004), lacustrine (Gu et al. 1996;Bernasconietal. d15N was used to explore N-limitation of algae and N 1997; Hodell and Schelske 1998), and riverine ecosys- uptake by the phytoplankton community. The above tems (McCallister et al. 2004). Measurements of d13C generalizations about d13C and d15N of lake sediment and d15N in dissolved and particulate matter in the water OM may not hold in all cases because a multitude of column and sediments have been used to identify the processes affect OM stable isotope values. For origin of lacustrine OM (Filley et al. 2001), infer past instance, changing relative abundance of terrestrial primary productivity (Hodell and Schelske 1998; versus aquatic OM in sediments across lakes, or within Bernasconi et al. 1997), document historical eutrophi- a lake through time, may complicate interpretations of cation (Gu et al. 1996; Brenner et al. 1999), elucidate relations between primary productivity and bulk biogeochemical cycles (Terranes and Bernasconi 2000; sediment d13C. Furthermore, although wastewater Lehman et al. 2004), and shed light on microbial activity inputs tend to drive d15N values in sediment OM (Hollander and Smith 2001;Guetal.2004; Kankaala higher, many lakes that receive P-rich nutrient et al. 2006). supplements develop N-fixing cyanobacteria blooms. Past studies of stable isotope signatures in lake There is no fractionation in the N-fixation process, and sediment OM enable a few generalizations. Allo- resultant blue-green biomass, i.e. OM, has a d15N chthonous OM usually has more negative d13C values signature near zero (Fogel and Cifuentes 1993). than does autochthonous OM. Values of d13C can Lake sediment OM and macro-elemental content, also be used to distinguish OM deposited during along with d13C and d15N signatures, can sometimes periods of high versus low primary productivity. provide insights into: (1) the origin of OM in water Fractionation occurs during photosynthesis because bodies, (2) past lacustrine productivity, and (3) algae discriminate against the heavier 13C isotope. mineralization processes in lakes. In this study, we Phytoplankton typically has d13C values *20% determined OM, C, N, P and d13C and d15N values in lower than the dissolved inorganic carbon (DIC) sediment cores from three subtropical lakes. We had substrate used in photosynthesis. Under conditions of two major objectives. First, we sought to evaluate low to moderate primary productivity, algae are able whether macro-element concentrations and stable to utilize lighter 12C preferentially. Consequently, the isotope values in surface sediment deposits reflect resultant autochthonous OM displays very low d13C. modern trophic state conditions in the lakes. Second, During periods of very high primary productivity, the we wanted to assess whether stratigraphic changes in 12C pool in the water column is utilized preferen- the measured variables might yield information about tially, and once diminished, algae are forced to use shifts in trophic status through time, or alternatively, the heavier isotope, yielding OM with relatively diagenetic changes in sediment OM. higher d13C (Mizutani and Wada 1982). Hypereu- trophic lakes with high rates of primary productivity Study sites have low dissolved concentrations of carbon dioxide

(CO2) in the water column. Moreover, in high-pH Three lakes in Florida (USA) were selected for this - waters, bicarbonate (HCO3 ) dominates the DIC and study, using trophic status criteria (Tables 1, 2; 13 2 has a d C that is *8% higher than dissolved CO2 Fig. 1). Lake Annie is a small (0.37 km ), relatively (Fogel and Cifuentes 1993). High demand for DIC deep (zmax = 20 m), oligo-mesotrophic lake in - and low free CO2 leads to utilization of HCO3 as a C south-central Florida (Highlands County), at the source, also yielding higher d13C values in algal OM north edge of the Archbold Biological Station. The (Goericke et al. 1994). lake sits atop the Lake Wales Ridge and is situated 123 J Paleolimnol (2012) 47:693–706 695

Table 1 Long-term water Select variables Minimum Average Maximum quality data for the three Florida lakes used Lake Annie (2000–2005) in this study Total phosphorus concentrations (lg/L) (n = 62) 4 9 27 Total nitrogen concentrations (mg/L) (n = 62) 0.26 0.43 0.74 Total chlorophyll concentrations (lg/L) (n = 62) 2 6 22 Secchi depth (m) (n = 62) 0.7 2.4 5.0 Lake Okeechobee (mud zone) (1972–2010) Total phosphorus concentrations (lg/L) (n = 555) 3 112 642 Total nitrogen concentrations (mg/L) (n = 548) 0.22 1.6 4.4 Data were obtained from Total chlorophyll concentrations (lg/L) (n = 454) 1.5 19 66 various sources. Lake Secchi depth (m) (n = 445) 0.04 0.3 1.4 Annie = Florida Lake Apopka (1987–2009) Lakewatch program; Lake Total phosphorus concentrations (lg/L) (n = 276) 58 167 377 Okeechobee = South Florida Water Management Total nitrogen concentrations (mg/L) (n = 276) 2.5 4.8 9.7 District (SFWMD). 2010. Total chlorophyll concentrations (lg/L) (n = 251) 27 77 196 DBHYDRO. Lake Secchi depth (m) (n = 271) 0.12 0.27 0.61 Apopka = (Coveney 2010)

