Please cite this article as: Bramburger, A.J., Reof the Laurentian Great Lakes, J. Great Lakes
a b s t r a c t
a r t i c l e i n f o
Article history:Received 27 December 2015Accepted 2 July 2016Available online xxxx
Communicated by Joseph Makarewicz
Phytoplankton biomass and primary productivity within Great Lakes deep chlorophyll layers (DCL) remainlargely uninvestigated. Consequently, the taxonomic makeup of DCL phytoplankton communities, as well asthe mechanisms regulating their formation and maintenance, is poorly understood. We examined 6 years ofphytoplankton compositional characteristics of Great Lakes summer DCL and epilimnetic communities as wellas spring communities from isothermal water columns. DCLs were regularly observed during summer stratifica-tion in all lakes with the frequent exception of Lake Erie. Relative compositions of summer chlorophyte andcryptophyte assemblages were not different between the epilimnion and DCL, but DCL phytoplankton commu-nities from other algal groups were distinct from their epilimnetic counterparts and comprised an integrationof phytoplankton from the overlying epilimnetic assemblages and relict taxa characteristic of spring. Summerepilimnetic communities were characterized by higher abundances of cyanophytes, and centric diatom commu-nities were dominated by Cyclotella sensu lato (i.e. species within Cyclotella and closely related genera). Cyclotellaspecies exhibited distinct patterns of vertical distribution, with small-bodied taxa being partitioned heavily intothe epilimnion, while larger-bodied forms tended to occupy the DCL. Vertical size partitioning was exemplifiedby larger mean individual cell sizes in epilimnetic siliceous algae (diatoms and chrysophytes) in the DCL com-pared to the epilimnion, while the opposite pattern was exhibited by cyanophytes. These findings demonstratethe importance of stratification intensity to vertical structuring of summer phytoplankton communities andimply that changing stratification regimes (such as that due to recent climate change)may exert profound effectson Great Lakes primary producer communities.
Index words:Great LakesLong-term monitoringPhytoplanktonAlgal ecology
Introduction
In water bodies that exhibit seasonal or permanent stratification,deep chlorophyll layers (DCL) (Fahnenstiel et al., 1984; Moll et al.,1984) often occur in the water column below the thermocline (Brooksand Torke, 1977; Pilati and Wurtsbaugh, 2003). While the DCL mayrepresent a large portion of thewater column chlorophyll and can be re-sponsible formuch of the primary production of a lake, themechanismsgoverning the general composition and dynamics of the DCL remainlargely uninvestigated (Camacho, 2006; Moll and Stoermer, 1982;Pilati and Wurtsbaugh, 2003). There remain several potentially validhypotheses regarding mechanisms that influence the formation andmaintenance of the DCL. These include active processes such as in situproduction in the metalimnion and hypolimnion (Cullen, 1982;Fasham et al., 1985; Venrick, 1982) and decreased gazing pressurebelow the thermocline (Fee, 1976), as well as active light and/or
er).
es Research. Published by Elsevier B
avie, E.D., A comparison of phRes. (2016), http://dx.doi.org
predation avoidance by motile taxa (Campbell et al., 2009; Fiedler,1982; Saros et al., 2005). Alternatively, DCL formation can be drivenby passive mechanisms, including formation of a relict community fol-lowing stratification and differential sinking of phytoplankton fromthe epilimnion (Kiefer and Kremer, 1981).
When they occur, DCLs can vary considerably in their taxonomiccomposition and structure (Cullen, 1982; Cullen and Eppley, 1981),and this can confound indirect measures of DCL productivity. Chloro-phyll a concentrations estimated by in situ fluorescence, not necessarilya reliable indicator of phytoplankton biomass (Falkowski and Kolber,1995), may be affected by several factors and can exhibit substantialheterogeneity both through space and among taxa (Yilmaz et al.,1994). Cullen (1982) cautioned that chlorophyll a profiles provide lim-ited information regarding mechanisms that regulate DCL formationand maintenance. Taxonomic investigations of phytoplankton commu-nities in both the DCL and overlying waters are necessary in order tounderstand the role of the DCL in vertical community structure andfunction.
Comprehensive taxonomic studies can provide insight into the im-portance of DCLs in contributing to overall water column productivity
.V. All rights reserved.
ytoplankton communities of the deep chlorophyll layers and epilimnia/10.1016/j.jglr.2016.07.004
2 A.J. Bramburger, E.D. Reavie / Journal of Great Lakes Research xxx (2016) xxx–xxx
as well as food web function and potentially as an indicator of climatechange effects on water column stratification. Although relationshipsbetween algal productivity, carbon uptake, and DCL algal communitieshave been investigated in marine systems (e.g., Jochem and Zeitzschel,1993; Shulenberger and Reid, 1981; Veldhuis et al., 1997), relatively lit-tle work has been conducted on DCL productivity in lakes (Fee, 1976).Planas (1990, 1973) showed that metalimnetic carbon assimilationrates can often be higher than those observed in the epilimnion. Currentunderstanding of what taxa are responsible for DCL productivity is min-imal (Camacho, 2006). Several authors have described deep, maximalabundances of eukaryotic algal groups (e.g., Barbiero and Tuchman,2004, 2001; Fahnenstiel et al., 1989; Pick et al., 1984; Wolin andStoermer, 2005)within theDCL,while cyanophytes have been implicat-ed as the primary component of DCL communities in other systems(Craig, 1987; Gervais et al., 2003; Kasprzak et al., 2000). Low grazingpressures in the metalimnion (Work and Havens, 2003) can providerefugia for palatable algal taxa capable of existing under low-light con-ditions (Gasol et al., 1992) and favor biomass accumulation of theseforms in the DCL during stratification (Naselli-Flores and Barone,2003). Whether these mechanisms exert sufficient influence toconstrain the development of a DCL-specific algal community acrossmultiple lakes is unknown.
The existence of DCL-specific assemblages could provide a usefulindicator of prolonged stratification periods that could be linked todata from paleolimnological reconstructions. For instance, increasesin Cyclotella sensu lato (including taxa from the genus Cyclotella andclosely related genera) taxa in the Great Lakes (Chraïbi et al., 2014)and in other northern lakes (e.g., Leavitt et al., 2009; Rühland et al.,2008) appear to be related to increasing atmospheric temperaturesthat are changing the physical characteristics of lake stratification.This group includes species from the genus Cyclotella and otherclosely related genera. Examples from the Laurentian Great Lakesinclude Cyclotella comensis Grunow, Discostella pseudostelligera(Hustedt) Houk and Klee, and Cyclotella cf. delicatula Reavie andKireta. This paleolimnological shift may be related to changing as-semblage characteristics of Great Lakes DCLs, but to date, no evalua-tion supports such a hypothesis.
Deep chlorophyll layers have been reported from the Great Lakes(Putnam and Olson, 1966; Watson et al., 1975) and have been studiedprimarily within Lakes Superior (Barbiero and Tuchman, 2001; PutnamandOlson, 1966;Watib et al., 1975;White andMatsumoto, 2012),Mich-igan (Fahnenstiel and Scavia, 1987; Scavia and Fahnenstiel, 1987), andHuron (Barbiero and Tuchman, 2001; Fahnenstiel and Carrick, 1992).To date, investigations of DCLs within the Great Lakes have been limitedto single lakes and short temporal durations. Fahnenstiel and Scavia(1987) provided a synopsis of the DCL community of Lake Michiganand its temporal trends from 1982 to 1984, while Twiss et al. (2012a)described growth and loss rates in phytoplankton communities in LakeOntario. Barbiero and Tuchman (2001) broadly summarized physical,chemical, and biological properties of DCLs in the Great Lakes based ona single season dataset (1998).
