Article history:Received 21 August 2012Accepted 7 March 2013Available online 6 May 2013
Communicated by William Taylor
Index words:Internal phosphorus loadHypoxiaCyanobacteriaHypolimnetic ironManganeseLake Simcoe
Hypoxia and cyanobacterial blooms were extensive in Lake Simcoe during the 1980s and are still a problemto a lesser degree despite extensive nutrient load reduction from the catchment basin. The continuing signs ofproductivity indicate a potential internal phosphorus (P) source. Internal P load, as a redox-dependent re-lease from bottom sediments, is hard to determine in a large, relatively shallow and partially unstratifiedlake such as Lake Simcoe. Of the lake's three major basins, only Kempenfelt Bay stratifies long enough to de-velop hypoxia in the stagnant summer hypolimnion. The following indications of sediment P release are avail-able from historic data: 1) hypolimnetic hypoxia still occurs in Kempenfelt Bay although the hypoxic factor(number of days that an area equal to the bay's surface area is overlain by water of≤2 mg/L dissolved oxygen,DO) has decreased substantially and significantly from 15.8 d/yr (1980–1994) to 4.0 d/yr (1995–2011);2) hypoxic factors for other lake sections and at different DO levels also indicate widespread hypoxia;3) concentrations of redox dependent metals, Fe and Mn, increase with depth; and 4) euphotic zone P andchlorophyll concentrations increase and water clarity decreases during fall turnover. Cyanobacterial bloomsappear to occur in response to internal load as supported by occasional cyanobacteria counts. These indicatorsprovide evidence that internal loading is likely occurring and affecting the water quality in Lake Simcoe. Weexpect that further monitoring, specific for internal load, will corroborate these results.
Lake Simcoe is a large (722 km2), mesotrophic lake located in adensely populated area of southern Ontario. Its high external phos-phorus (P) inputs have been managed since the 1990s in an effortto prevent the occurrence of end-of-summer hypolimnetic dissolvedoxygen levels that were lethal to coldwater fish species (Young etal., 2011). The lake is well-studied, and water quality has been exten-sively monitored since 1980 by local and regional agencies (LakeSimcoe Region Conservation Authority [LSRCA] and Ontario Ministryof the Environment [MOE]). Data collection includes vertical temper-ature and dissolved oxygen (DO) profiles, lake phosphorus (P) con-centrations, P loads from external sources, and chemical backgrounddata as well as detailed morphometric and phytoplankton surveys.Thus a wealth of information is available to determine whether inter-nal P loading is an important nutrient source to this lake.
Internal loading stems from former external inputs that have beenstored in the bottom sediments. After diagenesis most internal P load
ssociation for Great Lakes Research.
originates from P adsorbed onto ferric oxy-hydroxides in the sedi-ments that is released into the porewater and then into the overlyinglake water as soon as the sediment surfaces become anoxic (reduced).For management purposes, internal load is best quantified similar toexternal load, as gross load before any sedimentation and retention(Nürnberg, 2009).
In large, partially stratified lakes such as Lake Simcoe, where only5% of the area is deep and confined enough to thermally stratify, it isdifficult to separate internal inputs from external inputs of nutrientsbecause of the frequent exchange between water layers (Nürnberget al., 2012). Lake Simcoe has a small catchment basin area that isonly 4 times larger than its surface area (Table 1, O'Connor et al.,2012) suggesting that atmospheric loading and internal processeshave a strong influence onwater quality and other lake characteristics.Nonetheless, little is known about internal P loading in Lake Simcoealthough Nicholls (1995) suggested that this potential source had tobe considered in Lake Simcoe management plans. Indications of inter-nal P loading have been presented from time to time (Eimers andWinter, 2005; Nicholls, 1995), but in a recent overview of researchquestions concerning Lake Simcoe, it was not addressed (Palmeret al., 2011). Nevertheless, current experimental release rate studies
Table 1Stations, morphometry (Ontario Ministry of Natural Resources), total phosphorus (TP)average of euphotic zone (composite) samples (no long term trend), and Secchi trans-parency (during two different periods) of the studied sections of Lake Simcoe. The sta-tion names correspond with Fig. 1. n.m., not meaningful.
Fig. 1. Location of Lake Simcoe andmap indicating depths contours (m) and sample sta-tions (circle) for the three investigated basins, Kempenfelt Bay, Cook's Bay and MainBasin.Source: Ontario Ministry of Natural Resources and Lake Simcoe Region ConservationAuthority.
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observed redox and temperature dependent release of P and iron inLake Simcoe sediment cores and determined sediment P fractions ca-pable of redox-related release (Loh et al., 2013).