Table 2 Characteristics of the sampling sites in the three Florida lakes, with sampling date, location, sediment type and water variables Variable Lake Annie Lake Okeechobee Lake Apopka

Site Central M9 West Latitude 27°1202700 26°58017.600 28°3800100 Longitude 81°2104400 80°45038.400 81°3903600 Sampling date June 2005 July 2005 May 2005 Sediment type Mud/clay Mud Organic Water column depth (m) 20 4.0 2.0 Secchi depth (m) 2.0 0.08 0.3 Temperature (°C)a 30.2 29.5 26.6 Electrical conductivity (lScm-1)a 41.9 385 443 pHa 5.1 7.8 7.6 -1 a Dissolved oxygen (mg O2 L ) 6.4 6.5 8.7 Dissolved organic C (mg C L-1)b 13.8 14.5 31.1 Total P (lgPL-1)b 33 256 70 Dissolved reactive P (lgPL-1)b 79011 Total N (mg N L-1)b 1.81 3.44 11.15 Ammonium (mg N L-1)a 0.18 0.10 0.12 The Annie TP value is very high relative to that reported by Lakewatch (long-term mean = 9 lgPL-1) a Measured at 1 m depth in the water column b Mean concentration in the water column. For Lake Annie, values are the average of samples taken at the following depths: 0.5, 1.0, 2.0, 5.0, 10, 20 m; for Lake Okeechobee and Lake Apopka, values are an average of samples taken at 0.5, 1.0, and 2.0 m in nutrient-poor quartz sands. Water enters the lake periods of high rainfall (Battoe 1985). Water leaves principally in direct precipitation and as shallow the lake via evaporation and a small outﬂow stream groundwater, but two man-made ditches contribute on the north shore. Sediments in the littoral zone are surface waters and associated nutrients during sandy to organic (Layne 1979), whereas deposits in 123 696 J Paleolimnol (2012) 47:693–706

- C

A 025 50 100 150 200 250Kilometer s B

0 B

We s t

- 02461 Kilometer s

Fig. 1 Maps of the three subtropical study lakes with sampling sites and lake location in Florida: a Lake Annie (with water column depth in meters, modiﬁed from Layne 1979), b Lake Okeechobee with different sediment types, and c Lake Apopka deeper water have higher OM content. Because the from several sources, including agricultural drainage lake is located in a private reserve, it is subject to from adjacent vegetable farms (Schelske et al. 2005, relatively little anthropogenic impact (Layne 1979). 2010). Although these inputs were controlled and regu- Lake Okeechobee is a large (1,730 km2), shallow, lated to some degree, the eutrophication process contin- eutrophic lake located in south Florida that has ued and Lake Apopka is now considered hypereutrophic. experienced cultural eutrophication over the last Benthic sediments are unconsolidated and consist mainly 50 years (Engstrom et al. 2006). Benthic sediments of material of algal origin (Reddy and Graetz 1991). are characterized as mud (44% of the total lake surface area), sand and rock (28%), littoral areas dominated by macrophytes (19%), and peat or partially decomposed Materials and methods plant tissue (9%) (Fisher et al. 2001). Lake Apopka is a shallow lake (125 km2) located in Field sampling central Florida. Once a clear-water, macrophyte-dominated lake, it changed in 1947 to a turbid, algal-dominated Sediment–water interface cores of variable lengths water body (Clugston 1963), following nutrient input were collected using a piston corer (Fisher et al. 1992) 123 J Paleolimnol (2012) 47:693–706 697 or by SCUBA divers. Lake maps with sampling notation, with samples measured relative to the Pee locations are shown in Fig. 1. One central site (60-cm Dee Belemnite for C and atmospheric N2 for N. core) was sampled in Lake Annie on June 25, 2005. A Analytical accuracy and precision were established 73-cm core was collected on July 16, 2005 from the using known isotopic standards (wheat ﬂour, mud zone of Lake Okeechobee (site M9), an area that d13C =-26.4 %, d15N = 2.6 %, Iso-Analytical; has the highest concentration of P among the different IAEA-N1, d15N = 0.4 %; ANU-Sucrose, d13C = sediment types of this lake. A 72-cm core was taken -10.5 %). Analytical precision for standards was from a western site in Lake Apopka on May 28, 2005. within ±0.1% for d13C and ±0.3% for d15N. Sediment cores were sectioned at 4-cm intervals and samples were sealed in labeled plastic bags and returned to the laboratory on ice. Results