We compared and contrasted the composition and structure of phy-toplankton communities from the spring isothermal water column andsummer epilimnia and DCLs of the Great Lakes during the period span-ning 2007–2012, and evaluated dissimilarities between epilimnetic andDCL phytoplankton assemblages at the basin scale in order to determinewhether a characteristic DCL community exists within the Great Lakes.We also described general biovolume and abundance characteristics forepilimnetic and DCL assemblages in order to provide initial insight intothe relative contributions of DCL assemblages to the overall Great Lakesphytoplankton community. We hypothesize that the phytoplanktonassemblages of Great Lakes DCLs are compositionally distinct fromcorresponding epilimnetic assemblages. We further anticipate that thesame suite of taxa contributes to this dissimilarity across lakes.Additionally, we hypothesize that size differences exist betweenconspecific occupants of the DCL and epilimnion.
Please cite this article as: Bramburger, A.J., Reavie, E.D., A comparison of phof the Laurentian Great Lakes, J. Great Lakes Res. (2016), http://dx.doi.org
Methods
Sampling site locations and sample collection
A total of 1034 phytoplankton samples were collected from 71 sta-tions within the Great Lakes during a series of twice-annual cruises(April and August 2007–2012) by the R/V Lake Guardian as part of theUSEPA-GLNPO Monitoring Program (Fig. 1). Water quality parameters(temperature, specific conductivity, pH, irradiance, dissolved oxygen,turbidity, chlorophyll a by fluorescence) were measured in situ using aSeaBird 911 CTD equipped with auxiliary sensors. Additional parame-ters (total phosphorus, nitrates + nitrites, silica) were measuredaccording to methods described in detail by in the USEPA (2010) stan-dard operating procedure. Phytoplankton samples were collected si-multaneously with water quality measurements via Niskin bottlerosette. Integrated samples collected in spring (381) were producedby combining samples from discrete depths through the water column.Summer integrated epilimnetic samples (385) were produced by com-bining samples from discrete depths above the thermocline (surface,5 m, 10 m, 20 m), while summer DCL samples (268) were taken froma single discrete depth associated with the fluorescence-inferredchlorophyll a maximum below the thermocline at each site (USEPA,2010). When no DCL was detected at summer stations, only integratedepilimnetic samples were collected. Spring sampling cruises occurredannually in April, while summer cruises took place annually in August.This study is based on data from samples collected during the 2007–2012 cruises.
Sample preparation and algal enumeration
Whole-water phytoplankton samples were preserved with Lugol'siodine solution and returned to the laboratory for taxonomic analysis.Subsamples for soft-bodied algal analysis were loaded into Utermöhl(1958) counting chambers for inverted light microscope (LM) analysis.Diatom samples were subjected to digestion with heated 30% H2O2.Cleaned diatom material was mounted on coverslips and countedunder LM. Diatom and soft algae (all non-diatom and non-siliceousgroups) samples were enumerated along transects until a total countof 250 entities for soft algae or 500 diatom valves was achieved. Bothdiatoms and soft algae were identified to the lowest taxonomic levelpossible. For diatoms, identification was to species or variety, whileidentification was to species, and occasionally genus for soft algae. Upto 10 individuals of each taxonweremeasured (length,width, depth, di-ameter as applicable) in order to determine taxon-specific individualbiovolume (cell size) (Reavie et al., 2010). Count and measurementdata were used to calculate cell density, species-relative abundance,biovolume, and individual cell biovolume. These counting methodsfollow the standard GLNPO phytoplankton enumeration techniquesoutlined by USEPA (2010). Additional details of sample processing areprovided by Reavie et al. (2014a).
Statistical analysis
Paired-sample t-tests were used to examine differences in waterquality parameters between summer epilimnetic and DCL samples. Aseries of one-way analyses of variance (ANOVA) were used to evaluatedifferences in mean phytoplankton taxonomic richness, density, andbiovolume among spring integrated (SprINT), summer epilimnetic(SumEPI), and summer DCL (SumDCL) phytoplankton samples. Weemployed non-metric multidimensional scaling (NMDS), coupled withanalysis of similarity (ANOSIM) in order to visualize and quantify dis-similarities among spring and summer epilimnetic and summer DCLphytoplankton assemblages within each lake. Similarity percentages(SIMPER; per Clarke, 1993)were used to evaluate species' contributionsto assemblage dissimilarities. We used repeated-measures analysis ofvariance (rANOVA) and paired-sample t-tests in order to examine
ytoplankton communities of the deep chlorophyll layers and epilimnia/10.1016/j.jglr.2016.07.004
Fig. 1.Mapof the Great Lakes showing EPA-GLNPOphytoplankton/water quality sampling stations. Each station is sampled twice annually (early spring andmid-summer) by the R/V LakeGuardian.
3A.J. Bramburger, E.D. Reavie / Journal of Great Lakes Research xxx (2016) xxx–xxx
differences in species-specific individual biovolume (cell-size) amongspring integrated and summer epilimnetic and DCL assemblages.
Results
General observations
Deep chlorophyll layers were observed with varying frequency, andat different depths across the Great Lakes (Table 1). In general, physicaland chemical water quality parameters had few significant differencesbetween mean values for summer epilimnetic and DCL samples, withthe exceptions of temperature and photosynthetic irradiance, whichare both higher, unsurprisingly, in the epilimnion (Fig. 2A). Mean chlo-rophyll a is typically higher in the DCL than in the epilimnion but onlysignificantly so in Lake Michigan and Lake Huron (Fig. 2B). Lower pHwas typical in the DCL, significantly so in Lake Ontario and Lake Erie.Dissolved oxygen was higher in the DCL, with the exception of LakeErie, which showed no difference. Turbidity was significantly higher inLake Erie's epilimnion with no difference apparent in the other lakes.Higher nitrates + nitrites occurred in the DCLs for Lake Michigan andLake Ontario.
The upper Great Lakes (Superior, Michigan, Huron) display differentpatterns of phytoplankton species richness and density than the lowerLakes (Erie, Ontario) (Fig. 3). Mean taxonomic richness was lower insummer samples (SumEPI and SumDCL) than in spring samples(SprINT) for the upper lakes (Superior F = 22.04, p b 0.001, MichiganF = 7.40, p = 0.008, Huron F = 76.97, p b 0.001). No significant
Table 1Occurrence frequency and depth of DCLs sampled.
Please cite this article as: Bramburger, A.J., Reavie, E.D., A comparison of phof the Laurentian Great Lakes, J. Great Lakes Res. (2016), http://dx.doi.org
differences in richness were detected between SumEPI and SumDCLsamples in any of these lakes (p N 0.05). In the lower lakes, richnesswas higher in the summer than spring samples (Erie F = 5.29, p =0.006, Ontario F = 31.44, p b 0.001). In Lake Erie, SumDCL samplesexhibited mean richness values intermediate to spring and summerepilimnetic samples (Fig. 3).
