J. Great Lakes Res. 8(1):169-183 Internat. Assoc. Great Lakes Res., 1982
SEASONAL ABUNDANCE PATTERNS OF DIATOMS ON CLADOPHORA IN LAKE HURON
R. Jan Stevensonl and E. F. Stoermer Great Lakes Research Division University of Michigan Ann Arbor, Michigan 48109
ABSTRACT. Rocks bearing Cladophora were collected from May to November 1979 at two locations near Harbor Beach, Michigan, in Lake Huron to document seasonal patterns ofepiphytic diatom abundance and diatom proportion ofthe Cladophora-epiphyte assemblage biomass in an area receiving effluent from a municipal wastewater treatment plant. Data were examinedfor evidence of interactions between epiphytic diatoms and Cladophora. Cladophora first appeared in May at which time epiphytic diatoms comprised about 30% ofthe Cladophora-epiphytic assemblage biomass. Cladophora growth was greatest in June and July, accumulating much faster than diatoms. Peak Cladophora-epiphyte assemblage biomass was maintained from July to September. Cladophora biomass apparently decreased after August while diatom abundance increased to a September maximum. Diatoms were responsible for the sustained peak ofCladophora-epiphyte assemblage biomass as diatoms comprised over 60% ofthe assemblage biomass in September. The Cladophora-epiphyte assemblage collapsed by October. Low diversity of the epiphytic diatom taxocene and low diatom proportion of the Cladophora epiphyte assemblage biomass indicated Cladophora may have outcompeted diatom epiphytes during the June-July Cladophora growth pulse. Subsequently epiphytic diatoms may have enhanced Cladophora sloughing by shading and successful nutrient competition.
INTRODUCTION problems associated with Cladophora, some epi phytes of Cladophora are important components of Epiphytes associated with Cladophora contribute energy flow in aquatic biological systems. Epiphytic substantial biomass to shoreline nuisance algal diatoms and bacteria are among the most efficiently growths. Bacteria, algae, protozoa, and inverte assimilated foods for some invertebrates (Hargraves brates accumulate upon the long filaments of 1970). Gammarus pulex L. and Asselus aquaticus Cladophora. Taft and Kishler (1973) estimated that L. graze diatoms from Cladophora filaments in Cladophora increased the surface area available for several rivers (Moore 1975). Stalked protozoa algal colonization by 4,000 km2 in an 18 km2 area commonly occur in substantial numbers (Taft and of the Ohio Islands region of western Lake Erie. Kishler 1973) and probably feed upon the detrital Epiphytic organisms colonize Cladophora as bacteria-algal epiphytes. Snails fed diatoms had heavily as any other filamentous alga. The absence greater fecundity than those fed Cladophora (R. of mucilage on filaments of Cladophora facilitates Patrick, Acad. Nat. Sci. Phil., pers. comm.). epiphyte attachment. The thick growths and highly Epiphytes were major components of aquatic insect branched thallus of Cladophora provide a refuge diets in many studies cited by Soszka (1975). The that reduces removal of epiphytes that could result minnow Chrosomus erythrogaster also effectively from wave disturbance. The standing crop biomass grazed epiphytes in a Minnesota stream (Phillips of diatoms on Cladophora can be greater than 1969). biomass of Cladophora itself in brackish water A substantial amount of research has considered (Jansson 1967) and in the Great Lakes (Stoermer, macrophyte-epiphyte interactions. Mucilage cover unpublished data). of the host substrate surface may decrease as the In addition to enhancing the potential nuisance plants become older, thereby enabling firmer at tachment of epiphytic organisms (Ballantine 1979). I Present address: Department of Biology, University of Louisville, Louisville, KY 40292. Precipitation of CaC03 by Potamogeton inhibited 169 170 STEVENSON and STOERMER epiphytism (Cattaneo 1978). Fitzgerald (1969) re ONTARIO ported low epiphyte crops on Cladophora in low nitrogen waters because Cladophora acted as a nitrogen sink. Nutrient and dissolved organic carbon exchange between the host substrate and epiphytes has been documented. Allen (1971) demonstrated macro phyte release of dissolved organic carbon in sub stantial amounts in a form usable by epiphytic algae and bacteria. Harlin (1973) documented epiphyte uptake of carbon and phosphorus released MICHIGAN from the macrophyte host. McRoy and Goering (1974) documented nitrogen transfer from host to epiphytes and explained the presence of large ONTARIO epiphyte standing crops in nitrogen-poor waters by nitrogen transfer after uptake from sediments by the host. Penha1e and Thayer (1980) recorded epiphyte uptake of 15 to 100% of phosphorus released by the host. Cattaneo and Kalff (1979) found greater alkaline phosphatase activity by FIG. 1. Sampling locations in Lake Huron near Harbor epiphytes on artificial than natural plants. They Beach, Michigan. suggested macrophytic supplementation of the phosphorus supply available to epiphytes, even Beach municipal wastewater treatment plant is though epiphyte biomass did not increase. discharged to Lake Huron via Spring Creek. Epiphytes also have an impact upon their host Samples were collected at sites 0.14 km south substrate. Harlin (1973) demonstrated transfer of (Location 4) and 0.18 km north (Location 6) of the phosphorus and carbon from epiphytes to host. stream mouth. Additional, special-purpose samples Howard-Williams, Davies, and Cross (1978) were made at a site 0.09 km south of Spring Creek showed that bacteria pitted the surface of (Location 4.5). Potamogeton leaves. Host photosynthesis was re Rocks bearing Cladophora were collected from tarded by reduced diffusion of HC03 to heavily Locations 4 and 6 on 14 May, 2 June, 28 June, 12 epiphytized leaves in low ambient HC03 environ July, 25 August, 18 September, 19 October, and 15 ments (Sand-Jensen 1977). Shading of the host November 1979. The rocks were in water between plant by epiphytes also reduced photosynthesis 0.25 and 0.75 m deep. Rocks were dipped once in (Sand-Jensen 1977) and reduced growth of macro lake water to remove the loosely associated silt phytes in more nutrient-enriched waters (Eminson diatom matrix, placed in bags, and stored frozen. and Phillips 1978). After