Sediment properties Water column characteristics

Sediment samples were dried in a Virtis Unitrap II All three lakes had water transparency B2 m (Tables 1, freeze drier. Sediment bulk density was determined as 2). Most water-column variables represent the value for dry weight per unit wet volume (g dry cm-3 wet) a sample collected at 1 m depth in the water column, following freeze-drying. Dried samples were ground whereas dissolved organic carbon (DOC), total phos- in a mortar and pestle and passed through a phorus (TP), dissolved reactive phosphorus (DRP), and 2-mm-mesh sieve. Organic matter content (LOI%) total nitrogen (TN) were measured at several depths in was estimated on fine sediment fractions (samples each lake and mean values were calculated (Table 2). sieved through 2-mm screen) by weight loss on ignition For Lake Annie, values are the average of measure- at 550°C (LOI). Total P in samples was measured by ments taken at 0.5, 1, 2, 5, 10 and 20 m, whereas for ashing, followed by acid digestion (6 M HCl) and Lake Okeechobee and Lake Apopka values are aver- colorimetric measurement with a Bran ? Luebbe ages of samples taken at 0.5, 1 and 2 m. Electrical TechniconTM Autoanalyzer II (Anderson 1976; EPA conductivity values reflect the trophic status of each Method -365.1). Total carbon (TC) and total nitrogen lake, with the lowest mean value for Lake Annie (TN) were determined using a Flash EA-1121 NC soil (42 lScm-1), and higher mean values for Lake analyzer (Thermo Electron Corporation). Okeechobee (385 lScm-1) and Lake Apopka (3,443 lScm-1). Lake Annie water column pH was Stable isotope analyses low (5.1), whereas both Lake Okeechobee (7.8) and Lake Apopka (7.6) were above neutral. Daytime Sediment samples for organic C isotope analysis were dissolved oxygen concentrations ranged from 6.4 to pretreated with acid to remove inorganic (carbonate) C 8.7 mg L-1, with highest values measured in Lake (Harris et al. 2001). Samples were weighed in silver Apopka. Highest DOC values were found in Lake capsules, placed in the wells of a microtiter plate, and Apopka (31 mg C L-1), whereas DOC values in the 50 lL of deionized (DI) water was added to moisten other lakes were similar, around 14 mg C L-1. Total P the sediment. Plates were placed in a vacuum desic- in the water column was much higher in Lake cator with 100 mL of concentrated HCl and exposed Okeechobee (256 lgPL-1) than in either Lake Apo- to HCl vapor for 24 h. Samples were dried at 60°C for pka (70 lgPL-1)orLakeAnnie(33PlgL-1). 4 h to remove remaining HCl. Carbon (organic) and These values represent only the day water samples nitrogen (total) isotope values were determined using were collected and are different from long-term average the method described by Inglett et al. (2007). Isotope values presented in Table 1. Dissolved reactive phos- analyses were conducted using a Costech Model 4010 phorus showed similar relations, with the greatest Elemental Analyzer (Costech Analytical Industries, values in Lake Okeechobee (90 lgL-1), and smaller Inc., Valencia, CA) coupled to a Finnigan MAT values in Lake Apopka (11 lgPL-1) and Lake Annie DeltaPlusXL Mass Spectrometer (CF-IRMS, Thermo (7 lgL-1). Total nitrogen, however, was greatest in Finnigan) via a Finnigan Conflo II interface. Stable Lake Apopka (11 mg N L-1), with lower values mea- isotope results are expressed in standard delta sured in Lakes Okeechobee (3.4 mg N L-1) and Annie 123 698 J Paleolimnol (2012) 47:693–706

(1.8 mg N L-1). Ammonium-N values were rather sim- to values between 1,500 and 1,900 mg kg-1 in the ilar across the lakes, with Annie displaying the highest upper 16 cm (Fig. 2a). The TN/TP ratio was 12.5 in amount (0.18 mg N L-1), and Apopka and Okeechobee surface sediments (0–4 cm) and decreased to 10 at both containing approximately 0.1 mg N L-1. 16 cm depth (Fig. 2a). This was followed by a steady increase in ratios to 15 (Fig. 2c). The d13C values ranged from about -28 to -29% in the lower portion Sediment properties of the core (60–16 cm), but then declined to the lowest value of -30% in the surface sediments (Fig. 2e). The Lake Annie d15N values were positive, varying between about 2.0 and 2.3%, but declined to 0.9% in the topmost sediments Organic matter content (LOI %) in the Lake Annie (Fig. 2f). Surface sediments are low relative to subsur- core generally increased toward the sediment surface, face sediments, by 1.2% (d13C) and 1.1% (d15N). from a low of about 50% to a high of about 56% (Fig. 2d). Lake Annie sediment TC:TN ratios dis- Lake Okeechobee played a slight increase with depth, from 13 to 15 (Fig. 2b). Total P in sediments was *1,000 mg kg-1 Mud zone sediments from site M9 in Lake Okeecho- in the lower part of the core (28–60 cm), but increased bee showed OM (LOI) values ranging from about 18