Mean phytoplankton densities were higher within summer samples(SumEPI and SumDCL) than in spring samples in all lakes (F N 17.76,p b 0.001, Fig. 3). Summer epilimnetic phytoplankton densities weretypically higher than densities in the DCL. Lake Michigan, however, ex-hibited highermean phytoplankton density in the DCL than in the sum-mer epilimnion (Student's t, p = 0.002). Phytoplankton biovolumegenerally followed a trend similar to that of density (Fig. 3), with the ex-ception of Lake Erie, which exhibited no differences in mean biovolumeamong spring (SprINT) and summer (SumEPI and SumDCL) samples(F = 2.81, p = 0.062). Increases in density and biovolume wereaccounted for primarily by increases in soft-bodied algal abundanceduring the summer sampling season.
A repeated-measures ANOVA showed that significant differencesexisted in mean taxon-specific individual biovolume (cell size) amongspring integrated samples, summer DCL, and summer epilimnetic sam-ples for species that were observed in all three sample types (F= 8.68,p = 0.0002). Post-hoc Student's t-tests showed that taxon-specific cellsizes were larger in spring integrated samples than in either summerDCL (p = 0.023) or summer epilimnetic samples (p b 0.0001). Cellsizes in summer DCL samples were larger than conspecifics in summerepilimnetic samples but not significantly so (p = 0.061). When thisanalysis was performed for specific algal divisions, significant differ-ences among spring, summer DCL, and summer epilimnetic sampleswere observed in the chlorophytes (F=4.57, p=0.013), chrysophytes(F = 8.74, p = 0.0003), cryptophytes (F = 101.04, p b 0.0001), andcyanophytes (F = 3.26, p = 0.048). Among the chlorophytes andcryptophytes, cell sizes were larger in spring samples than in eithersummer sample group. Among chrysophytes, summer DCL samplescontained larger-celled individuals than either the spring integrated orsummer epilimnetic sample. The opposite pattern was observed in thecyanophytes (Fig. 4).
ytoplankton communities of the deep chlorophyll layers and epilimnia/10.1016/j.jglr.2016.07.004
4 A.J. Bramburger, E.D. Reavie / Journal of Great Lakes Research xxx (2016) xxx–xxx
Of course, not all species occurred in all three sample sets. A paired-sample t-test examining differences in taxon-specific cell size in taxathat occurred in both summer DCL and epilimnetic samples (regardlessof presence in spring samples) indicated no significant differences(t = −0.629, p = 0.53). Rather, cells within a given species were thesame biovolume in both the summer epilimnion and DCL. However,among the major algal divisions, cell size was larger in the DCL than inthe epilimnion for siliceous algae groups (centric diatoms t = 12.10,p b 0.001; pennate diatoms, t = 57.28, p b 0.001; chrysophytes, t =49.85, p b 0.001) (Fig. 4). In contrast, mean cell size was lower in DCLthan in epilimnetic samples for cyanophytes (t = 48.22, p b 0.001),and no significant difference in cell size was observed between DCLand epilimnetic samples for chlorophyte (t = 0.75, p = 0.39) andcryptophyte (t = 1.12, p = 0.29) taxa.
Fig. 2. A. Summary of general water quality parameters for Great Lakes summer epilimneticrepresent the 95% confidence interval of the mean. A * denotes significant difference betwturbidity concentrations for Great Lakes summer epilimnetic and DCL samples from 2007 to 2the mean. A * denotes significant difference between INT and DCL samples (paired-sample t-te
Please cite this article as: Bramburger, A.J., Reavie, E.D., A comparison of phof the Laurentian Great Lakes, J. Great Lakes Res. (2016), http://dx.doi.org
Relative biovolume contributions of major algal groups differedbetween spring and summer and between epilimnetic and DCL samplesduring the summer for all lakes (Fig. 5). Notably, cryptophytesand pyrrophytes represented large portions of the biovolume ofphytoplankton in the upper lakes (Superior, Michigan, Huron) duringthe unstratified spring season. Centric diatoms, especially Aulacoseiraislandica represented the majority of Lake Erie's spring biovolume. Inall lakes (except Huron), relative cyanophyte biovolume increased inthe summer andwas partitioned primarily into the epilimnion. Pennatediatoms also became more important during the stratified period inLakes Michigan, Erie, and Ontario, and were partitioned primarily intothe DCL (Fig. 5).
NMDS, ANOSIM, and SIMPER techniques revealed assemblagedissimilarities among algal assemblages from spring and summer
(INT) and DCL samples from 2007 to 2012. Columns represent mean values. Error barseen INT and DCL samples (paired-sample t-test, p ≤ 0.05). B. Summary of nutrient and012. Columns represent mean values. Error bars represent the 95% confidence interval ofst, p ≤ 0.05).
ytoplankton communities of the deep chlorophyll layers and epilimnia/10.1016/j.jglr.2016.07.004
5A.J. Bramburger, E.D. Reavie / Journal of Great Lakes Research xxx (2016) xxx–xxx
integrated epilimnetic samples, and summer DCL samples. Pronouncedseasonal shifts in epilimnetic algal community composition wereobserved in all lakes, alongwith frequent differences in vertical distribu-tion of taxa during the stratified season. During the spring, the epilimni-on was typically dominated by centric diatoms across all lakes. Specieswithin the genera Aulacoseira and Stephanodiscus were particularlyabundant in these assemblages. Summer epilimnetic assemblagesshowed higher relative abundance of taxa within the genus Cyclotellasensu lato and pennate diatom taxa including Fragilaria crotonensis,Synedra filiformis, and Synedra radians. SumDCL assemblage samplestended to cluster between SprINT and SumEPI samples in NMDS ordina-tions and contained taxa characteristic of both epilimnetic assemblages.A more in-depth description of lake-specific patterns is given below.
Lake Superior
In Lake Superior, the most abundant taxa in spring integrated sam-ples (by biovolume) were Gymnodinium helveticum, Cryptomonasreflexa, Cryptomonas erosa, Cyclotella comta, and Rhodamonas lens. Dur-ing the summer, Cyclotella comta, Cyclotella cf. delicatula, Cryptomonasreflexa, Gymnodinium helveticum, and Tabellaria flocculosa werethe most abundant taxa in the epilimnion, while Cyclotella comta,Gymnodinium helveticum, Cryptomonas reflexa, Oscillatoria limnetica,and Asterionella Formosa were the most abundant taxa in the DCL.Significant dissimilarities existed among SprINT, SumEPI, and SumDCLsample groups in Lake Superior (ANOSIM Global R = 0.447, p =0.001). Pairwise comparisons (SprINT–SumEPI, SprINT–SumDCL,SumEPI–SumDCL) also exhibited significant dissimilarities (0.238 ≤R ≤ 0.684, p=0.001). NMDS ordination illustrated complete separationbetween spring and summer integrated epilimnetic samples, while thesummer DCL samples exhibited some overlap with both epilimneticsample groups (Fig. 6).
