Factors Affecting the Contribution by Epiphytic Algae to thePrimary Productivity of an Oligotrophic Freshwater Lake'
RICHARD B. SHELDON AND CHARLES W. BOYLEN*Department of Chemical and Environmental Engineering, and Freshwater Institute and Department of
Biology, * Rensselaer Polytechnic Institute, Troy, New York 12181
Received for publication 12 May 1975
A diatom-dominated population of epiphytic algae was studied in an oligo-trophic lake to determine the factors which limit epiphyte growth and tomeasure their contribution to primary productivity. Algae were collected fromplants growing at four sites in Lake George, N.Y., during the spring, summer,and fall of 1974. Samples were taken from 3 m, corresponding to the depth atwhich macrophytes were most productive. Algae exhibited an optimum tempera-ture for H'4CO3- uptake at 30 C, although the summer littoral lake temperatureranged from 18 to 25 C. Light saturation occurred at an intensity of 8,608 lux,approximating the environmental intensity at the depth from which algae weretaken. Epiphytes exhibited their maximum photosynthetic capacity of 0.6 mg ofcarbon fixed/m2 of macrophyte surface area per h in the early afternoon in mid-August. They assimilated approximately 5% as much inorganic carbon as themacrophytes from which they were taken. Epiphyte population densities fol-lowed the seasonal growth patterns of the macrophytes, with maximal leafcolonization remaining essentially constant relative to the leaf position on theplant. There was little change in density between sampling sites at any giventime. Productivities of epiphytes from bottom leaves were 10-fold greater thanthose of epiphytes from top leaves. Addition of P04-3, NO3-, NH3, Si, and SO4-2had no stimulatory effect on photosynthesis. Addition of HCO3- stimulatedphotosynthesis greater than 30%, suggesting that carbon may be a limitingnutrient for epiphytic algae in Lake George.
Investigations attempting to understand thecomplex ecological interrelationships existingin aquatic environments have frequently over-looked the role ofthe epiphytic community. Theexact meaning of the term "epiphyte" is itself asubject of disagreement, as is illustrated byexamination of the literature. Ruttner (23) de-fines them as unrooted plants which use otherplants as a substrate without penetrating intothem and without withdrawing nutrient sub-stances from them. A subdivision of the Ger-man concept of the entire sessile benthic com-munity known as "Aufwuchs" or of the moreAmericanized term "periphyton," the term isused to identify the organisms growing uponthe free surfaces of submerged objects in water.Other investigations base their terminology onthe presence or absence of associations betweenthe individual sessile organisms on the fixedsubstrata. Wetzel (28) suggests the usage of theterm "periphyton" modified by an appropriateadjective such as epipelic (on the surface ofsediments), epilithic (on the surface of rocks),
' Contribution no. 213 from the Eastern Deciduous For-est Biome, US-IBP.
and epiphytic (on the surface of submergedaquatic plants). Allen (2) uses Wetzel's term"epiphytic periphyton" to describe both the at-tached algae and bacteria on aquatic plants.
In many aquatic environments, the epi-phytes have been shown to be an importantproductive component of the ecosystem. Astudy of the algal epiphytes of Utricularia inthe Everglades National Park suggests the pos-sibility that the epiphytes rather than theirmacrophyte hosts are responsible for most ofthe primary production (7). The epiphytic algaein the littoral zone of a small shallow lake inMichigan were shown to contribute approxi-mately 31% of the littoral primary production(2). The productivity of the epiphytes in a smallEnglish pond were shown to exceed that of thephytoplankton (15), whereas in a marine envi-ronment the blue-green epiphyte Dicothrix con-tributed 15% of the coastal Sargassum commu-nity production (9). The epiphytic alga Oedogo-nium, which forms a surface mat on Myriophyl-lum spicatum in Lake Wingra, Wisconsin, wasalso shown to be an important producer (18).The purpose ofthis research has been to ascer-
tain the role of the epiphytic algae in the pri-mary productivity of the littoral zone of LakeGeorge, an oligotrophic glacier-formed lake sit-uated in the Adirondack Mountains of EasternNew York State. Objectives have been to deter-mine: (i) the physical and chemical factorswhich limit or stimulate epiphyte growth; (ii)the variations in the role of the epiphytes due toenvironmental influences such as season, loca-tion, depth, and macrophyte host; (iii) the iden-tity of the organisms comprising the epiphyticalgal communities; and (iv) the percentage ofthe littoral macrophyte community productionattributed to the epiphytic algae.