To t a l P ho s ph o ru s ( mg k g -1) TC/ TN TN/TP 0 400 800 1200 1600 2000 10 12 14 16 9 10111213141516 0 0 0 4 4 4 8 8 8 12 12 12 16 16 16 20 20 20 24 24 24 28 28 28 32 32 32 36 36 36

Depth (cm) 40 40 40 44 44 44 48 48 48 52 52 52 56 56 56 60 A 60 B 60 C 64 64 64

LOI (%) δ13C δ15N 49 50 51 52 53 54 55 56 57 -31 -30 -29 -28 -27 0 1 2 3 4 0 0 0 4 4 4 8 8 8 12 12 12 16 16 16 20 20 20 24 24 24 28 28 28 32 32 32 36 36 36 Depth (cm) 40 40 40 44 44 44 48 48 48 52 52 52 56 56 56 60 D 60 E 60 F 64 64 64

Fig. 2 Lake Annie sediment depth proﬁle of: a total phosphorus, b TC:TN ratio, c TN:TP ratio, d organic matter content (LOI), e d13C of sediment organic carbon and f sediment d15N 123 J Paleolimnol (2012) 47:693–706 699 to 40%, with highest values recorded in the uppermost Lake Apopka deposits (Fig. 3d). The TC:TN ratios were relatively low (*18) near the base of the section, but increased Among the three lakes, OM content in the Apopka to a maximum of *32 at 24 cm depth (Fig. 3b). sediment core was greatest, varying between about 62 Thereafter, the ratios decreased to 15 in the topmost and 70%, with low values observed at depths 32–48 cm 12 cm. Total P in surface sediments was approxi- (Fig. 4d). Lake Apopka sediments displayed a narrow mately 1,000 mg P kg-1 and steadily decreased to range of TC:TN ratios, *11–12 (Fig. 4b). There was a 500 mg P at depths [36 cm (Fig. 3a). Overall, d13C general decrease from about 72–12 cm depth, and then values ranged from -26 to -25%, with surface an increase to the sediment surface (Fig. 4b). Total P sediments only slightly lower relative to subsurface concentration more than doubles between the base of the sediments (Fig. 3e). Nitrogen isotope values vary core (*600 mg P kg-1) and 20 cm depth ([1,400 mg from 2.6 to 3.9% and show *1.3% higher values in Pkg-1)(Fig.4a). The TN:TP ratios declined twofold surface sediments relative to sub-surface sediments moving upcore, reﬂecting recent increases in P concen- (Fig. 3f). tration (Fig. 4c). Organic matter d13C increased from

Total Phosphorus (mg kg-1) TC/TN TN/TP 0 200 400 600 800 1000 14 16 18 20 22 24 26 28 30 32 34 2 4 6 8 10 12 14 16 18 20 22 0 0 0 4 4 4 8 8 8 12 12 12 16 16 16 20 20 20 24 24 24 28 28 28 32 32 32 36 36 36 40 40 40 44 44 44 Depth (cm) 48 48 48 52 52 52 56 56 56 60 60 60 64 64 64 68 68 68 72 A 72 B 72 C 76 76 76

LOI (%) δ13C δ15N 16 18 20 22 24 26 28 30 32 34 36 38 40 42 -27 -26 -25 -24 234 0 0 0 4 4 4 8 8 8 12 12 12 16 16 16 20 20 20 24 24 24 28 28 28 32 32 32 36 36 36 40 40 40 44 44 44 Depth (cm) 48 48 48 52 52 52 56 56 56 60 60 60 64 64 64 68 68 68 72 D 72 E 72 F 76 76 76

Fig. 3 Lake Okeechobee sediment depth proﬁle of: a total phosphorus, b TC:TN ratio, c TN:TP ratio, d organic matter content (LOI), e d13C of sediment organic carbon and f sediment d15N

123 700 J Paleolimnol (2012) 47:693–706

Total Phosphorus (mg kg-1) TC/TN TN/TP 0 400 800 1200 1600 10 11 12 13 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 0 0 0 4 4 4 8 8 8 12 12 12 16 16 16 20 20 20 24 24 24 28 28 28 32 32 32 36 36 36 40 40 40 44 44 44 Depth (cm) 48 48 48 52 52 52 56 56 56 60 60 60 64 64 64 68 68 68 72 A 72 B 72 C 76 76 76