We used historical P monitoring data collected at Lake Simcoe'sstations in Cook's and Kempenfelt Bays and the main open-waterbasin (Fig. 1) since the early 1980s to gather evidence of internal Pload in Lake Simcoe for as many individual years as possible. Thistime frame included periods before and after zebra mussel establish-ment (1996) and external load abatement (greatest decrease by1998). We looked at typical signs of internal load. For example, sedi-ment P release is indicated when the total P (TP) concentration inhypolimnetic samples taken at discrete depths is elevated in compar-ison to composite epilimnetic samples andwhen the TP concentrationincreases with proximity to the bottom sediments. Further, increasinghypolimnetic TP concentration throughout the summer and especiallyin the fall is usually attributable to internal load, especially when hyp-oxia occurs simultaneously. Such observations are more pronouncedin eutrophic, stratified lakes and are less obvious in mesotrophic,polymictic lakes such as Lake Simcoe because of their relatively lowTP concentration (Nürnberg et al., 2012).
In general, we attempted to determine (1) the extent of hypoxia,(2) the importance of internal load compared to external load, whichmay be useful in P mass balances and models, and (3) the potentialinternal load effects on water quality concerns, such as cyanobacterialblooms.
We quantified the internal load in a separate study (Nürnberg etal., 2013–in this issue), using several independent approaches includ-ing an in situ estimate from increases of TP concentration throughoutthe summer and fall, and a gross estimate based on the extent of hyp-oxia and experimentally determined anoxic release rates, where P re-lease was measured during laboratory incubations.
Lake Simcoe characteristics and field data
Lake Simcoe can be divided into three distinct sections: the MainBasin with the largest area, Kempenfelt Bay with its fjord-like basinand Cook's Bay with its relatively shallow basin that receives theagriculture and urban affected Holland River (Fig. 1). Even thoughLake Simcoe is relatively deep at a maximum depth of 41 m, the mor-phometric indices of its sections are small because of the large, mostlyshallow areas (Table 1). This index is computed as the mean depth(m) divided by the square root of the area (km, Osgood, 1988). Thehigher the index value the stronger is the stratification in temperatelakes, and areas such as Kempenfelt Bay, with values above 3 m/km,are likely to undergo summer stratification. In contrast, values closeto 1 m/km and below as found in the Main Basin and Cook's Bay indi-cate frequent exchange between the bottom and mixed layers. Cook's
Bay is entirely polymictic while most of the much larger Main Basin isnot deep enough to stratify.
Monitoring data from 2 to 3 stations per basin (Table 1) were usedin this analysis (Young et al., 2010). The stations were sampled every2 weeks during the ice-free season (typically May through October)starting in 1980. In this paper, the period of record is 1980–2011 un-less stated otherwise.
DO and temperature depth profiles, and Secchi disk transparencywere measured at each site (Eimers and Winter, 2005). Compositewater samples through the euphotic zone (lower depth determinedas 2.5 times of Secchi disk transparency) to a maximum depth of15 m were collected with a polyvinylchloride (PVC) hose (fitted
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with a weighted one way check valve that allows water to enter asthe hose descends and traps the water in the hose as it ascends) forchemical and phytoplankton analysis. Starting in 2000 at least oneand in 2009–2011 two to three discrete hypolimnetic P sampleswere taken at 1, 5 or 10 m above the lake bottom with a Kemmererbottle. For 1999–2010 some hypolimnetic samples for metals (totalFe and total Mn) were available and used as indicators of internalload. Water chemistry parameters were measured in the laboratoryusing standard MOE analytical methods (Janhurst, 1998) and phyto-plankton was identified to genus-level (Winter et al., 2011).
Composite euphotic TP concentrations for each of the three lakesections were determined by volume-weighting TP concentrationusing volumes for each station within a section (Table 1). Chlorophylla (uncorrected for pheophytin) and Secchi disk depth had low vari-ability among open-water stations on a given day; therefore, datawere averaged over stations E50, E51, K38, K39, K42, K45, and S15to illustrate annual and seasonal patterns.
There were several important changes affecting water qualityduring the 32-year monitoring period (1980–2011, Nürnberg et al.,2013–in this issue). Probably the most important change was the sub-stantial decrease in external nutrient loading since the 1990s (externalloads for 1990–1997 were 131 t/yr, but external loads for 1998–2006were 70 t/yr). Besides this event, the invasion of the zebra mussel(Dreissena polymorpha) in 1991 and their widespread establishmentby 1996 (Evans et al., 2011) likely affected water clarity (Table 1)and phytoplankton biomass. An additional consideration was thelengthening of the stratification period over these years from 90 to112 days (Stainsby et al., 2011). To assess the influence of these factors,lake characteristics (as averages) of the following two periods were in-vestigated if data were available: (a) 1980–1994 (large external load,no zebra mussel and 90 day stratification period), and (b) 2000–2011(small external load, zebra mussels prolific and 112 day stratificationperiod), besides the long-term average for the entire period of record.
Theory and calculations
Computation of hypoxic factors
While DO contour plots present a visual summary and individualDO vertical profiles reveal detailed information on the oxygen condi-tions in a lake, the hypoxic factor (HF, d/season, Nürnberg, 2004)combines all DO data into one value per year that provides a moreconcise summary of hypoxia. This factor represents the number ofdays in a season or year that a sediment area equal to the lake surfacearea is overlain by hypoxic water.