MATERIALS AND METHODSSample collection. There are over 40 species of
rooted macrophytes commonly found in the littoralzone of Lake George (E. C. Ogden, K. Dean, C. W.Boylen, and R. B. Sheldon, Aquatic Plants of LakeGeorge, New York, in press). The epiphytic popula-tions may be suspected to vary depending on themacrophyte species with which the community isassociated. To do a comprehensive study of the com-munities found on each of the many species would behighly impractical. Therefore, experiments wereperformed on algal assemblages taken from plantsof a single species, Potamogeton amplifolius, com-mon throughout Lake George, predominating at a 3-m depth (6). Data were collected from June throughOctober, 1974.
Lake George consists of two basins partially sepa-rated near the middle by an area known as the"Narrows" (Fig. 1). Traditionally the lake has beenclassified as oligotrophic; however, in recent yearswith increased urbanization the southern half hasbecome considerably productive. There exists a five-fold difference in rooted macrophyte productivitybetween the two basins (R. B. Sheldon and C. W.Boylen, submitted for publication). Three experi-mental sites were chosen for seasonal measure-ments, one each in the southern and northern basinsand a third station near the only outlet for LakeGeorge at Ticonderoga, New York, which supporteda heavy growth ofmacrophytes atypical ofthe north-ern basin. Smith Bay, location of the RensselaerFreshwater Institute, provided a source of epiphytepopulations for nonseasonal experimentation.
Leaves from plants of P. amplifolius and associ-ated epiphytes were collected in triplicate by diversat a 3-m depth using self-contained underwaterbreathing apparatus. Leaves were removed from thefourth to sixth position from the top of the macro-phyte and placed in empty, inverted 125-ml Erlen-meyer flasks allowing for minimum loss of epiphytesfrom the leaves. The flasks were recapped underwa-ter, brought to the surface, and returned to thelaboratory. Epiphytes were removed from the leavesby swirling in lake water, followed by rinsing theleaf surface with a water spray. Leaves were fragileand easily torn by more vigorous treatment. It wasestimated by microscopic inspection that this proce-dure removed more than 95% of the algae attached
HEARTS BAY
N2 OUTLET
SMITH BAY
LAKE GEORGE
2w 5~~5km
grX WARNER BAY
FIG. 1. Map of Lake George, N.Y., showing thefour sampling stations.
to the leaf surface. The washed leaf was placed in a160-ml milk dilution bottle containing 100 ml of lakewater. The epiphyte solution was adjusted to 100-mltotal volume in lake water. Sample water tempera-ture and pH were taken to insure that samplesremained at lake values. Samples containing theintact leaf and epiphytic community were placeddirectly in bottles containing 100 ml of lake water.For standardization of values all comparisons be-tween macrophyte and epiphyte productivity wereexpressed as grams of carbon assimilated per hourper unit of surface area of the host macrophyte. Thedry weight-to-wet weight ratio was determined ex-perimentally and was used in conversions from wetweight to dry weight and ultimately to leaf surfacearea (Fig. 2).
Radioactive tracer experiments. The hourlyrates of net photosynthesis were determined using amodification of Wetzel (29). After 15 min for thermalequilibration, 1 1LCi of NaH'4CO3 at pH 9.5 (NewEngland Nuclear Corp.; specific activity, 100 uCi ofNaHCO3 per mg) was injected into each bottle. Incu-bations were run in duplicate with one dark controlfor 2 h on a rotating drum in an algal growth cham-ber (Chesapeake Bay Institute, Johns Hopkins Uni-versity, Annapolis, Md.) equipped with a fluores-cent light source rheostat controlled to yield a maxi-
FIG. 2. Relationship among macrophyte dryweight, wet weight, and surface area of leaves fromP. amplifolius collected at 3 m. Two independentcollections were made. Symbols: 0, dry weight-to-surface area ratio; *, dry weight-to-wet weight ratio.