thawing, the area covered by Cladophora was The objectives of this study were to evaluate outlined with a grease pencil for subsequent plani population and taxocene patterns of diatoms on meter measurement. Cladophora and epiphytes Cladophora as a function of season (May to were picked from the rock surface and placed in a November) in an area impacted by wastewater crucible for biomass determination. treatment plant effluent. Another purpose was The area outlined on the rocks was waxed. After estimations of the diatom epiphyte proportion of cooling, the wax was removed from the rock with the Cladophora-epiphyte assemblage biomass with attention focused on not stretching the wax form. respect to the temporal variable. Evidence which The wax form was traced on a piece of paper. Area suggests interactions between diatom epiphytes and of rock surface covered by Cladophora was deter Cladophora is presented and discussed. mined by planimeter measurement of the traced area (Fox et al. 1969). Dry weight and ash-free dry weight were deter METHODS mined for each Cladophora-epiphyte sample. The The study area was located at Harbor Beach, weight of each crucible was measured and sub Michigan on Lake Huron near the mouth of Spring tracted from the weight of crucible and Cladophora Creek (Figure 1). Treated effluent from the Harbor assemblage after drying in an oven at lO5°C for 24 DIATOMS ON CLADOPHORA IN LAKE HURON 171 hours. After ashing the sample at 500°C in a muffle epiphyte biomass, and diatom taxocene diversity. furnace, rewetting to replenish water of hydration, Epiphyte abundance was calculated as In cells/ cm2 and again drying the sample at 105° C for 24 hours, of rock surface area. Diatom profusion was cells/ g the ash-free dry weight of samples was calculated as total assemblage ash-free dry weight. Diatom the difference between the ash weight plus crucible proportion of assemblage biomass of a sample was weight and the dry weight plus crucible weight. estimated as the June-Location 4.5 average diatom Samples were then prepared for enumeration of ash-free dry weight times the number of diatoms in the epiphytic diatom association. The ash of a sample divided by the ash-free dry weight of the samples was placed in 150-mL tall beakers with 100 Cladophora-epiphyte assemblage (or average mL of nitric acid and boiled for 3 hours to loosen diatom biomass times diatom profusion). Species aggregates. The silt-diatom frustule suspension was diversity (Shannon and Weaver 1949) and evenness repeatedly settled and the supernatant siphoned (Hurlbert 1971) were computed for each diatom from the beaker to remove nitric acid. Aliquots of taxocene. the acid-free homogenized suspension were placed Throughout this paper, the term assemblage on coverslips, dried, and mounted on slides with refers to Cladophora and all epiphytic organisms. HYRAX®. Taxocene is defined as the group of all diatom Two slides were prepared from each sample and populations. Population refers to all individuals of valves of diatom taxa along two transects were a single diatom species or variety. Use of these term enumerated from each slide to check sample follows guidelines set by Hutchinson (1967). preparation variation. At least 500 valves were FIDO programs (data base management system identified along the two transects of each slide of Great Lakes Research Division) were used to using a Leitz Ortholux microscope with an oil facilitate summarizing count data in an interactive immersion objective. When counts of any taxon form for subsequent statistical analyses. Statistical reached 100 valves, subsequent identifications of analyses were computed using the Michigan Inter that taxon were added to the count for abundance active Data Analysis System (MIDAS). calculations but not considered in computations for Seasonal patterns were tested using backward, 500 valve slide totals. We did this to reduce error in stepwise selection procedures for significant inde estimations of rare taxa abundances by large pendent variables to determine the "best" form of community proportions of abundant taxa such as the following polynomial regression model: Cocconeis pediculus and Cymbella prostrata var. auerswaldii. Additional collections were made by squeezing the water and epiphytes from masses of Cla where Yjk is the assemblage biomass, epiphytic dophora from Location 4 on 9 May 1979 and from diatom abundance, profusion, a diatom association Location 4.5 and another location between Spring diversity measure, or diatom proportion ofbiomass Creek and Location 6 (Figure 1) on 18 June 1979. of the kth replicate sample from the ith sampling The taxa in the algal suspensions resulting from date (Julian day). Bo is a constant and B1 ... 3 are squeezings during June were quite similar to those coefficients of the three levels of the independent in diatom taxocenes observed in the enumerations variable, sampling date (Xj, Julian day). The eik are above. The algal suspensions were preserved in 4% residuals of kth replicate sample from the ith formaldehyde. The average dry weight and ash-free sampling date. dry weight of a diatom in the suspensions were Backward, stepwise selective procedures (Draper calculated by determining the concentration of and Smith 1966) were performed on the regression diatoms in the samples and biomass of a measured model to establish significance (a =0.10) of various volume of algal suspension. The average dry and levels of the independent variable, time, in the ash-free dry weight biomass estimates of an epi model. A significance level of 0.10 was used in the phytic diatom were made by dividing the biomass selection procedure to generate more accurate of the diatoms by the number ofdiatoms in a mL of descriptions of the patterns. However, conclusions suspension. concerning the interpretation of the defined pat Data analyses were designed to reveal seasonal terns required a significance of a =0.05. Assump patterns of Cladophora-epiphyte assemblage bio tions of regression analyses were checked for all mass, epiphytic diatom abundance and profusion, significant (a = 0.10) equations. Deviations from a estimated diatom proportion of Cladophora- normal distribution of the residuals with mean 172 STEVENSON