LOI (%) δ13C δ15N 60 62 64 66 68 70 -23 -22 -21 -20 -19 -18 345 0 0 0 4 4 4 8 8 8 12 12 12 16 16 16 20 20 20 24 24 24 28 28 28 32 32 32 36 36 36 40 40 40 44 44 44 Depth (cm) 48 48 48 52 52 52 56 56 56 60 60 60 64 64 64 68 68 68 72 D 72 E 72 F 76 76 76

Fig. 4 Lake Apopka sediment depth proﬁle of: a total phosphorus, b TC:TN ratio, c TN:TP ratio, d organic matter content (LOI), e d13C of sediment organic carbon and f sediment d15N

-23% in subsurface sediments to -18% in surface high proportions of allochthonous C contribution to sediments (Fig. 4e). Nitrogen isotope values also sediment OM (Gu et al. 1996). Terrestrial C3 plants display an increase upcore, from 3.9% (lower depths) discriminate against 13C, and organic matter derived to 4.7% (surface sediments) (Fig. 4f). from these plants typically has d13Cvaluesbetween -27 and -29% (Meyers 1997). Hammarlund et al. (1997) related progressive depletion of 13CinLake Discussion Tibetanus (Sweden) to increases in the input of OM from surrounding vegetation. Jonsson et al. (2001) Lake Annie reported negative d13C values of dissolved C in humic Lake O¨ rtra¨sket, Sweden, resulting from the mineraliza- Stratigraphic fluctuations in the d13Candd15Nvaluesof tion of allochthonous OM. Also, phytoplankton dis- 13 Lake Annie sediment OM probably reflect a combina- criminate against C in the water column when CO2 tion of factors, including a shift in relative contribution concentration is high, which should be the case in this of autochthonous/allochthonous OM, changing autoch- low-pH lake. Consequently, autochthonous OM in Lake thonous primary productivity, and relative microbial Annie might also be expected to show low d13Cvalues. biomass and activity (Torres et al. 2011). Small, The heterotrophic microbial community can also oligotrophic lakes might be expected to have relatively contribute to low d13C. Heterotrophic uptake of DOC 123 J Paleolimnol (2012) 47:693–706 701 preserves the C isotope signature of the source, difficult to determine with certainty the main factors and biomass associated with chemoautotrophic and that influence the C and N isotope signatures of Lake methanotrophic microorganisms is thus generally Annie sediment OM. For instance, allochthonous depleted in 13C (Kankaala et al. 2006). An isotope particulate and dissolved OM with relatively low study on sediments from eutrophic Lake Mendota, d13C may be a major source of C in the lake. The Wisconsin illustrated that mineralization of C by the microbial community that mineralizes and utilizes this heterotrophic microbial community, associated with C will have 13C-depleted biomass. Isotopically- ? expansion of anoxic conditions in the water column, depleted end products, such as CO2 and NH4 , which led to sediment OM with low d13C values (Hollander result from heterotrophic metabolism, will be utilized and Smith 2001). Both seasonal and long-term by primary producers that display isotopically- increases in the contribution of depleted microbial depleted autochthonous OM. Surface enrichment of biomass to sediments caused lower d13C values TP in sediments suggests that external P input (Hollander and Smith 2001). Lehman et al. (2002) occurred in the lake. Lake water quality data, however, reported that anaerobic decomposition in Lake Lug- show oligotrophic to mestrophic conditions. It is also ano, on the Swiss-Italian border, led to 13C-depleted likely that some dissolved P may have mobilized from OM of sinking particles and sediments. Terranes and subsurface sediments and precipitated with oxidized Bernasconi (2005) linked the d13C of sediment OM in iron oxides. A more detailed study of d13C and d15Nin Lake Baldeggersee, Switzerland to the relative inputs several compartments (e.g. DIC, DOC, nitrate, ammo- of eukaryotic biomass enriched in 13C, and to inputs of nia, phytoplankton biomass, bacteria biomass) may 13C-depleted microbial biomass produced in anoxic elucidate the principal processes that shape the bottom waters. In Lake Annie, the thermocline has isotopic signature of Lake Annie sediments. been moving to shallower depths, i.e. higher in the water column during thermal stratification, with Lake Okeechobee anoxia and sulfate reduction occurring below 5 m depth (Gaiser et al. 2009). The increasing volume of High TC:TN values in the middle section of the anoxic bottom water probably led to anaerobic sediment core probably indicate a large contribution decomposition of already 13C-depleted suspended from allochthonous OM, or perhaps loss of N through OM, resulting in deposition and preservation of mineralization. Low TC:TN values in recent deposits undecomposed OM. probably reflect a greater relative contribution from Similar processes affect N isotope signatures in phytoplankton. The concurrent increase in total P and Lake Annie. Plants discriminate against 15N during decline in TC:TN suggest recent eutrophication and inorganic N uptake (Inglett and Reddy 2006). Allo- greater primary production in the lake, fueled by chthonous OM derived from C3 terrestrial plants greater P input. TN:TP shows a general decrease from generally has a d15N value of about ?0.4% (Peterson the bottom of the sediment core to the surface, and Howarth 1987). Autochthonous OM in aquatic reflecting more rapid increase of TP relative to TN ecosystems also typically has higher d15N signatures, concentration (Fig. 3c). A similar trend was reported whereas N-fixing algae possess values near that of by Engstrom et al. (2006) in sediment cores from the atmospheric N2, i.e. 0% (Peterson and Howarth 1987). mud zone of Lake Okeechobee and was attributed to Several other microorganisms fix nitrogen, including increasing TP content of uppermost sediments, as a aerobic and anaerobic heterotrophic bacteria, meth- consequence of eutrophication. ane-oxidizing bacteria, and sulfate reducers. N-fixing The d13C sediment profile shows a pattern similar algae have not been detected in Lake Annie (E. Gaiser to that for TC:TN (Fig. 3b, e). Similar patterns, i.e. 13 15 pers. commun.), however, N2-fixation may occur in lower d C and higher d N, were reported by the heterotrophic microbial community. Rosenmeier et al. (2004) in a study of recent eutro- High N availability in the Lake Annie water column phication of Lake Peteń Itza´, Guatemala, where and sediments (Torres 2007) can lead to autochtho- changes were related to sewage input with depleted nous OM with low d15N, as high N concentrations 13C and enriched 15N, and increased presence of allow greater discrimination by algae against 15N cyanobacteria. Engstrom et al. (2006) also found (Fogel and Cifuentes 1993). For this reason, it is higher d15N values (1%) in recent deposits from 123 702 J Paleolimnol (2012) 47:693–706