mum of 8,070-lux light intensity. Addition of anincandescent light source did not increase the photo-synthetic capacity of the algae. Incubation tempera-tures duplicated the temperature of the water fromwhich the samples were taken. Uptake kineticswere linear in the region from 1 to 3 h, suggestingthat population changes were not occurring duringthe course of the experiments. The incorporation oflabel by the epiphytes was terminated by filtrationthrough a 0.45-jtm membrane filter and subsequentwashing with distilled water. The membrane filterwas dried to constant weight at 104 C. Dry weightmeasurements were made to determine algal bio-mass, followed by dissolution overnight in a liquidscintillation vial containing 10 ml of Aquasol (NewEngland Nuclear Corp.). Each sample was agitatedon a mechanical mixer, and the resultant suspen-sion of fine particles gelled with 2.5 ml of water,forming a homogeneous counting medium. Rates ofexcretion of photosynthetic products by epiphyticalgae were determined by the method of Wetzel andManny (30).The assimilation of inorganic carbon by macro-
phytes was terminated by removing leaves from theaqueous medium and rinsing them successively for 4s in 0.1 N HC1 and distilled water, after which theplant tissue was frozen at -15 C until further proc-essing. Leaves were dried to constant weight at104 C followed by digestion in 5 ml of 1 N NaOH for30 min in a boiling water bath. The solutions werecooled and neutralized with 5 ml of 1 N HCl, and theplant material was further fragmented in a glasshomogenizer. An aliquot of this solution was thentransferred to a vial containing 10 ml of Aquasol.Radioactivity was determined using a Beckmanmodel LS-133 liquid scintillation counter (BeckmanInstruments, Wakefield, Mass.). Extracellular 14Cdeposition and non-photosynthetic uptake of[14C]bicarbonate were accounted for by the use ofdark controls. Quench corrections were made by theexternal standard method with verification by theuse of internal standards. The contribution of thephytoplankton was determined for each experimentby the use of control samples containing lake waterfrom each respective station.
The validity of laboratory studies in evaluatingthe role of the epiphytes in their aquatic habitatnecessitated a comparison between in situ incuba-tions and incubation in an algal growth chamber.Close agreement in photosynthetic rates were ob-tained, indicating that environmental parameterssuch as light intensity, temperature, and agitationcould be satisfactorily duplicated in the laboratory.
Photosynthetic rate determination. The photo-synthetic rates of the epiphytes and macrophyteswere calculated in terms of inorganic carbon fixa-tion. The conversion from radioactivity (disintegra-tions per minute) to photosynthetic rate was accom-plished according to nomographic procedures givenin Standard Methods (3). Measurements were madeof pH, temperature, and dissolved filtrable residue.Total alkalinity was determined by titration with0.02 N HCO to pH 4.4. Knowing the volumes of theincubation solutions, the amount ofcarbon fixed in agiven time interval was calculated as follows: milli-grams of carbon fixed = sample activity/added activ-ity x milligrams of initial inorganic carbon x 1.064(isotope effect). The use of alkalinity data to deter-mine inorganic carbon concentrations was substanti-ated by infrared spectrophotometry, indicating neg-ligible contributions by noncarbon forms of alkalin-ity.
Nutrient stimulation. Using N as KNO3 andNH4Cl, P as KH2PO4, S as K2SO4, Si as Na2SiO3, andC as NaHCO3, nutrients were added to 100-ml sus-pensions of epiphytic algae in lake water and wereincubated with NaH'4CO3 for 2 h in the algal growthchamber. Control samples containing no additionalnutrients were used to determine the unstimulatedphotosynthetic rates.
RESULTSEffect of physical parameters. Tempera-
ture has previously been found to be an impor-tant variable in algal photosynthesis (2, 5). Anexperiment was performed in midsummer todetermine the effect of temperature variationon the photosynthetic rate ofepiphyte communi-ties. The results presented in Fig. 3a indicate atemperature optimum of 30 C. This is slightlyhigher than the maximum summer environ-mental temperature of 24 C occurring in earlyAugust.