Extent and duration of hypoxia were quantified by hypoxic factorsfor specific DO thresholds separately for the three lake sections follow-ing Nürnberg (2004). Specific DO thresholds arrive at specific factors;for example, a factor based on a threshold of 7 mg/L DO would repre-sent the annual extent in time and space unsuitable for coldwater fish.If computed using a low DO threshold, HF is also useful in the assess-ment of internal phosphorus load (Nürnberg, 2009), because most Prelease from the sediments is redox-dependent, and low DO in thewater indicates the potential of such release events.
Hypoxic factors were determined for all summers from 1980 to2011 with the following equation (Nürnberg, 2004):
HF ¼ ∑n
i¼1
ti � aiAo
ð1Þ
where ti is the period of hypoxia (days below a critical oxygen thresh-old), ai is the corresponding lake area that is hypoxic (m2), Ao is thelake surface area (m2), and n is the number of periods with differentdepths for the specific hypoxic level considered. In this calculation, DOprofiles of the deepest stations for each lake section (C9, K42, K45;
Fig. 1) were combined with the bathymetric information of each lakesection (provided by the Ontario Ministry of Natural Resources).
Inspection of DO vertical profile data from Lake Simcoe often re-vealed a hypolimnetic layer of hypoxic water of 2.0–3.5 mg/L DO, es-pecially at the stratified stations K42 and K45. To obtain informationabout the different levels of hypoxia, hypoxic factors (HF_2, HF_3and HF_3.5) were calculated for the three DO thresholds of 2, 3 and3.5 mg/L at stations C9, K42 and K45.
Modeled active sediment release factor
A more realistic estimate of the extent and duration of the sedi-ment release area in the well-mixed lake sections (than hypoxic fac-tors that are based on observed DO profiles), is the active sedimentarea factor (AA). This is because in weakly stratified sections, such asCook's Bay and the Main Basin, hypoxic factors based on observedDO profiles are relatively small because of mixing with and aerationby other water layers. But even in such mixed conditions a large sedi-ment surface area can be anoxic during quiescent periods and activelyreleasing phosphorus from sediments. Nürnberg (2005) found thatthe areal extent and time for such active sediment (of any lake, includ-ing polymictic lakes and bays) can be predicted from amodel original-ly developed for the anoxic factor (using a DO threshold of 1–2 mg/L)for stratified lakes (AA, Eq. (2), in units of days per summer, p b 0.001,n = 70, R2 = 67, Nürnberg, 1996).
where for each lake section, TPsummer is the euphotic TP concentration(μg/L) and z/Ao
0.5 is the morphometric factor [z is the mean depth (m)and Ao is the surface area (km2)].
AA was computed for all three sections separately using May toSeptember euphotic TP averages of volumetrically prorated compositesamples from C1, C6, C9 to represent Cook's Bay, K39 and K42 forKempenfelt Bay and E51, K45 and S15 for the Main Basin.
Computation of monthly external loads and flows
The following streams with monitored flows are representative ofthe inflow pattern for the three basins: Lovers Creek for KempenfeltBay, East Holland River for Cook's Bay, and Black and Beaver Riversfor the Main Basin. Long-term average and standard errors of monthlyflows were computed from daily flow estimates.
Seasonal external TP inputs were compared with internal TP loads.Monthly external P loads were computed for the years for whichmonthly values from relevant sources were available. Monthly loadswere summed from individual sources for the three basins (Jan 2004–May 2007) or just Kempenfelt Bay (Jan 1991–May 2007) and includedthe tributary contributions of each lake section's sub-watershed, atmo-spheric and septic system contributions, and loads from waste watertreatment plants (Appendix A).
Statistical analysis
Mann–Kendall trend tests were used to determine monotonictrends over time (defined as variable “year”). In addition, linear re-gression analyses were used to determine whether there were anysignificant linear trends with time. Influential outliers were deter-mined from studentized residuals and Cook's distance measure.
Paired t-tests and repeated measures analyses of variance(RM-ANOVAs), determined whether early summer averages weredifferent from late summer–fall averages for euphotic TP concentra-tion and the phytoplankton biomass indicators. Further, t-tests wereperformed to determine any significant differences in the averages ofHFs and AAs for the period before (1980–1994) and after (1995–2011)major changes in Lake Simcoe.
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Significance levels of 0.05 or lower were reported. Statistical anal-ysis was conducted with the SYSTAT statistical program, version 13for Windows.
Results and discussion
Many conditions can indicate P release from bottom sediments,and they differ depending on whether a lake is thermally stratifiedor not. In Lake Simcoe, we observed that the deep and relativelysmall Kempenfelt Bay had characteristics typical of a stratified lake(Table 2A), while shallow Cook's Bay was typical of a polymicticlake (Table 2B). The Main Basin was deep in some parts, but had alarge area and small morphometric index and displayed instances ofboth stratification and mixing (Table 2A, B).