Okeechobee’s mud zone, but did not discuss the Additionally, isotopic analysis of sediment in Lake mechanisms responsible. Stratigraphic changes in Lugano indicates a decline in d13C during early d13C and d15N in the mud zone were probably sediment diagenesis (Lehman et al. 2002). In the Lake controlled by the nature of autochthonous OM, Okeechobee mud zone, several factors probably availability of C and N, and varying intensities of influence the d13C and d15N values in the OM of mineralization. Lake Okeechobee mud zone sedi- sediments. They include the nature of the phytoplank- ments are probably C- and N-limited, and N demand is ton community, N limitation in the water column, high high in these sediments (Torres 2007). In the mud zone demand for C and N in sediments, and selective of Lake Okeechobee, high dissolved OM and abun- mineralization of OM. dant suspended material in the water column make light the limiting factor for the phytoplankton com- Lake Apopka munity during most of the year (Aldridge et al. 1995). During summer months, light limitation is relaxed and Nitrogen availability is high in Lake Apopka sediments N becomes the limiting factor for the phytoplankton (Torres 2007). In Lake Apopka sediments, nitrification community (Aldridge et al. 1995). The d15NofOMin is high in surface sediments where aerobic conditions - ? sediments of eutrophic and hypereutrophic lakes can prevail, and dissimilatory NO3 reduction to NH4 is be influenced by cyanobacterial N2-fixation (Gu et al. high in anaerobic sediments when the ratio of C/electron 1996; Rosenmeier et al. 2004), however non-N2-fixing acceptors is high (D’Angelo and Reddy 1993). Among cyanobacteria typically dominate the phytoplankton the lakes, Lake Apopka has the highest d13Cvaluesand community and the N2 fixation rate is low in the showed the greatest increase in values through time. In a central area of Lake Okeechobee (Cichra et al. 1995; study of 83 Florida lakes that ranged in trophic state, 13 Gu et al. 1997). Under non-N2 fixing conditions, N Lake Apopka plankton also had the highest d C(Gu limitation can lead to autochthonous OM with higher et al. 1996). Gu et al. (2004) found evidence for extreme d15N, as algae discrimination against 15N diminishes 13C enrichment of DIC in the water column and (Meyers 1997; Peterson and Howarth 1987). sediment pore water of this shallow polymictic, hyper- Some studies indicate that the isotopic signature of eutrophic lake. Greater d13C towards the surface probably OM is resistant to alteration during water-column indicates increased primary productivity, reflecting recent or post-burial diagenesis (Meyers and Eadie 1993; eutrophication (Brenner et al. 1999). Hodell and Schelske 1998; Terranes and Bernasconi The C isotope signature of autochthonous OM is 2000). Other studies, however, have shown that influenced by the d13C of the dissolved inorganic C selective degradation of OM fractions alters the pool in lake water. Hodell and Schelske (1998) related 13 isotopic signature (Bernasconi et al. 1997; Meyers the seasonal pattern of d Corg in Lake Ontario to 1997; Lehman et al. 2002, 2004). Labile organic seasonality of primary productivity. Gu et al. (2006) compounds including carbohydrates, proteins and reported that 13C enrichment of particulate OM in amino acids are generally more enriched in 13C, while Lake Wauberg (Florida) resulted from reduced isoto- lipids and cellulose are isotopically lighter (Meyers pic fractionation due to C-limitation and use of 1997). Selective loss of ‘‘heavy’’ amino acids, proteins inorganic 13C for photosynthesis. Lehman et al. and carbohydrates, which are particularly susceptible (2004) concluded that the most important process to microbial degradation, leaves residual (substrate) controlling the C-isotopic signature of suspended OM isotopically lighter, with respect to d13C, than the particulate OM in Lake Lugano is the concentration original material (Hedges et al. 1988). of CO2 in surface water, which is a function of Loss of compounds that are relatively rich in 15N phytoplankton photosynthesis. Algae fractionate (e.g. amino acids) can also occur, lowering the d15Nin against 13C, so autochthonous OM is depleted in 13C residual OM. Nevertheless, decomposition of OM is relative to the DIC pool. During periods of high generally thought to increase d15N through preferen- primary productivity, however, this fractionation tial loss of 14N. Bernasconi et al. (1997) reported shifts diminishes and more 13C is incorporated into primary to lower d13C and higher d15N of sinking OM in Lake producer biomass (Mizutani and Wada 1982). Lugano, which they attributed to selective removal Hypereutrophic lakes with high rates of primary 13 of C and N compounds during mineralization. productivity have C-enriched CO2 (aq) in the water 123 J Paleolimnol (2012) 47:693–706 703 column as a consequence of selective uptake of lighter relatively unimportant in N dynamics (Schelske 12 - C during photosynthesis. Moreover, in alkaline et al. 1992). High NO3 availability can also lead to - 15 waters bicarbonate (HCO3 ) is the dominant form of autochthonous OM with low d N values (Meyers inorganic C, and is *8% heavier than C in dissolved 1997). If, however, N incorporation uses a significant - - CO2 (Fogel et al. 1992). High demand for inorganic C amount of the lake’s NO3 pool, residual NO3 is - 15 and low free CO2 leads to utilization of HCO3 as a enriched, ultimately leading to an increase in the d N carbon source, resulting in higher d13C values of fixed of newly produced OM (Terranes and Bernasconi OM (Goericke et al. 1994). Gu et al. (2004) showed 2000; Syva¨ranta et al. 2006). Jones et al. (2004) that high d13C DIC in the water column was a result of reported higher sediment d15N when inorganic N was isotopic fractionation during methanogenesis in the low in the water column, reflecting reduced isotopic 13 sediments. Methanogenesis produces C-rich CO2 fractionation under N limitation. Nitrogen is the 13 and C-poor methane (CH4) (Games and Hayes primary limiting nutrient in Lake Apopka, though 1976). The Lake Apopka water column has low CO2 co-limitation with P can occur (Aldridge et al. 1993). partial pressure, high pH, and high buffering capacity. Periods of N limitation in the water column can lead to 13 Consequently, C-rich CO2 is transferred from the enrichment of autochthonous OM and stratigraphic sediments to the DIC of the water column (Gu et al. variation in the d15N signature of sediment OM in