Please cite this article as: Bramburger, A.J., Reavie, E.D., A comparison of phof the Laurentian Great Lakes, J. Great Lakes Res. (2016), http://dx.doi.org
SIMPER analysis demonstrated that SumDCL samples were slightlymore similar to SprINT (mean dissimilarity = 54.55) than to SumEPI(mean dissimilarity = 50.31) samples, while SumEPI samples weremost dissimilar to SprINT samples (mean dissimilarity = 64.80).Dissimilarities among SumEPI and SprINT samples, were accounted forprimarily by increased abundances of Aphanocapsa spp. (26.18%),Cyclotella comensis “rough center with process” (also known asCyclotella cf. delicatula, Reavie and Kireta, 2015) (8.59%), Discostellapseudostelligera (6.19%), and Cyclotella ocellata (5.08%), and by lowerabundances of Synedra filiformis var. exilis (4.12%) in the summer sam-ples. Similarly, increased abundances of Aphanocapsa spp. (21.59%),C. ocellata (6.36%), C. cf. delicatula (3.17%), and C. comensis (4.75%)during the summer months accounted for a large proportion of thedissimilarity between SprINT and SumDCL samples. Dissimilaritiesbetween SumEPI and SumDCL samples were accounted for largely byhigher abundances of Aphanocapsa spp. (27.58%), C. cf. delicatula(6.06%), and C. ocellata (5.79%), as well as by lower abundances ofS. filiformis and S. filiformis var. exilis in the epilimnetic samples.
Lake Michigan
In Lake Michigan, the most abundant taxa in spring integratedsamples were Stephanodiscus parvus, Gymnodinium helveticum,Stephanodiscus alpinus, Stephanodiscus hantzschii, and Cryptomonasreflexa. During the summer, Ceratium hirudinella, Fragilaria crotonensis,Anabaena flos-aquae, Cryptomonas reflexa, and Diatoma tenue var.elongatum were the most abundant taxa in the epilimnion, whileDiatoma tenue var. elongatum, Fragilaria crotonensis, Cryptomonas reflexa,Oscillatoria limnetica, and Ceratium hirundinellawere the most abundanttaxa in theDCL. Significant dissimilarities existed among SprINT, SumEPI,and SumDCL assemblages (Global R=0.557, p=0.001), as well as in allpairwise comparisons (0.258 ≤ R ≤ 0.796, p = 0.001). Similar to Lake
ytoplankton communities of the deep chlorophyll layers and epilimnia/10.1016/j.jglr.2016.07.004
Fig. 3. Mean taxonomic richness, density, and biovolume differences among springintegrated (SprINT), summer DCL (SumDCL), and summer epilimnetic samples(SumEPI) representing phytoplankton communities from the Great Lakes, 2007–2012.Error bars represent the 95% confidence interval of the mean. Bars not connected by thesame letter are significantly different (p b 0.05).
Fig. 4. z-normalized mean individual biovolume (cell size) differences among springintegrated (SprINT), summer DCL (SumDCL), and summer epilimnetic samples(SumEPI) for dominant algal groups in the Great Lakes. Error bars represent 95%confidence interval of the mean. Bars not connected by the same letter are significantlydifferent (p b 0.05).
6 A.J. Bramburger, E.D. Reavie / Journal of Great Lakes Research xxx (2016) xxx–xxx
Superior patterns, NMDS ordination showed that SprINT samples weredistinct from SumEPI samples. Here, however, SumDCL samples clus-tered more closely to SumEPI samples and were also largely separatedfrom SprINT samples (Fig. 6), indicating a stronger seasonal separationin assemblages than that observed in Lake Superior. SIMPER results forLake Michigan reflected the ordination patterns. SprINT samples weremost dissimilar to SumEPI samples (meandissimilarity=81.26), follow-ed by SumDCL samples (mean dissimilarity = 73.37). SumDCL sampleswere most similar to SumEPI samples (mean dissimilarity = 39.11).The dissimilarity between SprINT and SumEPI samples was due mainlyto higher abundances of Aphanocapsa spp. (14.96%) and Fragilariacrotonensis (8.31%), and lower abundances of Stephanodiscus sp. #51(also described as an unknown species of S. parvus by Reavie andKireta (2015); 11.31%) and S. parvus (8.316%) in the summer samples.High abundances of S. sp. #51 (12.16%) and S. parvus (9.72%), coupledwith relatively low abundances of S. filiformis (6.80%) and Aphanocapsaspp. (6.68%) in SprINT samples compared to SumDCL samples accountedfor a large proportion of the dissimilarity between these sample groups.The dissimilarity between Lake Michigan SumEPI and SumDCLsamples was driven primarily by high abundances of Aphanocapsa spp.(16.11%), F. crotonensis (6.84%), and Oscillatoria minima (5.56%), and
Please cite this article as: Bramburger, A.J., Reavie, E.D., A comparison of phof the Laurentian Great Lakes, J. Great Lakes Res. (2016), http://dx.doi.org
low abundances of S. filiformis (7.54%) in the epilimnetic samples,relative to SumDCL samples.
Lake Huron
In Lake Huron, the most abundant taxa in spring integratedsamples were Rhodamonas lens, Gymnodinium helveticum, Cryptomonasreflexa, Aulacoseira islandica, and Fragilaria crotonensis. During the sum-mer, Fragilaria crotonensis, Cyclotella cf. delicatula, Chrysosphaerellalongispina, Synedra filliformis, and Cyclotella comtawere the most abun-dant taxa in the epilimnion, while Fragilaria crotonensis, Cyclotellacomta, Asterionella formosa, Cyclotella cf. delicatula, and Cryptomonasreflexa were the most dominant taxa in the DCL. As with the otherupper lakes, Lake Huron exhibited significant dissimilarities amongSprINT, SumEPI, and SumDCL samples (Global R = 0.691, p = 0.001).Significant dissimilarities were also observed in all pairwise compari-sons (0.480 ≤ R ≤ 0.874, p=0.001) andNMDS ordination indicated littleoverlap among groups (Fig. 6). SIMPER analysis indicated thewidest di-vergence between SprINT and SumEPI samples (mean dissimilarity =74.84), which was driven largely by high abundances of Aphanocapsaspp. (23.02%) and C. comensis var. 1 (12.19%) in summer samples andS. filiformis (12.34%), A. formosa (8.61%), and N.acicularis (7.06%) inspring samples. The SumDCL sample groupwas roughly equally dissim-ilar to both the SprINT (mean dissimilarity= 64.09) and SumEPI (meandissimilarity = 60.92) samples. High abundances of Aphanocapsa spp.and C. comensis in SumDCL samples and S. filiformis, A. formosa, andNitzschia acicularis in SumEPI samples contributed strongly to thedissimilarity between these sample groups (13.66%, 10.27%, 10.17%,5.77%, 6.06%, respectively). Among summer samples (SumEPI andSumDCL), strong partitioning of C. comensis var. 1 (12.44%) andS. filiformis (8.00%) to the epilimnetic samples, as well as high abun-dances of Aphanocapsa spp. (22.91%) and C. comensis (12.64%) inSumDCL samples, accounted for most of the overall dissimilarity.
Lake Erie
In Lake Erie, Aulacoseira islandica, Stephanodiscus alpinus, Surirellaovata, Stephanodiscus binderanus, and Stephanodiscus parvus were themost abundant taxa in spring samples. In the summer, Microcystisaeruginosa, Aulacoseira granulata, Fragilaria crotonensis, Ceratiumhirudinella, and Aphanizomenon flos-aquae were the dominant taxa inthe epilimnion, while Fragilaria crotonensis, Aphanizomenon flos-aquae,
ytoplankton communities of the deep chlorophyll layers and epilimnia/10.1016/j.jglr.2016.07.004
Fig. 5.Mean relative biomass contributions of various phytoplankton types to spring integrated epilimnetic (INT), summer epilimnetic, and summer DCL samples. BAC= centric diatoms,BAP = pennate diatoms, CHL = chlorophytes, CHR = chrysophytes, CRY = cryptophytes, CYA = cyanophytes, EUG = euglenoids, PYR = pyrrhophytes, UNI = unidentified algae.