Since epiphytes were always taken fromleaves of plants growing at 3 m, it was neces-sary to determine what effect light intensityhad on epiphyte photosynthesis. Photosyn-thetic rates were determined at various intensi-ties up to 19,368 lux, yielding the curve pre-sented in Fig. 3b. Maximum photosynthesis oc-curred at approximately 8,608 lux, with a slightdecrease thereafter. The decline at higher lightintensities may be due to photosynthetic inhibi-tion (13). All subsequent laboratory experi-ments were carried out at 8,070 lux in the algalgrowth chamber. The time ofday had a noticea-
FIG. 3. Uptake of H'4C03- by epiphytes fromamplifolius as a function oftemperature (a) and li
intensity (b). Triplicate samples were removed frplants collected at 3 m, and homogeneous aliquwere incubated in the presence of 1 IACi ofNaH'4Cfor 2 h. Graphs (a) and (b) represent independercollected samples. Graph (a) has been correcteddark controls. Bars represent range of valuestained.
ble effect on the resulta't photosynthetic ri
of samples incubated in situ. To determine tmagnitude of this effect an experiment uperformed in which identical samples were inbated in Smith Bay at different times of diThe data in Table 1 indicate that maximiphotosynthesis occurred in the early afterno
Relative light penetration measureme
were taken during the summer at the four 9tions. A Gossen light exposure meter enca
in plastic was read at 3 m by the diver. Li1intensity at Warner Bay and the outlet avaged 30%, whereas the intensity at Hearts a
Smith Bay was approximately 40% of surflight intensity. Midday light intensities ranj
from 5,380 lux at 3 m with an overcast sky26,900 lux with a clear sky. The variationtemperature with depth was negligible atthree monthly sampling stations, since the (
lections were made far above the thermocliDissolved oxygen measurements indicated tsaturation conditions existed at all stationsall sampling dates. Measurements ofpH var
from 7.2 to 7.7 throughout the lake.
Relative contributions from epiphytes andmacrophytes to littoral productivity. For thepurpose of comparing the photosynthetic ratesof the epiphytes at different locations in LakeGeorge, the epiphyte photosynthetic rate was
expressed in terms of the surface area of themacrophyte leaf from which the epiphytes weretaken. To ascertain the significance of the epi-phytic population in this process, comparisons
0 were made by determining the photosyntheticrates of the macrophyte leaves alone, epiphytesalone, and the intact macrophyte-epiphyte sys-
tem. The latter determination yielded resultswhich were highly variable, because the epi-phyte communities were very small and contrib-uted to the overall photosynthesis in an amountless than the inherent variability in photosyn-thetic rates of the macrophyte leaves them-selves.The seasonal epiphyte photosynthetic rates
at various locations in Lake George are pre-
sented in Fig. 4a. All experiments were per-
formed under conditions of light saturation and00 ambient lake temperature. When the epiphyte
photosynthetic rate is expressed as a percent-P. age of the total photosynthetic rate of the leafght plus epiphytes, the extent ofthe epiphyte contri-`om bution to productivity is obtained on a seasonaltots basis (Table 2). In most instances, the epiphytes0tly contributed a slightly greater percentage of thefor total productivity in Warner Bay than at theob- other two stations. The average contribution of
the epiphytes was approximately 5% of that fortheir macrophyte host, P. amplifolius. Epi-
ate phyte biomass estimates were performed simul-the taneously with the photosynthetic rates at thevas three stations from June to October, 1974 (Fig.Cu- 4b). Peak epiphyte biomass was obtained inay. midsummer for both Warner and Hearts Bayum and slightly later for the outlet station.on. The epiphytic communities were found to dif-!nts fer in productivity with respect to their position;ta- on the macrophyte. The data in Table 3 indicatesedght TABLE 1. Diurnal variation in epiphyte in siturer- photosynthetic ratea
* The experiment was performed in triplicate with correc-tions for dark controls. Light intensities are low due tocloud cover throughout the experimental period. Surfacelight intensity ranged from 21,520 to 37,660 lux. SD, Stand-ard deviation.