2004). Lake Apopka sediments display high CH4 Lake Apopka may indicate periods of N limitation. production rates (Torres et al. 2011). Furthermore, Other mechanisms may also influence the d15Nof most of the OM generated by primary productivity in Lake Apopka sediments. The N isotopic signature of this lake is deposited in its sediments (Gale and Reddy sediment integrates multiple fractionation processes 1994). Primary productivity is dominated by cyano- that occur in the sediment and water column (Lehman bacteria (Synechococcus sp., Synechocystis sp. and et al. 2004). Ammonium production via OM mineral- Microcystis incerta) (Carrick et al. 1993; Carrick and ization is high in these sediments (Torres 2007). Such Schelske 1997). Cyanobacteria are capable of active mineralization processes can potentially lead to either - CO2 transport or utilizing HCO3 (Espie et al. 1991), higher isotope values in the remaining OM through and both can result in higher d13C values in phyto- preferential loss of isotopically lighter compounds plankton biomass. Jones et al. (2001) reported that (Bernasconi et al. 1997), or have little effect on the high phytoplankton d13C in Loch Ness (Scotland) d15N of the original organic matter (Inglett et al. 2007). resulted from high d13C DIC. Similar results were Moreover, denitrification discriminates against 15N, and found in urban Lake Jyva¨skyla¨ (Finland), where high increases in denitrification rates have been related to d13C DIC resulted in high d13C of phytoplankton and higher d15N signatures in sediments (Terranes and zooplankton biomass (Syva¨ranta et al. 2006). High Bernasconi 2000; Savage et al. 2004). Thus, the N d13C DIC in the water column, with high demand for isotope signature in Lake Apopka sediments is gener- inorganic C due to high primary productivity, pro- ated by multiple factors, including the isotopic signature duces autochthonous OM with high d13C, which is of autochthonous N sources, the primary producer deposited in the sediments. community, and N-related processes in the water It is generally thought that eutrophic and hypereu- column and sediments. trophic lakes have low d15N as a consequence of high When stable C and N isotope data (d13C and d15N) rates of N2 fixation (Fogel and Cifuentes 1993). We, were plotted against each other in ‘‘isotope space,’’ however, observed 15N enrichment in Lake Apopka there was fairly good separation among sediments sediments. High phytoplankton productivity reduces from the three study lakes (Fig. 5). Oligo-mesotrophic isotopic discrimination, causing high isotope values. Lake Annie has the lowest values for both d13C and Gu et al. (1996) also reported high d15N in Lake d15N, and displays no overlap with samples from Apopka sediments. In Lake Apopka, N assimilated by Okeechobee or Apopka. Lake Okeechobee displays phytoplankton is supplied primarily by transformation intermediate, distinct d13C values, but its d15N values ? - of organic N to NH4 and then to NO3 by nitrification overlap to some degree with samples from Lake (D’Angelo and Reddy 1993). Although the phyto- Apopka. Lake Apopka displays the highest values plankton community is dominated ([ 90%) by cya- with respect to both d13C and d15N. All its d13C nobacteria (Carrick et al. 1993), N2 fixation is signatures are greater than values determined for 123 704 J Paleolimnol (2012) 47:693–706