and STOERMER zero, independence, and homoscedasticity are indi JLg-N/L, ranged from 157.3 to 1475.0 JLg-N/L, and cated in presentation of the results. had a standard deviation of 474.67 JLg-N/L. We used polynomial regression to analyze sea sonal occurrence patterns. The least squares General Description of the regression fit provides the best estimate of popula Cladophora-Epiphyte Assemblage tion trends. We feel that this analysis is particularly Two hundred forty-five diatom taxa were identified appropriate since it minimizes the confusing effects in epiphyte taxocenes on Cladophora in Lake of residual variances due to local climatic or Huron near Harbor Beach, Michigan (Table 1). meteorological effects. If allows comparison or Cocconeis pediculus was generally the most population trends in, for example, successive years abundant diatom, averaging 26% of the epiphytic even though specific trends may be time displaced taxocenes. Fragilaria brevistriata, varieties of F. due to yearly variations in climatic cycle. pinnata, and Cymbella prostrata var. auerswaldii MIDAS output from the above polynomial each averaged about 7% of the diatom taxocenes. regression analysis does not include location means Although not enumerated, examination ofOctober nor Scheffe pairwise or multiple comparison allow samples before biomass determination revealed ances (SA) (Scheffe 1959). Analyses of variance substantial populations of the blue-green algae (ANOYA) output from MIDAS does include Fischerella muscicola (Thuret) Gomont and location means and Scheffe allowances, so ANOYA Chamaesiphon inerustans Grun. in Rabh. on the were run to obtain these statistics. Cladophora filaments. Estimates of average diatom biomass varied between 0.420 and 0.904 mg AFDW/106 cells for RESULTS the three samples collected. We chose our most conservative and representative estimate of diatom Physicochemical Description of Study Area ash-free dry weight as 0.420 mg/106 cells from Physicochemical data were collected at Locations 4 Location 4.5 in June because sizes of dominant and 6 during the summer of 1979 as part of a diatoms in the taxocene at Location 4.5 in June parallel study on Cladophora ecology (Auer et al. were most similar to those observed during the 1982, Canale and Auer 1982a and 1982b). Water study. Jansson's (1967) dry weight estimation of temperature and light were the only conditions Rhoicosphenia, Navicula, and Tabellaria was 4.8 which demonstrated seasonal patterns. Soluble mg/ 106 cells. This estimate was equal to the dry reactive phosphorus, total phosphorus, ammonia, weight of the average diatom in our average and nitrate concentrations in the water were sample. We did not estimate cell biovolumes for use extremely variable, due to wind induced changes in as a correction factor, although it may have position of the effluent plume. improved estimates of diatom biomass, because Temperature increased from a general May low diatom biomass is not necessarily linearly related to of 15°C to a July-August maximum of 23°C. By biovolume (Sicko-Goad et al. 1977). November the water temperature had dropped to 8°C. An upwelling event was evident in early May when water temperature suddenly dropped to Temporal Changes in Assemblage about 10° C. Light levels were greatest during late and Taxocene Patterns May and early June and ranged between 700 and Biomass of the Cladophora-epiphyte assemblage at 400 JLE/m2esec. Locations 4 and 6 reached a maximum during July, Soluble reactive phosphorus averaged 20.5 August, and September (Table 2, Figures 2 and 3). JLg-P/L, ranged from 3.0 to 54.2 JLg-P/L, and had Dry weight biomass peaked at 72.5 mg/ cm2 on 19 a standard deviation of 17.71 JLg-P/ L. Total September whereas ash-free dry weight peaked at phosphorus averaged 123.7 JLg-P/L, ranged from 8.4 mg/ cm2 on 12 July. Early and late seasonal dry 37.0 to 338.8 JLg-P/ L, and had a standard deviation weight biomass averaged 11.4 mg/ cm2 as compared of 83.66 JLg-P/L. to the mid-season value of about 48.4 mg/ cm2• Ammonia and nitrate were not measured Early and late seasonal ash-free dry weight throughout the season, but were in abundant averaged 2.0 mg/ cm2 in contrast to the mid-season supply. Ammonia averaged 54.3 JLg-N/L, ranged value of about 7.0 mg/ cm2• from 7.7 to 172.0 JLg-N/L, and had a standard It was necessary to supplement temporal pattern deviation of 44.2 JLg-N / L. Nitrate averaged 658.4 characterization by polynomial models (Equation DIATOMS ON CLADOPHORA IN LAKE HURON 173
TABLE 1. Diatom taxa observed in epiphytic communities on Cladophora. Achnanthes affinis Grun. Cymbella affinis Klitz. Achnanthes biasolettiana (Klitz.) Grun. Cymbella cistula (Ehr.) Kirchn. Achnanthes e/evei Grun. Cymbella cistula var. gibbosa Brun Achnanthes e/evei var. rostrata Hust. Cymbella delicatula Klitz. Achnanthes conspicua Mayer Cymbella hustedtii Krasske Achnanthes deflexa Reim. Cymbella microcephala Grun. Achnanthes detha Hohn et Hellerm. Cymbella microcephala val. crassa Reim. Achnanthes exigua Grun. Cymbella minuta Hilse Achnanthes hauckiana Grun. Cymbella minuta fo. latens (Krasske) Reim. Achnanthes hauckiana var. rostrata Schultz Cymbella minuta var. silesiaca (Bleisch) Reim. Achnanthes lanceolata (Breb.) Grun. Cymbella naviculiformis Auersw. Achnanthes lanceolata var. dubia Grun. Cymbella parva (W. Sm.) Cl. Achnanthes lanceolata val. elliptica Cl. Cymbella parvula Krasske Achnanthes lanceolata var. omissa Reim. Cymbella prostrata (Berk.) Cl. Achnanthes lapponica Hust. Cymbella prostrata val. auerswaldii (Rabh.) Reim. Achnanthes laterostrata Hust. Cymbella sinuata Greg. Achnanthes linearis (W.Sm.) Grun. Cymbella sp. #18 Achnanthes linearis fo. curta H.L. Sm. Cymbella sp. #4 Achnanthes minutissima Klitz. Cymbella tumida (Breb.) V.H. Achnanthes pinnata Hust. Denticula tenuis var. crassula (Nag.) W. et G. S. West Achnanthes sp. #17 Diatoma tenue Ag. Achnanthes spp. Diatoma vulgare Bory Actinocye/us normanii fo. subsalsa (Juhl.