FIG. 4. Seasonal photosynthetic rate (a) and bio-mass (b) of epiphytes from leaves of P. amplifoliuscollected at3 m. Graph (a) represents duplicate deter-minations corrected for dark controls; graph (b) rep-resents averages of triplicate determinations. Dataare expressed in terms of the leaf surface area of thehost macrophytes collected from three stations: *,Warner Bay; A, Hearts Bay; *, outlet.
that the epiphytic algae on lower leaves weremore productive than those on upper leaves.Because older leaves ofP. amplifolius were lessproductive than younger leaves, the relativeproductivity contribution by the epiphytes in-creased substantially on older leaves. AlthoughP. amplifolius was used throughout most ofthis study, a comparison of the epiphytic com-munities of three other species of rooted macro-phytes was made. Results are presented in Ta-ble 4. They indicate that the epiphyte commu-nity associated with Najas flexilis was the mosthighly productive for the four macrophyte spe-cies studied. Although P. amplifolius growsmost abundantly at the 3-m depth, the plantdoes grow at a range between less than 1 to 5 m.The variability in the productivity of the epi-phytes taken from plants growing at differentdepths was investigated. Table 5 indicates that,although the epiphytes were more productive
at the 3-m depth, the relative epiphyte biomasscontribution was greatest at the 1-m depth.
Nutrient studies. To determine if nutrientlimitation exists for epiphytes in Lake George,an experiment was designed in which differentamounts of nutrients were added to the lakewater in which the epiphyte incubations wereperformed. Any change in photosynthetic ratewas detected by expressing the ratio of the pho-tosynthetic rate ofthe solutions containing addi-tional nutrients to the photosynthetic rate of acontrol group of epiphytes which had no addednutrients. The results are presented in Table 6.In this experiment most of the nutrients resultin an inhibition ofgrowth, with the exception ofbicarbonate, which stimulated the growth rateby as much as 30% in a 2-h period. This wouldindicate the possibility that carbon is the limit-ing nutrient for epiphytes in Lake George. Thebicarbonate stimulation data are representedgraphically in Fig. 5. The slight change in pH(7.4 to 8.3) due to bicarbonate addition probablywould not be responsible for the increase inphotosynthetic rate, as indicated by studies oncarbon limitation by Allen (1), since a pH risewould decrease the available CO2.
Algal floristic studies. The relative abun-dances of the various epiphytic diatoms presentin the northern and southern basins of LakeGeorge during the investigation period (Junethrough October, 1974) are found in Table 7.The nondiatom algae represented an insignifi-cant contribution to the epiphytic communities.The total concentrations of diatoms present onthe middle leaves ofP. amplifolius were highlyvariable, with densities ranging between 3 x106 and 1.4 x 108 diatoms/M2 of leaf surfacearea. The major nondiatom components of theepiphytic community include the green algaeProtoderma, Scenedesmus, Spyrogyra, andMougeotia, the blue-green algae Nostoc, Spiru-lina, and Oscillatoria, and the desmid Cosmar-ium.
DISCUSSIONA number of factors have been shown to be of
considerable importance in regulating thegrowth of epiphytic algae in Lake George.Since the temperature optimum for epiphytegrowth was 30 C and the maximum lake watertemperature was 24 C, it is evident that temper-ature is a rate-controlling factor for photosyn-thesis in natural algal assemblages. Canaleand Vogel (8) have likewise demonstrated agrowth rate optimum of 30 C for diatoms. Anyfuture rise in the seasonal lake water tempera-ture would be expected to increase the produc-tivity of the present epiphyte community (23).
Average water temperature at 3 20.7 24.0 24.0 20.0 10.5m (C)
6 Relative epiphyte contribution is the percent contribution by the epiphytic algae to the total primary productivity oftheleaf and epiphyte constituents. Data from samples taken from Smith Bay under the ice on 3/13/75 indicate that, although P.amplifolius and its algal epiphytes are still viable, the epiphyte contribution to primary productivity during the winter isless than 1.0%. Data for photosynthetic rates are presented as mean ± standard deviation.