7A.J. Bramburger, E.D. Reavie / Journal of Great Lakes Research xxx (2016) xxx–xxx
Ceratium hirudinella, Cryptmonas reflexa, and Cryptomonas erosa werethe most abundant taxa in the DCL. Due to its shallower depth andstrong vertical mixing, Lake Erie does not always develop a DCL. WhileANOSIM indicated significant dissimilarities in the overall Erie sampleset (Global R = 0.852, p = 0.001), and SprINT algal assemblages weresignificantly dissimilar to those of SumEPI and SumDCL samples (R =0.916, p=0.001; R=0.866, p=0.001, respectively), SumDCL samples,when collected, were also significantly dissimilar to SumEPI samples(R=0.271, p=0.019). Ordination of these samples usingNMDS clearlyillustrated the distinction between spring and summer algal assem-blages, and to a lesser extent, SumEPI and SumDCL assemblages withinthe lake (Fig. 6). Dissimilarity between spring integrated and summerepilimnetic assemblages in Lake Erie (SprINT and SumEPI) were strong-ly influenced by high abundances of A. islandica (18.78%) and S. parvus(8.98%) in spring samples and high abundances of Aphanocapsa spp.(24.79%), Aphanothece spp. (4.45%), F. crotonensis (4.37%), and severalspecies of Cyclotella in summer samples (11.99%, collectively). Thesame suite of species contributed consistently to dissimilarities betweenSprINT and SumDCL samples. When a DCL did form, dissimilaritiesbetween epilimnetic and DCL samples were driven largely by highabundances of Aphanocapsa spp. (22.44%) and Microcystis aeruginosa(5.46%) in epilimnetic samples and F. crotonensis (14.84%), C. comensisvar. 1 (6.68%), and D. pseudostelligera (6.58%) in the DCL samples.Diatom abundances were typically higher in DCL assemblages.
Lake Ontario
In Lake Ontario, Stephanodiscus parvus, Gymnodinium helvaticum,Stephanodiscus alpinus, Stephanodiscus hantzschii, and Cryptomonasreflexa were the most abundant taxa in spring assemblages. Duringthe summer, Ceratium hirundinella, Fragilaria crotonensis, Anabaenaflos-aquae, Cryptomonas reflexa, and Diatoma tenue var. elongatumwere the most abundant taxa in the epilimnion, while Diatoma tenuevar. elongatum, Fragilaria crotonensis, Cryptomonas reflexa, Oscillatorialimnetica, and Ceratium hirundinella were the most abundant taxa inthe DCL. Algal assemblages in Lake Ontario samples were less dissimilarto one another than those in other lakes (ANOSIM Global R = 0.307,p = 0.001). Pairwise comparisons demonstrated significant dissimilar-ities among spring integrated, summer epilimnetic, and summer DCL
Please cite this article as: Bramburger, A.J., Reavie, E.D., A comparison of phof the Laurentian Great Lakes, J. Great Lakes Res. (2016), http://dx.doi.org
samples (0.047 ≤ R ≤ 0.459, 0.001 ≤ p ≤ 0.019). NMDS ordinationshowed that most SprINT samples were well separated from summersamples and that some close association existed between SumEPI andSumDCL sample sets (Fig. 6). SIMPER analysis indicated the greatest dis-similarity between SprINT and SumEPI samples (mean dissimilarity =88.02), which was accounted for by high abundances of S. parvus(18.59%) and Cyclotella atomus “fine form” [also described as C. atomusvar. 1 (Reavie and Kireta, 2015) 7.13%] in the SprINT samples andF. crotonensis (18.63%), C. comensis var. 1 (9.92%), and Synedra ostenfeldii(8.00%) in the SumEPI samples. Dissimilarities between SprINT andSumDCL samples were accounted for by elevated abundances ofF. crotonensis and Diatoma tenue in SumDCL samples (19.64%, 10.13%,respectively), as well as by higher abundances of Stephanodiscus parvusand C. atomus var. 1 in SprINT samples (18.54%, 7.27%, respectively).
Discussion
Deep chlorophyll layers are known to form in all of the Great Lakes(Putnam and Olson, 1966; Watson et al., 1975). With the exception ofLake Erie, we observed the formation of DCLs regularly in all lakesduring periods of summer stratification. Patterns of phytoplanktoncommunity structure were surprisingly consistent and revealed inter-esting vertical distribution characteristics, especially with respect todiatoms and cyanophytes. While spring integrated and summerepilimnetic assemblages were compositionally distinct, summer DCLassemblages were often more similar to spring assemblages than tosummer epilimnetic samples. This finding suggests that DCL assem-blages are composed, at least partially, of remnants of the algal commu-nity that was present during isothermal conditions in the spring. Springphytoplankton communities in the Great Lakes were frequently domi-nated by diatom taxa, primarily from the genera Aulacoseira andStephanodiscus. In general, cyanophyte taxa exhibited slightly higherabundances in summer epilimnetic samples, compared with springepilimnetic samples, and summer DCL samples. The shift to dominanceby cyanophytes during the stratified period is well understood in lenticsystems (e.g., Sommer, 1985). High relative abundances of cyanophytesin the summer epilimnion, compared to the DCL, suggest that the inher-ent buoyancy of cyanophytes allows them to maintain their position inthe euphotic zone better than other taxa (Reynolds et al., 1987;Walsby
ytoplankton communities of the deep chlorophyll layers and epilimnia/10.1016/j.jglr.2016.07.004
Fig. 6. NMDS ordinations of phytoplankton assemblages in the five Great Lakes. Symbols represent sample scores (SprINT= spring integrated epilimnetic; SumEPI= summer integratedepilimnetic; SumDCL= summer DCL). Vectors illustrate the relative direction and magnitude of species' contribution to dissimilarities among samples. Species shownwere correlated toamong-group differences with a Pearson correlation coefficient ≥ 0.5. Bray–Curtis dissimilarity was used as the distance metric, and distances were calculated based on speciesrelative abundances.
8 A.J. Bramburger, E.D. Reavie / Journal of Great Lakes Research xxx (2016) xxx–xxx
et al., 1997). Advantages conferred by enhanced buoyancy bear impor-tant implications for the formation of cyanophyte blooms under thepredictions of climate change models (Reynolds et al., 1987; Wagnerand Adrian, 2009). While these colonial cyanobacteria and other auto-trophic picoplankton represented only a small portion of the overallphytoplankton biovolume of the lakes, their importance to the ecologi-cal function of the photosynthetically active epilimnion is an avenue
Please cite this article as: Bramburger, A.J., Reavie, E.D., A comparison of phof the Laurentian Great Lakes, J. Great Lakes Res. (2016), http://dx.doi.org
worthy of investigation in light of ongoing oligtrophication and intensi-fied stratification within several Laurentian Great Lakes basins.