Indications of hypoxia
Dissolved oxygen concentration and hypoxic factorsContour plots based on DO profiles indicate frequent hypoxia close
to the bottom sediments at the occasionally stratified stations (i.e.,K42, K45, and C9) in the 1980s, before zebra mussel invasion andexternal load abatement (Fig. 2). Close inspection also reveals thathypoxia declined and was less widespread in the more recent years.
Similarly, hypoxia expressed more quantitatively as the hypoxicfactor for DO thresholds below or equal to 2 mg/L, 3 mg/L and3.5 mg/L (HF_2.0, HF_3.0 and HF_3.5) was substantially lower in theperiod after zebra mussel invasion and external load abatement inKempenfelt Bay and the Main Basin, except for 2008–2010 (Table 3,Fig. 3). Mann–Kendall trend tests and linear regression analysis (with“year” as independent variable) revealed that HF_3.5 decreased signifi-cantly in Kempenfelt Bay at a rate of −0.63 d/yr (p b 0.05, R2 = 0.18,n = 32) and in the Main Basin at −0.37 d/yr (p b 0.01, R2 = 0.26,n = 32), but not in Cook's Bay (Mann–Kendall: p = 0.21, linear regres-sion: p = 0.29, R2 = 0.04, n = 32).
Hypoxic factor values increased with increasing DO thresholdat all stations (Table 3, Fig. 3). Even the small increase in the DOthreshold from 3.0 to 3.5 mg/L further increased HF. On many occa-sions since 1997 there seemed to be large volumes of hypoxic waterat 3.0–3.5 mg/L, but only a small amount of water with lower DO inthe deeper waters of all stations (Fig. 2 and individual DO profiles,not shown), although the oxygen consumption rate at the sedimentwater interface is high in Lake Simcoe (Dittrich et al., 2013). Such athick hypoxic layer (rather than a distinct anoxic layer) is unusualin stratified lakes (Nürnberg, 1995) and such extended hypoxia isprobably based on the dynamic nature of the Lake Simcoe watermasses with intense exchange between the sections due to internalseiches and high winds (Bouffard and Boegman, 2011; Cossu andWells, 2013), as expected from the morphometric index.
Table 2Indicators of internal P load in stratified (A) and polymictic lake sections (B).After Nürnberg (2009).
A. Stratified (Kempenfelt Bay)
Severe hypolimnetic hypoxiaProfiles: increasing TP and dissolved reactive P (DRP) with depthSeasonality: increasing hypolimnetic TP and DRP throughout summer, not explicableby external sources
Concomitant iron, manganese or reduced gas developmentFall turnover: blooms, increased turbidity
B. Polymictic (Main Basin and Cook's Bay)
Seasonality: increasing TP and DRP throughout summer in the mixed water layer(even at the surface)
Turnover events during summer: blooms, increased turbidityThin oxic sediment layer; occasional anoxia in weed beds and open water duringquiescent conditions (early morning)
Occasional iron, manganese or reduced gas development during quiescent conditions
Because of the thick hypoxic layer we assumed that the HF_3.5mostresembles the area and extent at which the sediment surfaces are anox-ic and release P as internal loading in the stratified sections of LakeSimcoe, rather than HF_2 that is usually expected to represent the ex-tent of anoxic bottom sediment surfaces in stratified lakes (Nürnberg,2004). Accordingly, HF_ 3.5 was used in one of the models for internalload in the companion paper (Nürnberg et al., 2013–in this issue).
While HF_3.5 and AA should be similar in stratified sections,HF_3.5 is expected to be lower than AA in mixed sections (MainBasin and Cook's Bay), as here it underestimates the extent of sedi-ment anoxia because of frequent exchanges with aerated water.Therefore, modeled factors (AA, Eq. (2)) provide a better estimatefor sediment anoxia (explained above in section Modeled activesediment release factor).
Indeed, HF_3.5 and AA were most similar in stratified KempenfeltBay, where the 1980–2011 average of AA was similar to the averageof HF_3.5. But in the earlier period of 1980–1994, the average of AAresembled the average of HF_3.0, while thereafter annual HF_3.0and HF_3.5 values were much lower, with only occasional valuesclose to AA (Fig. 3, Table 3). In the Main Basin with its low morpho-metric index of 0.60 m/km (suggesting frequent exchange betweenupper and lower water layers), the AA factor was usually higherthan the hypoxic factors based on DO profiles (Table 3, Fig. 3). Inpolymictic Cook's Bay, AA was always higher than the HFs (Table 3,Fig. 3). Further, the high TP concentration predicted AA values evenhigher than in Kempenfelt Bay indicating a large active sedimentarea that may release P in Cook's Bay, while the overlaying waterwas exposed to air during frequent mixing events. Future monitoringin macrophyte stands and diurnal monitoring of DO concentrationclose to the sediment surface may confirm the extent of hypoxia atthe sediment water interface (Table 2).