TABLE 3. Variation in epiphyte productivity with leafposition
However, a rise in seasonal temperature wouldnot necessarily result in increased activity,since population changes may occur (5). Patrick(22) suggests 30 C as the temperature above
which the composition of benthic algae shiftsfrom diatoms to greens. Although light inten-sity to the 3-m depth indicated saturation formost of the daylight hours, the epiphytic com-
a Concentration per liter does not include the amountpresent in the lake water prior to nutrient addition.
b 95% confidence limits are + 0.084 as determined bypooling variances for all nutrient data after verification byCochran's test (10).
munity below this depth has light as a limitingfactor for productivity. Any increase in the tur-bidity of the water would decrease photosyn-thesis in the regions receiving insufficient lightand would effect a rise in the depth of theeuphotic zone. Increased turbidity is usuallydue to phytoplankton growth indicative ofhigher nutrient levels, which could tend to in-crease epiphyte productivity in the littoralzones. Therefore, a smaller volume of the lakewould be involved in primary production, butits rate would be greater in areas where it doesoccur. Relative light penetration measure-ments already indicate greater turbidity in the
littoral regions of the southern basin.The diurnal effect observed for the epiphytes
in situ indicated maximum photosynthesis inthe early afternoon. This is not consistent withthe theory of midday photosynthetic inhibition(4) but may be explained by the overcast skyduring the experimental period or the reductionin light intensity at the 3-m depth. Stross et al.(26) suggest the role of nutrients in affectingdaily rhythms in photosynthetic rates of LakeGeorge phytoplankton.The epiphytes exhibited their maximum pho-
tosynthetic capacity in midsummer, which aver-aged slightly higher in Warner Bay, furthersuggesting the influence of human activity inthe southern basin. The epiphytic algae contrib-uted to the primary productivity of the macro-phyte-epiphyte communities a seasonal aver-age of5.3% in Warner Bay, 3.4% in Hearts Bay,and 4.3% at the outlet (Table 2). The value of10.8% obtained at the outlet in October can beseen more as a reflection of the faster decline inmacrophyte productivity than an indication ofincreased epiphytic algal growth. The epi-phytes were responsible for less than 1% of themacrophyte-epiphyte winter productivity as de-termined from samples taken under the ice inSmith Bay during the winter of 1975. Winter
2.0LU
1.8C-,
1.6
C,)oD 1.4C-
BICARBONATE ADDED mg/ 100mlFIG. 5. Stimulation of epiphytic algal photosyn-
thetic rates by the addition ofbicarbonate. Values arebased on triplicate determinations and include correc-tions for radioisotope dilution and dark controls.Rates are expressed as milligrams ofC per hour.
a Algae were preserved in formalin at a final concentra-tion of 4% and identified by the keys of Ward and Whipple(27) and Needham and Needham (21).
' Percentage is expressed in terms of total numbers ofspecies.
c North Basin includes data from Hearts Bay, SmithBay, and outlet.
dSouth Basin includes data from Warner Bay only.
productivity, although still measurable, wasgreatly reduced because of low temperaturesand limited light due to ice cover.Although excretion of photosynthate can be
very high with some algal cells, the epiphytesremoved from P. amplifolius excreted less than1% of the carbon fixed during a 2-h incubationat 22 C. In a study of phytoplankton popula-tions containing diatom species similar to thosefound in Lake George epiphyte communities,less than 2% of the carbon fixed during short-term experiments was excreted under incuba-tion conditions of population densities and inor-ganic carbon concentrations similar to thoseused in this investigation (19).The photosynthetic rate maximum of 0.6 mg
of C/M2 of macrophyte surface area per h inmid-August for the Lake George epiphytes is onthe order of 50 times less than the values ob-tained by Allen (2) in his studies on the epi-phytes of Scirpus acutus, Najas flexilis, andChara sp. in Lawrence Lake, Michigan (258 mgof C/M2 of macrophyte surface area per day,average). Such values are typical of lakes moreeutrophic than Lake George and can be as greatas 2,300 mg of C/M2 of surface area per day for
the epiphytic community associated with Myrio-phyllum spicatum in Lake Wingra, Wisconsin(18).The population densities ofthe epiphytic com-
munities followed the seasonal growth patternsof the rooted macrophytes, with maximal leafcolonization remaining essentially constant rel-ative to the leaf position on the plant. Theaverage seasonal epiphyte biomass in grams(dry weight) of epiphytes per square meter ofmacrophyte surface area was 1.54 at the outlet,1.12 in Hearts Bay, and 1.06 in Warner Bay.Both epiphyte and macrophyte productivity (Ta-ble 2), as well as population densities at thelake outlet, are atypical for the northern basin.This abundance may have been due to the visi-bly swift currents leaving the lake through thenarrow-channelled outlet, bathing the plants ina continuous supply of nutrients. The data forHearts and Warner Bay appear contradictoryto the average seasonal productivity data pre-sented in Table 2. This inconsistency may beexplained by the inherent variations in dry-weight determinations due to the contributionby detrital materials. Biomass estimates bychlorophyll extraction methods yielded evenmore variable results due to the low concentra-tions of epiphytic algae present in all samplescollected during the course of this study.