-Dannf.) Hust. Diploneis oculata (Breb.) Cl. Amphipleura pellucida (Klitz.) Klitz. Epithemia spp. Amphora michiganensis Stoerm. et Yang Epithemia zebra (Ehr.) Klitz. Amphora ovalis var. affinis (Kliz.) V.H. Fragilaria brevistriata Grun. Amphora ovalis val. constricta Skv. Fragilaria brevistriata val. capitata Herib. Amphora ovalis val. gracilis (Ehr.) V.H. Fragilaria capucina Desm. Amphora ovalis var. pediculus (Klitz.) V.H. Fragilaria construens (Ehr.) Grun. Amphora perpusilla (Grun.) Grun. Fragilaria construens var. binodis (Ehr.) Grun. Amphora rotunda Skv. Fragilaria construens val. minuta Temp. et M. Perag. Amphora spp. Fragilaria construens val. subsalina Hust. Anomoeoneis vitrea (Grun.) Ross Fragilaria construens var. venter (Ehr.) Grun. Asterionella formosa Hass. Fragilaria crotonensis Kitton Caloneis bacillum (Grun.) Cl. Fragilaria intermedia Grun. Caloneis bacillum val. lancettula (Schultz) Hust. Fragilaria leptostauron (Ehr.) Hust. Caloneis hyalina Hust. Fragilaria pinnata Ehr. Caloneis sp. #1 Fragilaria pinnata var. ? Cocconeis diminuta Pant. Fragilaria pinnata val. intercedens (Grun.) Hust. Cocconeis pediculus Ehr. Fragilaria pinnata val. lancettula (Schum.) Hust. Cocconeis placentula var. euglypta (Ehr.) Cl. Fragilaria sp. #18 Cocconeis placentula var. lineata (Ehr.) V.H. Fragilaria spinosa Skv. Cocconeis sp. #2 Fragilaria spp. Cye/otella comensis Grun. Fragilaria vaucheriae (Klitz.) Peters. Cye/otella comta (Ehr.) Klitz. Fragilaria vaucheriae var. capitellata (Grun.) Patr. Cye/otella keutzingiana Thw. Fragilaria vaucheriae var. lanceolata Mayer Cye/otella meneghiniana Klitz. Fragilaria vaucheriae val. parvula (Klitz.) Cl.-E. Cye/otella michiganiana Skv. Fragilaria vaucheriae var. truncata (Grev.) Grun. Cye/otella ocellata Pant. Gomphoneis herculeana (Ehr.) Cl. Cye/otella pseudostelligera Hist. Gomphonema angustatum (Klitz.) Rabh. Cye/otella sp. #6 Gomphonema intricatum var. dichotomum (Klitz.) Cye/otella sp. auxospore Grun. Cye/otella spp. Gomphonema intricatum var. pumila Grun. Cye/otella stelligera (Cl. et Grun.) V.H. Gomphonema olivaceoides Hust. Cye/otella wolterecki Hust. Gomphonema olivaceum var. calcarea (Cl.) Cl. Cyratopleura elliptica (Breb. et Godey) W. Sm. Gomphonema olivaceum (Lyngb.) Klitz. 174 STEVENSON and STOERMER
TABLE 1. Continued Gomphonema parvulum (Klitz.) Klitz. Navicula sp. #79 Gomphonema parvulum var. micropus (Klitz.) Cl. Navicula sp. #8 Gomphonema spp. Navicula sp. #80 Gyrosigma acuminatum (Klitz.) Rabh. Navicula sp. #81 Melosira granulata (Ehr.) Ralfs. Navicula sp. #82 Melosira islandica O. Mlill. Navicula sp. #88 Melosira italica subsp. subarctica O. Mlill. Navicula splendicula Van Landingham Melosira spp. Navicula spp. Navicula acceptata Hust. Navicula stroesei «(/)str.) Cl. Navicula accomoda Hust. Navicula subgastriformis Hust. Navicula aurora Sov. Navicula subrotundata Hust. Navicula balcanica Hust. Navicula subtilissima Cl. Navicula capitata Ehr. Navicula tantula Hust. Navicula capitata var. luneburgensis (Grun.) Patr. Navicula tripunctata (O.F. Mlill.) Bory Navicula cincta (Ehr.) Ralfs Navicula tuscula fo. minor Hust. Navicula cocconeiformis Greg. Navicula tuscula var. angulata Hust. Navicula costulata Cl. et Grun. Navicula viridula (Klitz.) Ehr. Navicula cryptocephala Klitz. Navicula viridula var. avenacea (Breb.) V.H. Navicula cryptocephala var. intermedia V.H. Navicula zanoni Hust. Navicula cryptocephala var. veneta (Klitz.) Rabh. Nitzschia acula Hantz. Navicula decussis (/)str. Nitzschia amphibia Grun. Navicula exigua (Greg.) Grun. Nitzschia angustata (W. Sm.) Grun. Navicula exiguiformis Hust. Nitzschia angustata var. acuta Grun. Navicula graci/oides Mayer Nitzschia apiculata (Greg.) Grun. Navicula gregaria Donk. Nitzschia dissipata (Klitz.) Grun. Navicula hustedtii fo. obtusa (Hust.) Hust. Nitzschia fonticola Grun. Navicula kriegeri Krasske Nitzschia frustulum (Klitz.) Grun. Navicula lanceolata (Ag.) Klitz. Nitzschia frustulum var. perminuta Grun. Navicula luzonensis Hust. Nitzschia frustulum var. tenella Grun. Navicula menisculus var. Krenneri Cl.-E. Nitzschia gracilis Hantzs. Navicula menisculus var. obtusa Hust. Nitzschiahantzschiana Rabh. Navicula minima Grun. Nitzschia inconspicua Grun. Navicula minima var. okamurae Skv. Nitzschia lauenbergiana Hust. Navicula minuscula Grun. Nitzschia palea (Klitz.) W. Sm. Navicula minusculoides Hust. Nitzschia palea var. debilis (Klitz.) Grun. Navicula monoculata Hust. Nitzschia palea var. ? Navicula mutica var. cohnii (Hilse) Grun. Nitzschia paleacea Grun. Navicula odiosa Wallace Nitzschia pusilla (Klitz.) Grun. emend. Lang-Bertalot Navicula oppugnata Hust. Nitzschia recta Hantz. Navicula paludosa Hust. Nitzschia romana Grun. Navicula pelliculosa Hilse Nitzschia sinuata var. tabel/aria (Grun.) Grun. Navicula peratomus Hust. Nitzschia sociabilis Hust. Navicula pupula Klitz. Nitzschia sp. #1 Navicula pygmaea var. Nitzschia sp. #10 Navicula radiosa Klitz. Nitzschia sp. #39 Navicula radiosa var. parva Wallace Nitzschia spp. Navicula radiosa var. tenella (Breb.) Cl. et Moll. Nitzschia tropica Hust. Navicula rotunda Hust. Nitzschia tryblionel/a var. debilis (Am.) Mayer Navicula salinarum Grun. Opephora sp. #3 Navicula scutelloides W. Sm. Rhoicosphenia curvata (Klitz.) Grun. Navicula seminuloides Hust. Stauroneis smithii Grun. Navicula seminulum Grun. Stephanodiscus alpinus Hust. Navicula sp. #24 Stephanodiscus hantzschii Grun. Navicula sp. #38 Stephanodiscus niagarae Ehr. Navicula sp. #44 Stephanodiscus sp. #10 Navicula sp. #48 Stephanodiscus spp. DIATOMS ON CLADOPHORA IN LAKE HURON 175
TABLE 1. Continued Stephanodiscus subtilis (Van Goor) CL-E. Synedra parasitica (W. Sm.) Hust. Surirella angusta Klitz. Synedra rumpens Klitz. Surirella ovata Klitz. Synedra rumpens var. fragi/arioides Grun. in V.H. Surirella ovata var. pinnata (W. Sm.) Rabh. Synedra rumpens var. meneghiniana Grun. in V.H. Surirella spp. Synedra sp. #17 Synedra acus Klitz. Synedra spp. Synedra delicatissima W. Sm. Synedra ulna (Nitzsch) Ehr. Synedra fili/ormis var. exi/is Cl.-E. Tabellaria fenestrata (Lyngb.) Klitz. Synedra minuscula Grun. Tabellaria flocculosa (Roth.) Klitz. Synedra ostenfeldii (Krieger) Ct.-E. Tabellaria flocculosa var. linearis Koppen
