July 1964 LIMNOLOGY VOLUME AND NUMBER OCEANOGRAPHY EVIDENCE FOR THE EUTROPHICATION OF LAKE PHYTOPLANKTON RECORDS ERIE IX 3 FROM Charles C. Davis Department of Biology, Western Reserve University, Cleveland, Ohio ABSTRACI’ The Division Avenue Filtration Plant of the Cleveland Division of Water and Heat has undertaken almost daily phytoplankton counts of water samples from Lake Erie since 1919. Data exist for 25 full years and for 7 additional partial years between 1919 and 1963. There has been a consistent increase in the average quantity of phytoplankton. The vernal and autumnal phytoplankton maxima have consistently become more intense and have lasted longer. The periods of minimum phytoplankton development in winter and summer have become shorter and less well marked, until the winter minimum failed to develop at all in some of the latest years. Certain marked qualitative changes also have occurred. These effects are thought to have been caused by an increasingly rapid eutrophication of the water in Lake Erie. INTRODUCTIOK in the lower Great Lakes, particularly in Most limnologists agree that many lakes Lake Erie and to a lesser degree in lower Lake Michigan. Lake Erie lies in a highly evolve slowly from oligotrophy toward industrialized and heavily populated area. eutrophy and that one of the important effects of domestic wastes, whether un- Striking changes of the bottom fauna of treated or fully treated in disposal plants, western Lake Erie have occurred; these is to speed up enormously the process of came to the attention of biologists espeeutrophication through the addition of cially in 1953 (Britt 1955a), when a stratification of water in the western basin relarge quantities of plant nutrient minerals. Such man-made eutrophication has been sulted in the destruction of the major porreviewed by Hasler ( 1947) ; since his re- tion of the theretofore heavy population of view, much additional evidence has accu- nymphal Hexagenia ( Canadian soldiers ) . partial recovery (Britt mulated from various locations (for exam- A subsequent 195%) proved to be temporary ( Britt ple, see Edmondson, Anderson, and Peter1963; Carr and Hiltunen 1963)) and at son 1956 and Edmondson 1961 for condipresent the original benthic community tions in Lake Washington). dominated by Hexagenia has been reUntil recent years, the lakes that were known to have become eutrophic because placed almost entirely by one dominated and oligochaetes. Simiof domestic drainage were relatively small, by chironomids larly, there have been striking changes in and it was widely held that the vast diluthe fish populations of the lake. These tion factor characteristic of the world’s and other evidences of a rapid eutrophicalargest lakes would prevent any clear indication of eutrophication in them. Re- tion of Lake Erie have been reviewed and discussed by Beeton ( 1961, 1964). cently, however, concern has arisen that In his 1961 paper, Beeton was unable to rapid eutrophication may be taking place 275 276 CHARLES point to any evidence of changes in the plankton associated with eutrophication; since then, however, additional information has been forthcoming. An apparent increase of abundance of the copepod Diaptomus siciloides ( characteristically an inhabitant of shallow, eutrophic waters ) has been discussed by Davis (lQ62, 1964) and by Bradshaw ( 1964). In addition, Bradshaw has reported, from Chandler’s ( 1940) 1938-39 western basin data and from his own information collected in 1948-49 and 1959, that there was a considerable increase in the total numbers of Cladocera and Copepoda. To date, however, the only evidence suggesting that phytoplankton changes associated with eutrophication have occurred is that reported by Verduin ( 1964)) who stated that in western Lake Erie the dominant phytoplankters before 1950 had been Asterionellu formosa, Tabelluria f enestrata, and Melosira ambiguu, whereas by 196O61 the dominants were Fragilaria capucina, Coscinodiscus radiutus, and Melosira binderanu. Verduin associated this change with increased fertility, caused principally by an increased runoff of commercial fertilizers from farms in northwestern Ohio. METHODS The Division Avenue Filtration Plant of the Cleveland Division of Water and Heat has undertaken regular quantitative analyses of planktonic microorganisms (mostly phytoplankters) since 1919, usually for at least 5 days a week, 52 weeks a year. Their samples have been obtained from the raw Lake Erie water coming directly through a conduit from an intake crib 5.9 km from shore and 13 m beneath the lake surface. Through the courtesy of Plant Superintendent Roy L. Simpson, the data still in his files have been made available. Permission to use the information has been granted by Commissioner Thomas E. Stanton of the Cleveland Division of Water and Heat. My sincere thanks are given for the cooperation of these two men. Thanks are also extended to Mr. John Wolk for compiling some of the data used in Table 1. C. DAVIS Data exist for 25 full years and for 7 additional partial years, from 1919 through 1963. AS far as can be ascertained, the methods of concentration and examination have remained comparable throughout the period, consisting of the sand-filtration method ( Whipple, Fair, and Whipple 1927), followed by examination of an aliquot in a Sedgwick-Rafter cell. Results have been