Other studies on epiphyte assemblages havebeen carried out in more eutrophic habitatsthan those present in Lake George. However,with increased urbanization of the villagesaround the southern half of this lake and themarsh areas draining only into the southernbasin, nutrient levels can be expected to in-crease. Such input has already influenced thehumic sediment character in the littoral areasof the southern basin (Sheldon and Boylen, un-published data). These factors have resulted ina fivefold difference in macrophyte and epi-phyte standing crops in the two basins (Sheldonand Boylen, submitted for publication). The epi-phyte standing crop differences are more a re-flection of greater macrophyte substrate areaavailable for colonization than a reflection ofgreater epiphyte productivity, since epiphytedensities appear similar for all stations (Fig.4b). Macrophytes have been shown to be thedominant producers in the littoral zone of LakeGeorge (Sheldon and Boylen, submitted for pub-lication). The maximum productivity occurredin Warner Bay and for all macrophytes was 140mg of C/M2 of littoral area per h, 10.4 mg ofC/M2 of littoral area per h for epiphytes, and12.9 mg of C/M2 of littoral area per h for phyto-plankton at the 3-m depth. In deeper regionsthe contribution by the phytoplankton in-
crt-nAses aS a Result o. the g eater volume ofwater, wherea 3 the macroph, te and epiphytecontributions decrease due to light limitation.These hourly productivity values can be extrap-olated to daily and seasonal productivities withcertain limitations. All productivity data havebeen calculated from photosynthetic rates deter-mined under conditions of light saturation (Fig.3b). Since productivity data can vary greatly ona daily basis during a single season because ofvarying light input, these data indicate thepotential contribution to littoral communityproductivity.The productivity of epiphytes from the lower
leaves was 10-fold greater than from the upperleaves, implicating the role of released nutri-ents in the decomposition of the lower leaves aswell as the longer time available for coloniza-tion. The choice of P. amplifolius as the repre-sentative rooted macrophyte for sampling ofepiphytic communities was supported by thedetermination that the relative epiphyte pro-ductivity for P. amplifolius fell between themaximum value obtained from Najas flexilisand the minimum value obtained from P. rob-binsii (Table 4). Considerable morphologicalvariation is exhibited by the four macrophytespecies examined. The Potamogeton spp. pro-duce single broad leaves born on stems and V.americana produces long ribbonlike leaves de-veloping from a single basal position, whereasN. flexilis produces abundant, closely clusteredleaves less than 1 mm wide and 20 mm long.Such variation may provide substrata for differ-ing degrees of success of epiphyte attachment.The release of materials by these plants, whichinhibit or stimulate epiphyte growth, is notknown.