TABLE2. Results oftemporalpattern analyses ofCladophora-epq,hyte assemblage andepq,hytic diatom taxocenepa rameters (YoJ. Presented are the assemblage and taxocene parameters (dependent variables) andcoefficients (B,,) and significance of coefficients (a(B,,)) from the "best"form ofEquation (1). The "best"form was determined by stepwise backward regression of the dependent variable as a function ofpolynomial levels ofthe independent variable. Julian day (X'/'). Regression model assumptions which were not satisfactory are indicated. Constant ) X.2 X.3 (Bo Xi 1 1 Parameter Bo a (Bo) B\ a (B\) B2 a (B2) B3 a (B3) *g DW/cm2 -3.55 X 10-2 .26 3.80 X 10-6 .06 -1.04 X 10-8 .06 g AFDW/cm2 -1.44 X 10-2 .02 1.34 X 10-4 .00 -8.44 X 10-10 .00 Abundance 9.76 .00 2.53 X 10-4 .00 -6.64 X 10-7 .00 Profusion 1.00 X 10 10 .02 -1.45 X 108 .03 6.95 X 105 .02 -1.03 X 103 .03 Diatom proportion of assemblage biomass 4.21 .02 -6.09 X 10-2 .03 2.92 X 10-4 .02 -4.32 X 10-7 .03 Species Diversity 13.8 .01 -1.53 X 10-1 .03 6.56 X 10-4 .05 -8.95 X 10-7 .07 Evenness 3.69 .00 -4.21 X 10-2 .02 1.86 X 10-4 .03 -2.60 X 10-7 .04 Cover -40.87 .62 9.54 X 10- 1 .23 -2.34 X 10-3 .19 S: Skewness of residuals> 1.5 or < -1.5 *Assumptions not satisfactory K: Kurtosis of residuals> 1.5 or < -1.5
1) with Scheffe comparisons (available from September) peaks had negative coefficients for the authors by request) of monthly parameter means so linear time variable, positive coefficients for the the month of a parameter peak could be identified. squared time variable, and negative coefficients for The curves generated by the polynomial models the cubed time variable. Curves with early and late described the general pattern of changes in a season peaks of parameter values were generally parameter, but did not readily identify the month indicated by a negative coefficient for one time of a peak. Generally, curves with only a negative variable and a positive coefficient for a time coefficient for a time variable delineated an early variable of higher power. season peak of the parameter value. Curves with Diatom epiphyte abundance with respect to rock only a positive coefficient indicated a late season surface covered by Cladophora (1 n cells/ cm2) at peak. Curves with a positive coefficient for a time Locations 4 and 6 peaked in September with a variable and a negative coefficient from a time maximum of 16.1/ cm2 (Figure 4). A significant variable of greater power than the former showed a (PR, a = 0.00) increase in early seasonal abun mid-season peak. Bimodel curves had an early dances was followed by a significant (PR, a = 0.00) season peak and either a mid-season or late season decrease (Table 2). peak. Curves with early and mid-season (usually Diatom profusion [cells/ g total assemblage ash- 176 STEVENSON and STOERMER
100.0 ~tO.O ~ CJl E N E 80.0 ;:: 8.0 i\, u ::t: ...... C) ,' ,, c> E iii , \ , ~ ~ ,' , I- 60.0 ,\ ~ 6.0 , I , , Q \ 0 , w I \ ~ I \ ~ >- , \ a: 0:: 40.0 lL 4.0 ~ 0 ::t: , w (/) I (!) , 16.0 '" E'" 16.0)( 108 o N :.s ~ 15.0 Q) ...... c> en il 12.0)( 108 QI E u 14.0 Q) c '"o w !?: 8.0)( 10 8 ~ 13.0 !!! Q) g u z :::> 12.0 z 4.0)( 108 lD Q 3.50 0.90 3.00 0.80 2.50 > f- en 2.00 ~ 0.70 0:: w W z / z / > w o 1.50 > / (f) w 0.60 \ / ~ \ ;f ~ 1.00 \ / a.. l:f (f) 0.50 0.50 : May: June: Jul ; Aug.: Sept. : Oct. : Nov. : 0.00 r.------0.40 ~"""""'-+,-_L....---I---''-----L-+---'-_-jJ-_....L--4 : May: June: July : Aug.: Sept.: Oct. : Nov. : 100 150 200 250 300 350 JULIAN DAY 100 150 200 250 200 250 JULIAN DAY FIG. 8. Temporal pattern of epiphytic diatom taxocene FIG. 9. Temporal pattern ofepiphytic diatom taxocene species diversity (Shannon and Weaver 1949). Triangles evenness (Hurlbert 1971). Triangles designate the ob designate the observed average of Locations 4 and 6. served average ofLocations 4 and 6. Circles designate Circles designate the pattern defined by polynomial the pattern defined by polynomial regression analysis regression analysis using Equation 1. Coefficients and using Equation 1. Coefficients and their significance their significance which define the pattern are presented which define the pattern are presented in Table 3. in Table 3. var. intercedens, F. sp. #18, Navicula cryptocephala The following discussion attempts a synthesis of var. intermedia, and N. radiosa var. tenella (Table our results and observations. Within the current 3). Several taxa maintained higher abundances state of the art it is not possible to positively from September to October while total diatom identify causation of some of the patterns and abundance decreased. These taxa were Achnanthes trends present in our data. Indeed some of them minutissima, Caloneis bacillum, Nitzschiajonticola, may not be general. We have taken the liberty to and N. inconspicua. engage in a certain amount of frank speculation in Despite the lower total diatom abundance at the order to convey our notion of most probable causes beginning of the season in May and the end of the and to point the way to most interesting areas for season in November, abundances of several taxa further research. were highest during one or both of these periods. Several diatom taxocenes developed and were May abundance peaks were noted for Diatoma replaced during the Cladophora season. Sessile tenue, Fragilaria vaucheriae var. capitata, and Fragilaria species and Amphoraperpusilla were the Gomphoneis herculeana (Table 3). A November numerically dominant epiphytes in late May and abundance peak was noted for Rhoicosphenia early June. Varieties of Fragilaria pinnata, and curvata. Gomphonema olivaceum abundances were undetermined variety of F. vaucheriae, and F. higher at the beginning and end of the Cladophora brevistriata were dominant components of the season, whereas Navicula tripunctata reached taxocene throughout the year. Cocconeis pediculus maxima in May and October. was the overwhelming dominant (about 40%) ofthe taxocene in late June through August. By Sep DISCUSSION tember, many of these diatoms and Cymbella One of the major objectives of this research was to prostrata var. auerswaldii were abundant in a very discover the plausible range of Cladophora diverse epiphyte taxocene. By November, Rhoicos epiphyte interactions within the habitat studied. phenia curvata emerged as the numerical dominant. DIATOMS ON CLADOPHORA IN LAKE HURON 179 TABLE 3. Results oftemporalpattern analyses ofdiatom population abundances (YilJ from samples ofCladophora- epiphyte assemblages. Presented are the population parameters (dependent variables) and the coefficients (BJ and significance