5.0 the topmost three samples in Okeechobee showed 15 4.5 overlap with d N values from Lake Apopka. The

4.0 Lake Okeechobee isotope signatures resulted from

3.5 several factors, including the nature of the phytoplankton community, high demand for C and N in 3.0 N

15 sediments, and selective mineralization of OM. In δ 2.5 Lake Apopka, high d13C DIC in the water column, 2.0 with high demand for inorganic C as a consequence of 1.5 high primary productivity, produced autochthonous 13 15 1.0 OM with high d C. The high d N signature in Lake

0.5 Apopka sediments was probably generated by a -30 -28 -26 -24 -22 -20 -18 -16 combination of factors, including the isotopic signa- δ 13C ture of autochthonous N sources, the primary producer Fig. 5 Carbon versus nitrogen isotope values of sediment core community, and N-related processes in the water samples from Lake Annie (circles), Lake Okeechobee column and sediments. Water depth differences (squares), and Lake Apopka (triangles), Florida among the three study lakes may be a key factor influencing the isotope values in sediments, with better sediment OM in the other two lakes, but its d15N preservation of OM deposited in deep Lake Annie values show some overlap with Okeechobee d15N compared to shallow Lakes Apopka and Okeechobee. values. High OM decomposition rates in shallow lakes A more detailed study of d13C and d15N in various (Apopka and Okeechobee) typically results in compartments, i.e. DIC, DOC, different N com- enriched 13C, compared to deep lakes (Annie), where pounds, phytoplankton biomass, bacteria biomass, OM is well preserved. In general, there is higher d13C and other particulate OM in the water column and and d15N with increasing trophic state. Enrichment in sediment, may lead to a better understanding of the 13C with increasing lake productivity agrees with major processes affecting the isotope signatures of findings from other studies (Brenner et al. 1999). We OM in the sediments from these lakes. found, however, that d15N generally increases in the autochthonous OM as trophic state increases, in Acknowledgments This work was funded in part by USDA/ agreement with the findings of Gu (2009), but contrary NRI grant No. 2004.35107-14918. We thank M. Fisher, J. Smith, A. Albertin and K. McKee for assistance in the field, and to those of Brenner et al. (1999), who observed Y. Wang and J. Bright for laboratory support. The authors thank 15 decreases in d N as lakes became more eutrophic. T. Stephens and J. Holmes for their critical reviews that greatly helped to improve the overall quality the manuscript.

Conclusions References

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