These patterns can be explained by the fact that AA did not changesignificantly throughout the years (Mann–Kendall tests and regres-sion analysis with “year” as independent variable, p > 0.05 for alllake sections) unlike the hypoxic factors, because lake summer com-posite TP concentration has not changed during these periods (Younget al., 2011) as discussed in section Spatial and temporal pattern ofphosphorus concentration. The observed decrease in the hypoxic fac-tors could be caused by the reduction of external input of nutrientsand probably also of organic matter which may have decreased thelevel of sediment oxygen demand and water hypoxia, even if such ef-fects can lag several years behind restoration efforts (Charlton et al.,1991).
We concluded that before 1996, Kempenfelt Bay reacted like othermesotrophic stratified lakes with respect to TP concentration andmorphometry influenced oxygen depletion, and changes after 1996(Dreissena invasion and reduced external load) had a beneficial effectand decreased hypoxia, despite undetected trends in TP concentra-tions (Young et al., 2011). However, greater hypoxia has been ob-served in the recent years of 2008–2010 at all stations, weakeningthe diminishing trend, and continued monitoring will show whetherthe decrease in hypolimnetic hypoxia is permanent in Lake Simcoe.Similar trends observed in Lake Erie indicated that anoxia decreasedinitially during the invasion of the mussel, but then drastically in-creased to create a large “dead zone” (Smith and Matisoff, 2008).
In summary, the quantification as hypoxic factors revealed a simi-lar decrease of hypoxia since 1995 as the “end-of-summer minimumvolume-weighted hypolimnetic DO” (MVWHDO) determined forK42 and used in empirical models connecting DO with external TPload (Young et al., 2011). Hypoxic factors calculated with a DO thresh-old relevant to the fisheries may also be useful for providing manage-ment directions with respect to fisheries and P load reductions.
Increased metals close to the bottomIron and manganese increased in concentration towards the lake
bottom in the fall before turnover in November (e.g., Kempenfelt
1980 1981 1982 1983 1984 1985 1986 1987 1988
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Fig. 2. Contour plots of DO concentration (mg/L, labels on solid lines) in Kempenfelt Bay (K42), the Main Basin (K45) and Cook's Bay (C9) for 1980–1988 and 2003–2011. Colorsrange from blue for low DO over green to orange and red for the highest concentration.
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Bay, station K42, 2009, Fig. 4). Manganese usually increased earlierin the year and higher in the water-column above the sedimentcompared to iron, reflecting its earlier reducibility compared to iron(at about 400 mV compared to 220 mV, respectively; Stumm andMorgan, 1996). These patterns indicate the sediment origin of thesemetals (being released under different redox conditions). Besidesthe indication of hypoxia, iron release also indicates the potentialfor P release, because the reduction of sediment iron releases any
Table 3Hypoxic factor averages (d/summer; Eq. (1)) calculated from profiles for three thresh-olds and modeled active sediment area factor (AA; Eq. (2)). “T-test” refers to signifi-cance levels of t-test between periods 1980–1994 vs 1995–2011; n.s., not significant;1980–1994 is the period before invasion of the zebra mussel and external TP loadabatement.
phosphate that may be adsorbed to sediment iron oxy-hydroxides(as long as the solubility product for ferrous phosphate formationssuch as vivianite is not exceeded, which can occur in hypereutrophicsediments). Elevated dissolved iron concentrations were also foundin experimental release rate studies with Lake Simcoe sediments(Loh et al., 2013).
While these increases in bottom iron concentration support theinternal load hypothesis, concentrations are not high enough to resultin any P re-adsorption upon aeration (Nürnberg, 1985). Physical ad-sorption is highly dependent on dilution and P-limited phytoplanktoncan outcompete the adsorption processes in many circumstances ofthermocline erosion, fall turnover mixing and polymixis.
Chironomid densitiesChironomids are indicative of anoxic conditions in the surficial
sediment. For example, chironomid head capsules were used tohind-cast the extent of anoxia as the anoxic factor in paleolimnologicalstudies (e.g., Quinlan and Smol, 2002). A comparison of macrobenthosbetween 2008 and earlier years in Kempenfelt Bay and the Main Basinrevealed that overall chironomid abundance was lower in 2008 thanin 1983 and 2005, but greater than in 1926, while biomass increasedas individual organisms became larger, indicating low oxygen condi-tions (Jimenez et al., 2011). Similarly, total macrobenthos and otherspecies that are sensitive to oxygen depletion, such as oligochaeta,decreased. This is another indication of variable anoxia on sedimentsurfaces since 1983 even if the overlaying water may not always beanoxic at such times.
Similarly, paleolimnological studies on chironomid-based inferencesrevealed that the largest DO declines in Lake Simcoe correspondedto urban development (~1960–1990), but recent (since 2000) resultsshowedmodest improvements in water quality, although water qualitywas still degraded relative to pre-disturbance conditions (Rodé, 2009).
Fig. 3. Hypoxic factors (HF) for DO levels of 2.0, 3.0 and 3.5 mg/L, and modeled activesediment area factor (AA) in the three sections of Lake Simcoe. Changes in externalload and zebra mussel abundance (Dreissena) are indicated by weighted arrows.