ofcoefficients (a(B,,)) from the "best"form ofEquation (1). The "best"form was determined by stepwise backward regression ofthe dependent variable, abundance (YilJ, as a function ofpolynomialleveisofthe independent variable, Julian doy (X'!'). Regression model assumptions which were not satisfactory are indicated. Constant ) X.2 X.3 (Bo Xi 1 1 Taxon Bo a (Bo) B\ a (B\) B2(XIO=3) a (B2)B3(XIO=6) a (B3) Cocconeis pediculus -12.6 .00 .220 .00 -.457 .00 Amphora ovalis var. pediculus 3.69 .03 .270 .01 -7.47 .02 Amphora perpusil/a 33.58 .00 -.396 .oI 2.10 .01 -3.39 .00 • Cye/otella comensis .884 .71 .415 .01 -1.04 .03 Cymbella microcephala 4.59 .01 .280 .01 -.691 .02 Cymbella minuta 32.4 .02 -.392 .04 2.08 .02 -3.38 .02 Cymbella prostrata var. auerswaldii 42.0 .02 -.535 .03 2.79 .02 -4.48 .01 Fragilaria brevistriata 7.13 .00 .263 .00 -.692 .00 Fragilaria construens Fragilaria pinnata 7.66 .00 .215 .02 -.595 .03 Fragilaria pinnata var. intercedens 8.03 .00 .196 .03 -.525 .04 Fragilaria sp. #18 39.9 .01 -.484 .03 2.42 .02 -3.75 .02 Navicula cryptocephala var. intermedia 46.0 .07 -.728 .06 3.98 .03 -6.48 .02 Navicula radiosa var.tenella -.997 .63 .539 .00 -1.31 .00 Achnanthes minutissima 28.7 .02 -3.17 .07 1.61 .05 -2.49 .05 Caloneis bacil/um 2.42 .43 .416 .04 -1.02 .07 Nitzschia fonticola 3.97 .00 .051 .02 Nitzschia inconspicua 1.07 .64 .359 .02 -.857 .05 Diatoma tenue 10.2 .00 -.032 .00 Fragilaria vaucheriae var. capitellata 23.2 .00 -.156 .01 .272 .03 Gomphoneis herculeana 6.51 .00 -.019 .03 Rhoicosphenia curvata 8.76 .00 .032 .00 Gomphonema olivaceum 25.6 .00 -.148 .00 .839 .00 Gomphonema olivaceum 25.6 .00 -.148 .00 .839 .00 Navicula tripunctata 55.3 .00 -.710 .01 3.38 .01 -5.09 .01 S: Skewness of residuals> 1.5 or < -1.5 *Assumptions not satisfactory K: Kurtosis of residuals> 1.5 or < -1.5 Most abundant epiphytic diatom populations frequency environmental variability and statistical had distinct temporal maxima. The time of their problems such as mutlicolinearity would have abundance maxima did not necessarily coincide made correlation results unreliable. We presented with the peak Cladophora standing crop in June the environmental conditions in the results to and July. Some taxa were most abundant in May, generally characterize the Harbor Beach area. and others in October or November. About two Abundance maxima of populations before and thirds of the populations with significant temporal after the assemblage biomass maximum indicated patterns had abundance maxima in September, just seasonally dictated environmental conditions such after peak Cladophora standing crop. Only the as temperature and photoperiod may have been abundance of Cocconeis pediculus and Amphora more important for some diatom populations than ovalis var. pediculus had maxima coincident with the availability of Cladophora substrate. Cladophora. Cladophora-epiphyte assemblage biomass was We did not attempt correlation of the epiphytic about 10 mg DW/ cm2 or 1.0 mg AFDW/ cm2 from diatom dominants with the physical and chemical May through early June. Assemblage biomass then conditions that were discussed in the results. High increased to a sustained seasonal maximum from 180 STEVENSON and STOERMER July to September. The assemblage peak during Fitzgerald (1969) reported low epiphytic algal these three months varied from less than 30 mg standing 2 crops of Cladophora in low nitrogen DW/cm to more than 70 mg DW/cm2• waters and suggested Cladophora acted Diatom taxocene abundance as a demonstrated a nitrogen sink. Live, actively metabolizing seasonal pattern similar to assemblage macro biomass. phytic substrates have commonly been noted with The rate of accumulation of the diatom taxocene fewer epiphytes than dead macrophytes. It has been from early June to mid-July was apparently not as proposed that thallus mucilage reduces the capacity great as Cladophora. While taxocene abundance ofepiphytes to attach to the macrophyte (Ballantine increased slightly, the number of diatoms per gram 1979) and nutrient competition reduces the growth of assemblage biomass dropped significantly from rate of algal epiphytes on live substrates. Cla May to late June, then steadily increased to a dophora has very little mucilage. Nutrient competi September maximum. Similarly, the diatom pro tion was probably not for nitrate at these sites portion ofassemblage biomass decreased from 30% because of constant replenishment of nitrate from in May to 10% in late June. The diatom proportion nitrate-rich offshore waters. Competition for some of assemblage biomass subsequently increased to other macro- or micronutrient may have been about 2/3 of the assemblage. important. Cladophora biomass therefore increased faster Cladophora biomass apparently decreased after than biomass of the epiphytic diatom taxocene. August. The proportion of the substrate covered Rapid Cladophora biomass accumulation by has been Cladophora decreased from its July peak to a late regularly recorded during June and July (Bellis and season September minimum. As peak assemblage McLarty 1967, Mantai 1978, Storr and Sweeney biomass was maintained from July to September, 1971). The more rapid accumulation of Cladoph the diatom proportion of assemblage biomass ora than diatom epiphytes simply suggested that increased from about 20% to a seasonal maximum substrate (the Cladophora thallus) must be present of greater than 60%. Diatom numbers also demon before epiphytes can colonize it. The epiphyte strated a September maximum of about 1.0 X 107 proportion of a macrophyte-epiphyte assemblage 2 cells/ cm of rock surface area covered by biomass would therefore increase subsequent to the Cladophora. increase in macrophyte biomass. Alternatively, a non-diatom component Cladophora outcompeting of the epiphytic diatoms for assemblage other than Cladophora may nutrients may also have have contributed to the decreased to cause the increase in epiphytic diatom profusion diatom propor peak occurring 2 tion of assemblage biomass. This does months after peak not seem assemblage biomass was ob likely because casual observation of tained. We suspected fresh samples nutrient limitation of showed increasing amounts of blue-green epiphytes because species algal diversity had maxima