Nutrient levels in Lake George are indicativeof the lake's current oligotrophic status (11).Phosphate levels throughout the lake are lessthan 5 gg of P/liter, and nitrate levels rangefrom 4 to 12 ug of N/liter; the higher concentra-tions are found in the southern basin. Alkalin-ity ranges from 21 to 25 mg of CaCO311iterthroughout the lake. A previous investigationon Lake George indicated that phosphorus wasthe limiting nutrient for Nitella flexilis (25).Fuhs et al. (12) found the addition of nitrogenand phosphorus to stimulate Lake George phy-toplankton growth when administered simulta-neously, but they also hypothesized the possibil-ity of carbon limitation. Williams and Clesceri(31) suggest the possible seasonal variation inlimitation by all three of the elements carbon,nitrogen, and phosphorus for the lake's diatompopulations. They further suggest the possibil-ity of a shift to other types of algae if the input
of these nutrients contil , to increase wh Zthe levels of silicon and manganese are ma:-tained. The use of the "IC method of detern::. -ing photosynthetic rates provides an excellentmeans ofassessing nutrient limitation by evalu-ating the effects of nutrient additions on photo-synthetic rates in algal stimulation studies.The addition of P043-, N03-, P043- + N03-,NH3, SiO32-, and S042- to epiphytic algae re-sulted in no stimulation of photosynthetic rateand in many cases had an inhibitory effect uponalgal growth. In the case of Si, the inhibitionmay have been due to the rise in pH effected byaddition of SiO32. It is unlikely that Si is alimiting nutrient for diatoms in Lake George,since concentrations range from 215 pg/liter inthe northern basin to 352 pgoliter in the south-ern basin (11). The addition of bicarbonate toalgal epiphytes stimulated photosynthesisgreater than 30% (when the decrease in specificradioactivity of the radioisotope was consid-ered), suggesting that carbon may be the limit-ing nutrient for these communities in LakeGeorge.
According to Liebig's Law of the Minimum,the total crop of any organism will be deter-mined by the abundance of the substance that,in relation to the needs of the organism, is leastabundant in the environment (16). Since carbonis the primary constituent of all organisms, it islikely to be a limiting nutrient, although inmost instances it has not been found to be defi-cient since it is readily available as dissolvedC02 from the atmosphere (24). The considera-tion of carbon as the limiting nutrient for epi-phytes in Lake George would imply that thediffusion rate of atmospheric C02 was insuffi-cient to support a maximal rate of photosyn-thesis. Kuentzel (17) has proposed a similarhypothesis concerning algal blooms resultingfrom C02 produced by bacterial decomposition.Goldman (14) elaborates on the controversyover carbon limitation. The possibility does ex-ist that the bicarbonate stimulation observed inthe epiphytes was actually a manifestation ofluxury carbon uptake, a phenomenon that mayoccur in P-limited as well as N-limited algae(12). However, the epiphytes were found to beneither P nor N limited.The low nutrient levels in Lake George are
suggested to be a major factor maintaining alarge species diversity of epiphytic algae. Theheavier nutrient load in the southern basin isreflected by the decrease from 21 predominantdiatoms in the northern basin to 17 predomi-nant diatoms in the southern basin. A percentincrease in the more eutrophic-associated dia-tom of the genus Synedra has occurred in the
southern basin in the short time since Williamsand Clesceri (31) first suggested the shift in di-atom populations due to trophic changes occur-ring in the lake. Genera common to oligotrophicfreshwaters such as Cyclotella, Navicula, andTabellaria are prevalent in the epiphytic com-munities of Lake George. In 1922, Needham etal. reported only four species of diatoms but in-cluded a greater relative abundance of greenand blue-green algae (20).The epiphytic algae of Lake George contrib-
ute a small amount to the total primary produc-tivity of this aquatic ecosystem. For the presenttime their contribution is almost negligible,since the epiphytes are responsible only for ap-proximately 5% of the littoral macrophyte-epi-phyte component of the total lake primary pro-ductivity. The role of the epiphytes as food forgrazing forms in the littoral zone is important.Should nutrient or other factors in the lakechange so as to increase algal growth, the roleof the epiphytes could be considerably en-hanced. The results of this study in an oligo-trophic lake and similar studies in more eu-trophic environments (2, 7, 15, 18, 28) suggestthat the role of algal epiphytes in primary pro-ductivity becomes more important as thetrophic level of the aquatic ecosystem ap-proaches the eutrophic state.
ACKNOWLEDGMENTSAppreciation is offered to J. J. Ferris for his critical re-
view and helpful suggestions during the preparation of themanuscript.
This research was supported by the Eastern DeciduousForest Biome, US-IBP, funded by the National ScienceFoundation under Interagency Agreement AG-199, BMS69-01147 A09, with the Energy Research and DevelopmentAdministration, Oak Ridge National Laboratory.
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