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Fig. 4. Total iron (TFe) and total manganese (TMn) profiles at Kempenfelt Bay (K42) in2009 (early summer, dotted line; fall, solid lines; after fall turnover, broken line). Thetop two values are from the euphotic zone composite samples (plotted at the surfaceand the bottom of the euphotic zone), and the three bottom points are from discretesamples.
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Spatial and temporal pattern of phosphorus concentration
Spatial and temporal patterns of total P (TP) and dissolved or solublereactive P (DRP or SRP) can indicate internal loading (Steinman et al.,2009). Specifically, DRP is not usually present in large amounts (e.g.,>15 μg/L) in the mixed water layers during the growing season ofmesotrophic lakes, unless recently released from sediments (Table 2).
Almost all TP data for Lake Simcoe since 1980 are based on eupho-tic composite water samples taken from the surface to a depth of 2.5times the Secchi disk transparency to a maximum depth of 15 m. Be-cause Secchi transparency varied spatially and temporally, the com-posite samples were taken at varying depths. If there was anyinternal P load from the bottom sediments, the deeper compositeswould have exhibited elevated TP concentrations. Thus the compositesamples may include some internal load even during the stratified pe-riods in Kempenfelt Bay and the Main Basin.
There has been no long-term trend in composite TP concentrationat most lake stations since 1980 (Young et al., 2010), despite thedecrease in external load since 1998. Such a lack of response to exter-nal load abatement usually results from increased flux out of the sed-iments as an internal P load (Larsen et al., 1981; Marsden, 1989).Theoretically, it could also be due to a decrease in the proportion
of external P load that settles to the sediment, which could occurwhen the composition of external P inputs changes (e.g., a larger pro-portion is dissolved). While there are no DRP loading data availablethe evidence of internal load presented here supports the first expla-nation, despite observed decreases in hypoxia.
Euphotic TP concentration typically decreased from the spring run-off in April to low levels in the summer and increased in the fall,starting in August (long-term average by month, Fig. 5). Differencesbetween average composite TP concentration of July versus Oct/Novwere highly significant in the stratified sections (t-test, p b 0.0001,n = 33 for Kempenfelt Bay and the Main Basin) but marginally signif-icant in polymictic Cook's Bay (p b 0.05, n = 29). These fall increasesmay be due to entrainment of P-enriched hypolimnetic water duringthermocline erosion and fall turnover, particularly in the stratifiedlake sections. (Accordingly, seasonal TP increases were used as ap-proximate estimates of internal load (Nürnberg et al., 2013–in thisissue)).
Increasing hypolimnetic TP concentration throughout the summerand in the fall is often attributable to internal load, especially whenhypoxia occurs at the same time and depth. Most hypolimnetic TPsamples taken at discrete depths below 27 m at station K42 wereelevated in comparison to composite euphotic samples (Fig. 6) andwere higher the closer the samples were located to the bottom sedi-ments, indicating sediment P release in Kempenfelt Bay.
Elevated TP in hypolimnetic samples taken at discrete depths inK42 and K45 in combination with hypoxic conditions was previouslydescribed as an indication of sediment P release in Lake Simcoe (in1990 and 1991; Nicholls, 1995). Other observations showed
Fig. 5.Monthly averages of euphotic zone composite TP concentration in the three Lake Simcoe areas, prorated by volume (1980–2011, lines on top of bars indicate standard errors).
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progressive increases in TP and iron concentrations and decreasing DOat depths of 1 m and 5 m above the lake bottom at station K42 (in1998–1999; Eimers and Winter, 2005). In these studies deep water Pwas elevated when DO was approximately 3–4 mg/L at 1 m abovethe bottom.
Although no DRP depth profiles are available to investigatehypolimnetic concentration changes directly, there were some signsof internal loading related to DRP concentrations. Elevated DRP in thesummer hypolimnion would be distributed throughout the mixedwater layer during periods of thermocline erosion and destratificationat the end of summer and fall and may be analyzed as DRP in the com-posite sample, before phytoplankton could incorporate it and turn itinto organic and particulate P. Therefore, elevated fall DRP concentra-tion in the mixed layer would be another indication of hypolimnetic Pincreases in the preceding summer (Table 2). Indeed, DRP concentra-tions were occasionally elevated above 15 μg/L at the intermittentlystratified stations (K38, K39, K42, K45, C9), especially in the fall of theyears before 1997 (Appendix B: Elevated DRP). In contrast, and asexpected, there was no increased fall in DRP in shallow mixed Cook'sBay stations (C1, C6), which had increased DRP throughout the sum-mers until 1996, possibly a reflection of elevated input from externalpoint sources before load reduction.
Occasional discrete samples from 5 or 10 m above the bottom atK42 between 2000 and 2008 showed slightly elevated DRP concen-trations, to a maximum of 18 μg/L at 5 m above the bottom (17 Sep2003) and 13 μg/L at 10 m above the bottom (18 Sep 2000). Elevateddissolved P concentrations were also found in anoxic release ratestudies with Lake Simcoe sediments (Loh et al., 2013).