in epiphytes as well as other forms. Therefore, May and September and main a minimum from late July tenance of the assemblage biomass peak to August. The evenness from July component of diversity through September was a result of diatom demonstrated the same biomass seasonal pattern. The low replacing the sloughing Cladophora biomass. diversity and evenness during the period of maxi Storr and Sweeney (1971) attributed the seasonal mum Cladophora growth indicated that only pattern of Cladophora growth to effects selected diatom populations of tem were able to colonize perature and photoperiod. They reported optimum and grow on the active Cladophora thallus. Cladophora growth at 18°C. Canale et al. (19820 Cocconeis pediculus was the opportunistic popu have concluded that Cladophora seasonal trends lation that rapidly colonized the Cladophora are very importantly related to light and tempera thallus. C. pediculus reached an abundance max ture cycles, even though spatial distribution ima in September. This at diatom taxon was also Harbor Beach is regulated by phosphorus significantly negatively correlated to species diver availability. sity and evenness. We have commonly observed C. We propose that thick coats of epiphytes around pediculus as the pioneer colonizer of Cladophora in the Cladophora may have accelerated sloughing. the Great Lakes and many midwestern streams and After Cladophora growth slowed and epiphytes lakes. C. pediculus may have been so successfully became a greater proportion of the assemblage opportunistic because it was the only diatom biomass, the physicochemical conditions may have population able to compete with Cladophora for been more conducive nutrients. for growth of epiphytic diatoms than Cladophora. Many epiphytic diatom DIATOMS ON CLADOPHORA IN LAKE HURON 181 populations were indeed able to colonize Cla sloughing were cropped at a few inches long. The dophora from July to September as indicated by occurrence of filament separation in the general the increase of diatom taxocene evenness to a zone along the filament where epiphytes and wave September maximum. action would have had their greatest impact may Nutrient starvation of Cladophora as a result of just have been a coincidence. Nonetheless, this an epiphyte nutrient shield could physiologically seemed a coincidence worth noting. weaken the filaments and enhance sloughing. Reduction of diatom abundance and profusion Epiphytes successfully outcompeting Cladophora and Cladophora-epiphyte assemblage ash-free dry for nutrients has not been demonstrated. Epiphytes weight from September to October was observed. did reduce HC03 diffusion to leaves of the macro The decrease of assemblage biomass was propor phyte Zostera marina L. (Sand-Jensen 1977). If tionally lower than diatom abundance, which seasonal conditions did cause nutrient uptake rates indicated that biomass of the non-diatom part of of Cladophora to be less than maximum and less the assemblage decreased more slowly than the than those ofepiphytes, this host-epiphyte relation diatom part. This was substantiated by the marked ship would seem to have been a likely occurrence. reduction in diatom profusion from September to Cladophora may also have been shaded by October. epiphytes. Cladophora growth is a direct function Wind induced wave disturbance could have of light intensity at optimal temperatures (Graham rinsed epiphytes from the assemblage. Herbivores et al. 1982). Sand-Jensen (1977) showed negative may have eaten epiphytes. If Cladophora and effects of epiphyte shading on eelgrass photo epiphytes decreased proportionally by sloughing, synthesis. Field and laboratory experiments have increased bacterial, blue-green algal, or fungal demonstrated reduced macrophyte growth in en biomass could have also accounted for the decrease riched aquatic systems which was attributed to in diatom profusion, not discounting herbivory as a shading by epiphytes (Eminson and Phillips 1978; source of epiphyte loss. Phillips, Eminson, and Moss 1978). Much of the Cladophora would have been more In addition to the enhancement of Cladophora senescent after the assemblage biomass peak and sloughing via possible mechanisms of outcompet thus more capable of releasing cellular compounds ing the host for nutrients and light, epiphytes have later in the season. Release and subsequent utiliza reportedly physically damaged cell walls. Howard tion of released compounds containing nitrogen, Williams et al. (1978) showed that bacteria pitted carbon, and phosphorus have been demonstrated the surface of Potamogeton leaves. Also, Geitler (Allen 1971, Harlin 1973, McRoy and Goering (1977) reported that Cocconeis placentula caused 1974, and Penhale and Thayer 1980). Bacteria, cell wall thickening and the production of blue-green algae, and fungi flourish in organically cystolithe-like protuberances of Fontinalis anti enriched environments; thus an increase in their pyretica Hedw. At Harbor Beach the walls of older proportion of assemblage biomass would seem to Cladophora cells were thicker than young cells at have been probable late in the seasonal cycle of the tip of the filament which had few epiphytes. The Cladophora. thick walls of Cladophora cells may have been an Competitive interaction between Cladophora indication of impact from heavy epiphyte coloniza and epiphytes was indicated by many of the results tion on the older cells nearer the base of the of this study. Cladophora outcompetes diatoms for filament. The process of cell wall thickening has substrate space early as filaments cover most rocks. been illustrated within Cladophora by Bornefeld Low diatom epiphyte abundance and diversity on (1979). Cladophora in June and July indicated Cladophora Tension on cells of Cladophora filaments from was more able to sequester nutrients than were wave action would have been greatest near the base epiphytes. High epiphytic diatom abundance and of filaments. The zone of greatest impact of the diversity and epiphyte proportion of assemblage epiphytes upon Cladophora would have been near biomass in September indicated diatoms were then the base of the filament rather than on the more growing faster than Cladophora. This successional sparsely epiphytized filament tips. This would have pattern may have been due to either genetically been the area of greatest physiological and physical predetermined seasonal senescence of the Cla weakening of the Cladophora filament and thus the dophora population or superior competitive abili most probable site of filament separation. ties of certain diatom populations under the Indeed, Cladophora filaments that remain after seasonally modified physical conditions. 