The effects of incipient climate change have also resulted in commu-nity reorganization at finer levels of taxonomic organization. Severalauthors have proposed that Cyclotella abundances in lakes haveincreased globally as an indirect result of elevated atmospheric temper-atures (e.g. Chraïbi et al., 2014; Rühland et al., 2008), although the
ytoplankton communities of the deep chlorophyll layers and epilimnia/10.1016/j.jglr.2016.07.004
9A.J. Bramburger, E.D. Reavie / Journal of Great Lakes Research xxx (2016) xxx–xxx
mechanism responsible for Cyclotella increases in warmer waters hasnot been determined. In this study, summer epilimnetic assemblageswere characterized by higher abundances of taxa within Cyclotellasensu lato, particularly C. comensis and C. comensis var. 1, than theirspringtime and summer DCL counterparts.
NMDS illustrated the taxonomic composition of the DCL assem-blages as intermediate communities composed of elements of boththe spring and summer epilimnetic communities (Fig. 5). It is apparentthat settling from the epilimnion is an important source of propagulesto the DCL. In certain lakes, there are variations in water quality(e.g., nutrients) that might drive differences in phytoplankton betweenepilimnia and DCLs, but the consistency across lakes in the relationshipbetween spring and summer DCL assemblages indicates that the chem-ical variables we present were less important determinants of theunique DCL community. Further, spring epilimnetic assemblages aremore similar to DCL assemblages than they are to summer epilimneticassemblages, suggesting that passive settling affects taxa differently;rather, sinking throughout the late spring and summer as stratificationsets up is at least partly responsible for the DCL phytoplankton assem-blage. Fahnenstiel and Scavia (1987) noted that DCL phytoplankton as-semblages in Lake Michigan were similar to spring assemblages butsuggested that in situ production was also important to maintenanceof these assemblages. We suggest that the DCL community is a relict in-tegration of propagules from both spring and summer epilimnetic as-semblages, while the summer epilimnetic community represents adistinct assemblage. Unfortunately, temporal sampling resolution istoo low to address vertical community structuring in the spring watercolumn. As such, we are currently unable to confirm whether compo-nents of the summer DCL are descendants of sunken propagules fromspring (i.e., active DCL maintenance) or simply remnants of the springphytoplankton community (i.e., passive DCL formation). Further, dueto the constraints of the USEPA sampling regime, we are also unableto assess rates of photosynthesis and primary production within theDCL and epilimnion, and are unable to comment on the relativecontributions of these strata to total water column production.
The infrequency of summer DCL formation in Lake Erie despitestrong thermal stratification is not surprising, considering the relativeshallowness of the lake and the high epilimnetic turbidity and suscepti-bility to meteorological drivers (Lick et al., 1994). When DCLs are ob-served within Lake Erie, they occur predominantly within the centralbasin and occur at shallower mean and maximum depths than in theother lakes (although mean DCL depths are similar to Lake Ontario).Differences between spring and summer algal assemblages in LakeErie were driven primarily by high spring abundances of Aulacoseiraislandica, which is known to grow under the ice in Lake Erie (Saxtonet al., 2012; Twiss et al., 2012b), and large blooms of this taxon occurregularly in the spring within Lake Erie (Reavie et al., 2014b).After the onset of stratification in the summer months, Lake Erie'sepilimnetic phytoplankton community becomes increasingly dominat-ed by cyanophytes, including the potentially harmful Microcystis.When a DCL does form in Lake Erie, the DCL phytoplankton communityis composed primarily of pennate and centric diatoms, despite overlyingepilimnetic assemblages being dominated by cyanophytes, suggestingthat low diatom biovolume in the summer epilimnion in Lake Erie isdue in part to losses via sinking. Higher cyanophyte abundances withinthe summer epilimnion are likely supported in part by the inherentbuoyancy of many cyanophyte taxa (per Dokulil and Teubner, 2000;Wynne et al., 2013).
In all of the lakes, summer epilimnetic and DCL phytoplankton com-munities were significantly dissimilar to one another, suggesting thatthe summer epilimnetic community is distinct. With the exception ofLake Erie, whose summer epilimnetic community is characterized byhigh abundances of cyanophytes, vertical dissimilarity is driven largelyby differences in diatom assemblages between the epilimnion andthe DCL. Large, Fragilaria-like pennate diatoms including Fragilariacrotonensis, Synedra radians, and Synedra ostenfeldii are typically more
Please cite this article as: Bramburger, A.J., Reavie, E.D., A comparison of phof the Laurentian Great Lakes, J. Great Lakes Res. (2016), http://dx.doi.org
abundant in the DCL than in the epilimnion. These findings areconsistent with results from Lake Michigan during the early 1980s(Fahnenstiel and Scavia, 1987), where the upper portions of the DCLwere also dominated by Fragilaria crotonensis and other similar pennatetaxa. Across the entire basin, centric diatom communities shift frombeing dominated by Stephanodiscus species in the spring to Cyclotellasensu lato species, particularly C. comensis and its varieties, in the sum-mer. Interestingly, Cyclotella sensu lato exhibits differential vertical dis-tributions in the summer water column. Typically, taxa with smallercell sizes including C. comensis var. #1 and C. pseudostelligera are morestrongly represented in the epilimnion than in the DCL. Conversely,larger-celled Cyclotella taxa such as C. comensis, C. ocellata, and Cyclotellatripartita are more abundant in the DCL. These results are in contrast todata presented by Barbiero and Tuchman (2001), who suggested thatC. comensis and C. comta were more abundant in the epilimnion thanin the DCL in Lakes Superior and Huron during the 1998 stratified sea-son. Cyclotella taxa that exhibit a broad range of individual biovolumesare distributed approximately evenly between the epilimnion andDCL, although larger individuals of these taxa tend to be favored withinthe DCL and vice versa, suggesting that inter-species variability in watercolumn position is likely driven by differential sinking rates.
The distribution of different-sized conspecific individuals across adepth gradient is not limited to Cyclotella. In general, siliceous algae(diatoms and chrysophytes) exhibited higher mean cell sizes in theDCL than in the epilimnion, suggesting that larger, heavier individualswere more prone to sinking out of the epilimnion. In contrast,cyanophyteswere typically larger in the epilimnion than in theDCL, im-plying a buoyancy effect among larger individuals. The lack of signifi-cant vertical distribution patterns among other groups is likely due tothe confounding influences of individual motility (cryptophytes and di-noflagellates) and variable colony shape and size (chlorophytes). Theopposite patterns of vertical distribution displayed by heavy, siliceoustaxa and largely unicellular, buoyant small taxa suggest that patternsof vertical community structure are regulated at least in part by differ-ential sinking rates. This implies that summer stratification intensity im-parts an important structuring influence on algal communities withinthe Great Lakes and promotes the existence of an epilimnion-specificphytoplankton assemblage.
In summary, summer epilimnia and DCLs within the LaurentianGreat Lakes support distinct phytoplankton communities. While sum-mer epilimnetic assemblages are characterized by taxa typically foundin warm, stratified waters, DCL assemblages contain a mixture of indi-viduals representing both spring and summer epilimnetic components.In fact, DCL assemblages are often more similar to spring communitiesthan to their summer epilimnetic counterparts, suggesting that passivesinking from the spring community plays an important role in DCL de-velopment. Further, within-species size differences between DCL andsummer epilimnetic assemblages illustrate the importance of buoyancyand loss due to sinking in the development of vertically structured com-munities in stratified water columns. The development of a distinctepilimnetic and DCL algal communities during summer stratificationin the Great Lakes provides modern context for paleolinmological indi-cators thought to represent periods of stratification consistent withclimate-driven water column warming.