Fig. 6. Kempenfelt Bay (K42) TP concentration for discrete-depth samples below 27 m(broken line), and euphotic zone composite samples (surface down to 15 m; solid line)for the period 2000–2011.
External input
The timing of internal P fluxes in late summer and fall can be usedto distinguish internal from external inputs. In particular, seasonal ormonthly patterns of external loads were examined to determinewhether increases in lake TP concentration can be explained by exter-nal sources alone or whether there are indications of an alternatesource such as internal load.
Long-term average monthly flows of Lovers Creek (representingKempenfelt Bay), East Holland River (Cook's Bay), and Black andBeaver River (Main Basin) were lowest in July, August and September(Fig. 7).
Similar to inflows, external TP inputs (Appendix A) were smallestin the summer and early fall, declining from March to October, basedon 17 years of data for Kempenfelt Bay (Fig. 8, upper panel). The samepattern occurred in the other two lake sections, based on observa-tions for three years (Fig. 8, lower panel). This suggests that generallythe late summer and early fall water quality was least affected byexternal nutrient input. Consequently, increases in TP and deteriorat-ing water quality at that time were likely caused by internal P loadingsimilar to conditions in the large, shallow Lake Balaton, Hungary(Istvanovics et al., 2004).
Internal P load and phytoplankton
The timing of internal loading in late summer and fall made itespecially suitable as fertilizer for phytoplankton in the open waterof Lake Simcoe, because external inputs were relatively low (Fig. 8).Sediment P is released as highly bioavailable phosphate (Nürnbergand Peters, 1984) directly into the bottomwater without any associat-ed water inputs probably creating the observed pattern of fall TP con-centration increases in the deeper sections (Fig. 5). From there it getsdistributed throughout the water column, depending on mixing con-ditions. Anoxic P release can be expected to occur during hypolimneticstratification in stratified bays and during stagnant periods of relative-ly high temperature (which enhances sediment oxygen demand andrelease rates, Liikanen et al., 2002) in the mixed sections of LakeSimcoe. Because of their lowmorphometric ratio a frequent exchangebetween surface and bottom water is expected. Consequently, the in-fluence of internal loading on phytoplankton should be largest in thesummer and fall and the following sections investigate whether sucha pattern existed indeed, for (1) the algal pigment chlorophyll a,(2) Secchi transparency, and (3) phytoplankton biomass and speciescomposition. If, instead, there was no internal load, a more even sea-sonal distribution of phytoplanktonwould be expected, as determined
Fig. 7. Monthly flow of representative rivers (1980–2009).
267G.K. Nürnberg et al. / Journal of Great Lakes Research 39 (2013) 259–270
in a study that compared seasonal chlorophyll patterns in lakes withdiffering trophic states (Marshall and Peters, 1989).
ChlorophyllChlorophyll a often serves as an indicator of algal biomass and
phytoplankton blooms. Chlorophyll averages for the Aug–Oct periodwere consistently higher than those for the May–July period (Fig. 9,long-term 1980–2011 average 2.70 μg/L versus 1.77 μg/L) and thepairwise t-tests as well as analyses of variance (RM-ANOVAs), werehighly significant (p b 0.0001).
Secchi disk transparencySecchi disk transparency reflects turbidity and color due to pig-
ments of phytoplankton, natural chromophoric organic acids, detritus,
0
500
1,000
1,500
2,000
2,500
Ext
ern
al T
P lo
ad (
kg/m
on
th)
0
2,000
4,000
6,000
8,000
10,000
12,000
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Ext
ern
al T
P lo
ad (
kg/m
on
th)
Kempenfelt
Main
Cook's
Fig. 8. Total monthly external TP load (average and standard error) to Kempenfelt Bayfor 17 years from Jan 1991–May 2007 (upper panel) and for all three lake sections for3 years from Jun 2004–May 2007 (lower panel).
silts and clays. In Lake Simcoe open water, there was little color andorganic acids and turbidity were low, except for occasional “whiting”events when calcium precipitation occurred during warming periodsand produced low transparency in the early summer (Young et al.,2010). Therefore, we assumed that most of the variability in Secchitransparency (especially increases in the late summer and fall) wasdue to phytoplankton biomass. Of all months, August and Septemberexhibit the lowest transparency most consistently, followed byOctober (data not shown). Averages for the Aug–Oct period wereconsistently lower than those for the May–July period (Fig. 9, long-term 1980–2011 average 4.74 m versus 6.31 m) and the pairwiset-tests as well as RM-ANOVAs, were highly significant (p b 0.0001,n = 32). May transparencies were low in the early years (1980–1991) but have been extremely high since then (to a maximum of12 m inMay 2005, data not shown). Transparency was relatively con-stant, between 2 and 6 m before 1995, the year when Dreissena invad-ed Lake Simcoe. Since then, transparency has increased dramaticallywith monthly averages between 4 and 12 m. However since 2000,August and September open-water averages leveled off at about5.5 m, well below the early summer monthly averages. Similar obser-vations of a strong seasonal pattern were made by Guan et al. (2011).