182 STEVENSON and STOERMER ACKNOWLEDGMENTS or antagonism among bacteria, algae, and aquatic weeds. J. Phycol. 5:351-359. We would like to thank Drs. Martin Auer and Fox, J. L., Odlaug, T. 0., and Olson, T. A. 1969. The Raymond Canale for their assistance in obtaining ecology of periphyton in western Lake Superior. Part funds for this project. Tom Bugliosi deserves I. Taxonomy and distribution. Water Resources special recognition for sampling assistance. Fund Center, University of Minnesota, Minnespolis. ing for this study was supplied by the United States Geitler, L. 1977. Beeinflussung der Blattzellen von Environmental Protection Agency under Grant Fontinalis antipyretica durch den Bewuchs von No. R806600. Contribution No. 000 of the Great Cocconeis placentula. Plant Syst. Evol. 128:37-45. Lakes Research Division. Graham, J. M., Auer, M. T., Canale, R. P., and Hoffmann, J. P. 1982. Ecological studies and mathe matical modeling of Cladophora in Lake Huron. 4. Photosynthesis and respiration as functions of light LITERATURE CITED and temperature. J. Great Lakes Res. 8(1): lOO-ll1. Allen, H. L. 1971. Primary productivity, chemo Hargraves, J. L. 1970. The utilization of benthic micro organotrophy, and nutritional interactions of epi flora by Hyalella azteca (Amphipoda). J. Anim. Ecol. phytic algae and bacateria on macrophytes in the 39:427-437. littoral of a lake. Ecol. Monogr. 41(2):97-127. Harlin, M. M. 1973. Transfer of products between Auer, M. T., Canale, R. P., and Grundler, H. C. 1982. epiphytic marine algae and host plants. J. Phycol. Ecological studies and mathematical modeling of 9:243-248. Cladophora in Lake Huron: I. Program description Howard-Williams, C., Davies, B. R., and Cross, R. H. M. and field monitoring. J. Great Lakes Res. 8(1):73-83. 1978. The influence of periphyton on the surface Ballantine, D. L. 1979. The distribution ofalgal epiphytes structure of a Potamogeton pectinatus L. leaf (an on macrophyte hosts offshore from La Parguera, hypothesis). A quat. Bot. 5:87-91. Puerto Rico. Bot. Mar. 22:107-111. Hurlbert, S. H. 1971. The nonconcept of species diver Bellis, V. J., and McLarty, D. A. 1967. Ecology of sity: a critique and alternative parameters. Ecology Cladophora glomerata (L.) Klitz. in southern Ontario. 52:749-752. J. Phycol. 3(2):57-63. Hutchinson, G. E. 1967. A Treatise on Limnology. Bornefeld, T. 1979. Ober schleifenartige Strukturen in Volume 2. Introduction to Lake Biology and the der Zellwand von Cladophora. Nova Hedwigia 31(4): Limnoplankton. J. Wiley & Sons, Inc., New York. 969-976. Jansson, A-M. 1967. The food-web of the Cladophora Canale, R. P., and Auer, M. T. 1982a. Ecological studies belt fauna. Helgolonder wiss. Meeresunters. 15: and mathematical modeling on Cladophora in Lake 574-588. Huron: 5. Model development and calibration. J. Mantai, K. E. 1978. The response of Cladophora Great Lakes Res. 8(1):112-125. glomerata to changes in soluble orthophosphate ____, and . 1982b. Ecological studies concentrations in Lake Erie. Verh. Internat. Verein. and mathematical modeling of Cladophora in Lake Limnol. 20:347-351. Huron: 7. Model verification and system response. J. McRoy, C. P., and Goering, J. J. 1975. Nutrient transfer Great Lakes Res. 8(1):134-143. between the seagrass Zostera marina and its epi ____, , and Graham, J. M. 1982. phytes. Nature 248:173-174. Ecological studies and mathematical modeling of Moore, J. W. 1975. The role of algae in the diet of Cladophora in Lake Huron: 6. Seasonal and spatial Asellus aquaticus L. and Gammarus pulex L. J. variation in growth kinetics. J. Great Lakes Res. Anim. Ecol. 44:719-730. 8(1): 126-133. Penhale, P. A., and Thayer, G. W. 1980. Uptake and Cattaneo, A. 1978. The microdistribution of epiphytes transfer of carbon and phosphorus by eelgrass on the leaves of natural and artificial macrophytes. (Zostera marina L.) and its epiphytes. J. Exp. Mar. Br. phycol. J. 13:183-188. Bioi. Ecol. 42: 113-123. ____, and Kalff, J. 1979. Primary production of Phillips, G. L. 1969. Diet of the minnow Chrosomus algae growing on natural and artificial aquatic plants: erythrogaster (Cyprinidae) in a Minnesota stream. A study of interactions between epiphytes and their Am. Midi. Nat. 82:99-109. substrate. Limnol. Oceanogr. 24(6):1031-1037. ____, Eminson, D., and Moss, B. 1978. A mech Draper, N. R., and Smith, H. 1966. Applied Regression anism to account for macrophyte decline in progres Analysis. J. Wiley and Sons, Inc. New York. sively entrophicated freshwaters. Aquat. Bot. Eminson, D., and Phillips, G. 1978. A laboratory experi 4:103-126. ment to examine the effects ofnutrient enrichment on Sand-Jensen, K. 1977. Effect of epiphytes on eelgrass macrophyte and epiphyte growth. Verh. Internat. photosynthesis. Aquat. Bot. 3:55-63. Verein. Limnol. 20:82-87. Scheffe, H. 1959. The Analysis of Variance. John Wiley Fitzgerald, G. P. 1969. Some factors in the competition and Sons, Inc. DIATOMS ON CLADOPHORA IN LAKE HURON 183 Shannon, C. E., and Weaver, W. 1949. The Mathema Storr, J. F., and Sweeney, R. A. 1971. Development of tical Theory of Communication. Univ. Illinois Press, a theoretical seasonal growth response curve of Urbana. Cladophora glomerata to temperature and photo Sicko-Goad, L., Stoermer, E. F., and Ladewski, B. G. period, pp. 119-127./n: Proc. 14th Conf. Great Lakes 1977. A morphometric method for correcting phyto Res., Internal. Assoc. Great Lakes Res. plankton cell volume estimates. Protoplasma 93: Taft, C. E., and Kishler, W. J. 1973. Cladophora as 147-163. related to pollution and eutrophication in western Soszka, G. J. 1975. The invertebrates on submerged Lake Erie. Water Resources Center, The Ohio State macrophytes in three Masurian lakes. Ekol. pol University. Published in cooperation with the Center 23(3):371-391. for Lake Erie Area Research.