Acknowledgments
This project was financially supported through the US Environmen-tal Protection Agency Great Lakes National Program Office (GLNPO)Surveillance and Monitoring program, under Cooperative AgreementGL-00E23101-2. This document has not been subjected to the EPA's re-quired peer and policy review and therefore does not necessarily reflectthe view of the agency, and no official endorsement should be inferred.Michael Agbeti supported algal assessments of the phytoplanktonsamples The authors would like to acknowledge field and laboratorypersonnel Kitty Kennedy and Lisa Estepp and the crew of the R/V Lake
ytoplankton communities of the deep chlorophyll layers and epilimnia/10.1016/j.jglr.2016.07.004
10 A.J. Bramburger, E.D. Reavie / Journal of Great Lakes Research xxx (2016) xxx–xxx
Guardian. We also thank MacKenzie Waller for GIS and mapping assis-tance. This is contribution number [issued on acceptance] of the Centerfor Water and the Environment, Natural Resources Research Institute,University of Minnesota Duluth.
References
Barbiero, R.P., Tuchman, M.L., 2001. Results from the US EPA's biological open water sur-veillance program of the Laurentian Great Lakes: II. Deep chlorophyll maxima. J. GreatLakes Res. 27, 155–166.
Barbiero, R.P., Tuchman, M.L., 2004. The deep chlorophyll maximum in Lake Superior.J. Great Lakes Res. 30, 256–268.
Brooks, A.S., Torke, B.G., 1977. Vertical and seasonal distribution of chlorophyll a in LakeMichigan. J. Fish. Res. Board Can. 34, 2280–2287.
Camacho, A., 2006. On the occurrence and ecological features of deep chlorophyll maxima(DCM) in Spanish stratified lakes. Limnetica 25, 453–478.
Campbell, R.G., Sherr, E.B., Ashjian, C.J., Plourde, S., Sherr, B.F., Hill, V., Stockwell, D.A.,2009. Mesozooplankton prey preference and grazing impact in the western ArcticOcean. Deep-Sea Res. II Top. Stud. Oceanogr. 56, 1274–1289.
Chraïbi, V.L.S., Kireta, A.R., Reavie, E.D., Cai, M., Brown, T.N., 2014. A paleolimnologicalassessment of human impacts on Lake Superior. J. Great Lakes Res. 40, 886–897.
Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in communitystructure. Aust. J. Ecol. 138, 143–157.
Craig, S.R., 1987. The distribution and contribution of picoplankton to deep photosynthet-ic layers in some meromictic lakes. Acta Acad. Aboensis. 47, 55–81.
Cullen, J.J., 1982. The deep chlorophyll maximum: comparing vertical profiles ofchlorophyll a. Can. J. Fish. Aquat. Sci. 39, 791–803.
Cullen, J.J., Eppley, R.W., 1981. Chlorophyll maximum layers of the Southern-CaliforniaBight and possible mechanisms of their formation and maintenance. Oceanol. Acta4, 23–32.
Dokulil, M.T., Teubner, K., 2000. Cyanobacterial dominance in lakes. Hydrobiologia 438,1–12.
Fahnenstiel, G.L., Carrick, H.J., 1992. Phototrophic picoplankton in Lakes Huron andMichigan: abundance, distribution, composition, and contribution to biomass andproduction. Can. J. Fish. Aquat. Sci. 49, 379–388.
Fahnenstiel, G.L., Scavia, D., 1987. Dynamics of Lake Michigan phytoplankton: the deepchlorophyll layer. J. Great Lakes Res. 13, 285–295.
Fahnenstiel, G.L., Scavia, D., Schelske, C.L., 1984. Nutrient-light interactions in the LakeMichigan subsurface chlorophyll layer. Verh. Internat. Verein. Limnol. 22, 499–508.
Fahnenstiel, G.L., Chandler, J.F., Carrick, H.J., Scavia, D., 1989. Photosynthetic characteris-tics of phytoplankton communities in Lakes Huron and Michigan: PI parametersand end-products. J. Great Lakes Res. 15, 394–407.
Falkowski, P.G., Kolber, Z., 1995. Variations in chlorophyll fluorescence yields in phyto-plankton in the world oceans. Funct. Plant Biol. 22, 341–355.
Fasham,M.J.R., Platt, T., Irwin, B., Jones, K., 1985. Factors affecting the spatial pattern of thedeep chlorophyll maximum in the region of the Azores front. Prog. Oceanogr. 14,129–165.
Fee, E.J., 1976. The vertical and seasonal distribution of chlorophyll in lakes of theExperimental Lakes Area, northwestern Ontario: Implications for primary productionestimates. Limnol. Oceanogr. 21, 767–783.
Gasol, J.M., Guerrero, R., Pedrós-Alió, C., 1992. Spatial and temporal dynamics of ametalimnetic Cryptomonas peak. J. Plankton Res. 14, 1565–1579.
Gervais, F., Siedel, U., Heilmann, B., Weithoff, G., Heisig-Gunkel, G., Nicklisch, A., 2003.Small-scale vertical distribution of phytoplankton, nutrients and sulphide below theoxycline of a mesotrophic lake. J. Plankton Res. 25, 273–278.
Jochem, F.J., Zeitzschel, B., 1993. Productivity regime and phytoplankton size structure inthe tropical and subtropical North Atlantic in spring 1989. Deep-Sea Res. II Top. Stud.Oceanogr. 40, 495–519.
Kasprzak, P., Gervais, F., Adrian, R., Weiler, W., Radke, R., Jäger, I., Riest, S., Siedel, U.,Schneider, B., Böhme, M., Eckmann, R., 2000. Trophic characterization, pelagic foodweb structure and comparison of two mesotrophic lakes in Brandenburg(Germany).Int. Rev. Hydrobiol. 85, 167–189.
Kiefer, D.A., Kremer, J.N., 1981. Origins of vertical patterns of phytoplankton and nutrientsin the temperate, open ocean: a stratigraphic hypothesis. Deep Sea Res. Part A 28,1087–1105.
Leavitt, P.R., Fritz, S.C., Anderson, N.J., Baker, P.A., Blenckner, T., Bunting, L., Catalan, J.,Conley, D.J., Hobbs, W.O., Jeppesen, E., Korhola, A., 2009. Paleolimnological evidenceof the effects on lakes of energy and mass transfer from climate and humans. Limnol.Oceanogr. 54, 2330–2348.
Lick, W., Lick, J., Ziegler, C.K., 1994. The resuspension and transport of fine-grainedsediments in Lake Erie. J. Great Lakes Res. 20, 599–612.
Moll, R.A., Stoermer, E.F., 1982. Hypothesis relating trophic status and subsurfacechlorophyll maxima of lakes. Arch. Hydrobiol. Suppl. 94, 426–440.
Moll, R.A., Brache, M.Z., Peterson, T.P., 1984. Phytoplankton dynamics within thesubsurface chlorophyll maximum of Lake Michigan. J. Plankton Res. 6, 751–766.
Naselli-Flores, L., Barone, R., 2003. Steady-state assemblages in aMediterranean hypertro-phic reservoir. The role of Microcystis ecomorphological variability in maintaining anapparent equilibrium. Hydrobiologia 502, 133–143.