Phytoplankton biomass and speciesMonthly phytoplankton counts were available for several growing
seasons between 1971 and 2009. While the long-term trend indicatesa decline in cyanobacteria biomass since 1992, seasonal patterns did
0
2
4
6
8
10
1980 1985 1990 1995 2000 2005 2010
Sec
chi (
m),
Chl
orop
hyll
(µg
/L)
Secchi 5-7 Secchi 8-10 Chl 5-7 Chl 8-10
Fig. 9. Chlorophyll a (Chl) and Secchi disk transparency averages (stations E50, E51,K38, K39, K42, K45, and S15) for months May to July (5–7) and August to October(8–10), 1980–2011.
268 G.K. Nürnberg et al. / Journal of Great Lakes Research 39 (2013) 259–270
not change. Maximum biomass occurred in August and September asevident from absolute and percentage (of total phytoplankton bio-mass) cyanobacteria data in Kempenfelt Bay (Fig. 10A). Even recently,some biomass was high enough to indicate fall blooms (e.g., in 2006,2007, 2009). A similar pattern is apparent for the Main Basin stationK45 (Fig. 10B) and other open water stations (not shown).
Comparison of cyanobacteria biomass with internal P loadCorrelations based on 13 years of available phytoplankton bio-
mass data (August–October averages) with internal load estimates
Fig. 10. Monthly cyanobacteria biomass averages (Apr–Nov) for (A) the Kempenfelt Bay stamass for K42 (graph inset), and (B) the Main Basin station K45 (1971–2009, month numbe
presented in Nürnberg et al. (2013–in this issue) are not significant.However, the averages for 1980–1992 and 1997–2009 indicate simul-taneous decreasing trends of both cyanobacteria biomass and internalloads estimated as in situ and RR × HF (Fig. 11). Any dependency ofbiomass on internal loading is obscured by simultaneous decreasesin external load and increases in transparency (Table 1;section Secchi disk transparency). Yet, external loads possibly haveless influence because they were relatively small during the periodof internal loading in the late summer even before 1997 (Fig. 8) andare usually in a less bioavailable form (Nürnberg, 2009).
tions K39 (1975–1993) and K42 (1980–2009) and percent of total phytoplankton bio-r on right axis).
Fig. 11. Comparison of Aug–Oct cyanobacteria biomass, hypoxic factor (HF_3.5) andthree estimates of internal load in Kempenfelt Bay for the two different time periods. In-ternal loads were determined from summer–fall euphotic TP increases, in situ; as theproduct of HF_3.5 and P release rate, RR × HF_3.5; and as the product of AA and Prelease rate, RR × AA (Nürnberg et al., 2013). Only years with available cyanobacteriaestimates are included in means and SE (first bar, 1980–1992: 7 years, second bar,1997–2009: 5 years).
269G.K. Nürnberg et al. / Journal of Great Lakes Research 39 (2013) 259–270
In summary, there is evidence in many years that phytoplank-ton biomass and in particular cyanobacteria increased throughoutthe summer and peaked in August–September and occasionally inOctober, based on Secchi disk transparency readings, chlorophyll aconcentrations, and phytoplankton biomass. Even though much ofthis evidence of internal load is circumstantial, it is supported bythe seasonal patterns of external inputs. External P loads are typicallylow during the late summer and fall months, so that these fall bloomsmay have been maintained by biologically available P release fromanoxic sediments. The positive effect on cyanobacteria could be en-hanced by concomitant release of ferrous iron that can stimulate thegrowth of some cyanobacteria (Molot et al., 2010). Similar observa-tions exist in Missisquoi Bay, a large wind-mixed bay of Lake Cham-plain, where redox-related P concentrations were correlated withcyanobacteria cell counts (Smith et al., 2011).
Conclusions
There is abundant circumstantial evidence that Lake Simcoe expe-rienced internal P load at least in the Main Basin and stratifiedKempenfelt Bay, the strongest being the wide spread hypoxia. It islikely that sediment release also occurred in polymictic Cook's Baybecause of a long history of external nutrient input that potentiallyincreased the releasable P fraction in the sediment (Hiriart-Baer etal., 2011; Loh et al., 2013) and the relatively warm temperatures thatenhance oxygen demand and release rates (Liikanen et al., 2002).Nürnberg et al. (2013–in this issue) estimated in situ internal loadingrates of 45 to 89% of external loads and hence, internal loading is a rel-atively important source of P in Lake Simcoe.
The effect of internal P loading on the water quality of Lake Simcoeis especially evident when considering the timing of algal andcyanobacterial blooms in the late summer and fall as observed by Secchitransparency decreases, and chlorophyll and biomass increases.
Acknowledgments
This work was funded by Environment Canada's Lake SimcoeClean Up Fund. Bruce LaZerte's helpful involvement throughout thestudy is greatly appreciated as are comments and encouragementfrom several anonymous reviewers.
Appendix A. Supplementary data
Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.jglr.2013.03.016.
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