Please cite this article as: Bramburger, A.J., Reavie, E.D., A comparison of phof the Laurentian Great Lakes, J. Great Lakes Res. (2016), http://dx.doi.org
Pick, F.R., Nalewajko, C., Lean, D.R.S., 1984. The origin of a metalimnetic chrysophyte peak.Limnol. Oceanogr. 29, 125–134.
Pilati, A., Wurtsbaugh, W.A., 2003. Importance of zooplankton for the persistence ofa deep chlorophyll layer: a limnocorral experiment. Limnol. Oceanogr. 48,249–260.
Planas, M.D., 1973. Composición, ciclo y productividad del fitoplancton del Lago deBanyoles. Oecol. Aquat. 1, 3–106.
Planas, M.D., 1990. Factores de control de la distribución espacial y temporal de laproducción primaria del fitoplancton del Lago de Banyoles. Sci. Gerundensis 16,193–204.
Putnam, H.D., Olson, T.A., 1966. Primary productivity at a fixed station in western LakeSuperior. In Proc. 9th Conf. Great Lakes Res, pp. 119–128.
Reavie, E.D., Kireta, A.R., 2015. Centric, Araphid and Eunotioid Diatoms of the CoastalLaurentian Great Lakes. Gebr. Borntraeger Verlagsbuchandlung, Stuttgart.
Reavie, E.D., Jicha, T.M., Angradi, T.R., Bolgrien, D.W., Hill, B.H., 2010. Algal assemblagesfor large river monitoring: comparison among biovolume, absolute and relativeabundance metrics. Ecol. Indic. 10, 167–177.
Reavie, E.D., Heathcote, A.J., Chraïbi, V.L.S., 2014a. Laurentian Great Lakes phytoplanktonand their water quality characteristics, including a diatom-based model forpaleoreconstruction of phosphorus. PLoS One 9, e104705.
Reavie, E.D., Barbiero, R.P., Allinger, L.E., Warren, G.J., 2014b. Phytoplankton trends in theGreat Lakes, 2001–2011. J. Great Lakes Res. 40, 618–639.
Reynolds, C.S., Oliver, R.L., Walsby, A.E., 1987. Cyanobacterial dominance: the role ofbuoyancy regulation in dynamic lake environments. N. Z. J. Mar. Freshw. Res. 21,379–390.
Rühland, K.M., Paterson, A.M., Smol, J.P., 2008. Lake diatom responses to warming:reviewing the evidence. J. Paleolimnol. 54, 1–35.
Saros, J.E., Interlandi, S.J., Doyle, S., Michel, T.J., Williamson, C.E., 2005. Are the deepchlorophyll maxima in alpine lakes primarily inducedby nutrient availability, notUV avoidance? Arct. Antarct. Alp. Res. 37, 557–563.
Saxton, M.A., Arnold, R.J., Bourbonniere, R.A., McKay, R.M.L., Wilhelm, S.W., 2012.Plasticity of total and intracellular phosphorus quotas in Microcystis aeruginosacultures and Lake Erie algal assemblages. Front. Microbiol. 3, 1–9.
Scavia, D., Fahnenstiel, G.L., 1987. Dynamics of Lake Michigan phytoplankton: mecha-nisms controlling epilimnetic communities. J. Great Lakes Res. 13, 103–120.
Shulenberger, E., Reid, J.L., 1981. The Pacific shallow oxygen maximum, deep chlorophyllmaximum, and primary productivity, reconsidered. Deep Sea Res. Part A 28, 901–919.
Sommer, U., 1985. Seasonal succession of phytoplankton in Lake Constance. Bioscience 35(6), 351–357.
Twiss, M.R., Ulrich, C., Zastepa, A., Pick, F.R., 2012a. On phytoplankton growth and lossrates in the epilimnion and metalimnion of Lake Ontario in mid-summer. J. GreatLakes Res. 38, 146–153.
Twiss, M.R., McKay, R.M.L., Bourbonniere, R.A., Bullerjahn, G.S., Carrick, H.J., Smith, R.E.H.,Wilhelm, S.W., 2012b. Diatoms abound in ice-covered Lake Erie: an investigation ofoffshore winter limnology in Lake Erie over the period 2007 to 2010. J. Great LakesRes. 38, 18–30.
USEPA, 2010. Sampling and analytical procedures for GLNPO's open lake water qualitysurvey of the Great Lakes. United States Environmental Protection Agency, GreatLakes National Program Office. Chicago, Illinois. EPA 905-R-05-001. http://www.epa.gov/glnpo/monitoring/sop/ (Accessed 15 February 2016).
Utermöhl, H., 1958. Zur vervollkommnung der quantitativen phytoplankton-methodik.Mitt. Int. Ver. Theor. Angew. Limnol. 9, 1–38.
Veldhuis, M.J., Kraay, G.W., Van Bleijswijk, J.D., Baars, M.A., 1997. Seasonal and spatial var-iability in phytoplankton biomass, productivity and growth in the northwesternIndian Ocean: the southwest and northeast monsoon, 1992–1993. Deep-Sea Res. I44, 425–449.
Venrick, E.L., 1982. Phytoplankton in an oligotrophic ocean: observations and questions.Ecol. Monogr. 52, 129–154.
Wagner, C., Adrian, R., 2009. Cyanobacteria dominance: quantifying the effects of climatechange. Limnol. Oceanogr. 54, 2460–2468.
Walsby, A.E., Hayes, P.K., Boje, R., Stal, L.J., 1997. The selective advantage of buoyancy pro-vided by gas vesicles for planktonic cyanobacteria in the Baltic Sea. New Phytol. 136,407–417.
Watib, N.H.F., Thomson, K.P.B., Elder, F.C., 1975. Sub thermocline biomass concentrationdetected by transmissometer in Lake Superior. Verh. Internat. Verein. Limnol. 19,682–688.
Watson, N.H.F., Nicholson, H.F., Culp, L.R., 1975. Chlorophyll a and primary production inLake Superior, May to November 1973. Fish. and Marine Service, Techn. Rep. 525.Great Lakes Biolimnology Laboratory, Canada Center for Inland Waters.
White, B., Matsumoto, K., 2012. Causal mechanisms of the deep chlorophyll maxi-mum in Lake Superior: a numerical modeling investigation. J. Great Lakes Res.38, 504–513.
Wolin, J.A., Stoermer, E.F., 2005. Response of a LakeMichigan coastal lake to anthropogen-ic catchment disturbance. J. Paleolimnol. 33, 73–94.
Work, K.A., Havens, K.E., 2003. Zooplankton grazing on bacteria and cyanobacteria in aeutrophic lake. J. Plankton Res. 25, 1301–1306.
Wynne, T.T., Stumpf, R.P., Tomlinson, M.C., Fahnenstiel, G.L., Dyble, J., Schwab, D.J., Joshi,S.J., 2013. Evolution of a cyanobacterial bloom forecast system in western Lake Erie:development and initial evaluation. J. Great Lakes Res. 39, 90–99.
Yilmaz, A., Ediger, D., Basturk, O., Tugrul, S., 1994. Phytoplankton fluorescence anddeep chlorophyll maxima in the Northeastern Mediterranean. Oceanol. Acta 17,69–77.
ytoplankton communities of the deep chlorophyll layers and epilimnia/10.1016/j.jglr.2016.07.004