expressed as phytoplankton cells per milliliter of lake water. The examinations of the samples were undertaken to predict clogging rates in the sand filters used at the filtration plant. Both living and dead cells were counted, without distinction, but other studies (Davis 1955) have indicated that the fraction of dead cells at this distance from the shore of Lake Erie is relatively small for most species. Because the same person could not have made all of the counts over a period of 44 years, there have probably been variations in technique; the records suggest that at times the samples were concentrated by persons other than the enumerator. Some of the estimations of phytoplankton cell numbers ( particularly the low values shown for- the years 1928 and 1929) may have come about through On the other variations in techniques. hand, as will be shown, major changes over the years have occurred gradually, though with the expected up-and-down fluctuations. It does not seem likely that changes of technique would occur gradually and consistently in one direction over so many years. In spite of inevitable questions concerning their accuracy, it appears worthwhile to present some of the available data and to make certain gcneralizations concerning them. Probably none of the analysts who made the counts was a specialist in the taxonomy of the phytoplankters involved. Some obvious taxonomic errors have been made, as when ( occasionally) large numbers of cells have been identified as Protococcus, a nonplanktonic genus that may be either terrestrial or attached to damp or submerged objects. In this instance, it would bc: unwise to conjecture as to the identity EUTROPIIICA’ITON of the organism in question (Ch2or&? Anacystis? Chlamydomonas?). Probably Melmira and Mougeotia (and perhaps also Ulothrix) were at times confused. In any case, Mougeotia has tended in many instances in the present records to increase and decrease in proportion to the changes of the numbers of Melorira; also, other more detailed studies of Lake Erie phytoplankton ( Davis 1954, 1962; Chandler 1940, 1942, 1944; Chandler and Weeks 1945; Burkholder 1960) have never reported Mougeotiu to be common. Aside from Melosira, however, the phytoplankton genera that have usually been reported as the predominant forms are distinct enough even at low magnifications that they probably have not been confused. OF LAKE 277 ERIE YEARS FIG. 1. Avcragc phytoplankton cells per millilitcr for all years with complete records, 1920 to 1963 (2 weeks of records are lacking for 1960 near the height of the autumnal phytoplankton maximum), RESULTS In the records for 13 years between 1919 and 1934, single counts exceeding 4,000 cells/ml occurred only in 2 years (4,072 cells/ml in November 1930 and 4,108/m1 in November 1932). After 1934, on the other hand, counts of more than 4,000 cells/ml occurred in all of the 19 years for which records are available except 1937. Between 1934 and 1963, there was an irregular but persistent increase of records higher than 4,000 cells/ml until the grcatest incidences were reached in 1961 (40 instances) and 1962 (42 instances). The absolute maxima attained in single counts fluctuated considerably but increased fairly regularly until 1944; thereafter no clear trend is shown in the records. Absolute maxima, however, are not thought to be so significant as the number of high records per year or the averages to be discussed below. Maxima ranged from a low of 421 cells/ml in 1928 to a high of 11,032 cells/ml in 1944. In contrast, in oligotrophic Lake Baikal, the largest standing crop of phytoplankters ever reported was 415 cells/ml ( Koxhov 1963). Fig. 1 shows the average phytoplankton numbers per milliliter for each year for which records are available for the entire year (2 weeks of records are lacking for 1960 at or near the peak of the fall phyto- plankton maximum; had they been available, the average for that year might have been somewhat higher). There were notabl e quantitative differences in Lake Erie from year to year; this is a regular feature of the phytoplankton in any lake, probably associated with varying meteorological and cnvironmcntal factors. Nevertheless, it is clear that there has been a steady increase in the average numbers since 1927. The increase has been so steady and consistent that it is obviously not associated with changes of counting techniques. If WC accept the low values obtained for 1928 and 1929, the average number of cells varied from 81/ml in 1929 to 2,423/m1 in 1962, an increase of nearly 30 times. The mean of the values for the first 13 complete years (between 1920 and 1937) was 410 cells/ml, whereas the mean for the last 12 full years (between 1944 and 1963) was 1,254 cells/ml. This was an increase of slightly more than 3 times. Yearlong phytoplankton studies in Lake Eric, such as those by Chandler (1940, 1942, 1944)) Chandler and Weeks ( 1945)) and Davis ( 1954, 1962)) have consistently suggested that there are phytoplankton maxima in the spring and the fall, separated by minima in winter and summer, a classical pattern that occurs in a number 278 CIIARLES of the larger temperate lakes, but not nccessarily in smaller lakes ( Pennak 1946). The present records indicate that such a typical pattern occurred in a number of the earlier years (for example, see Fig, 2 for 1927)) and that, with considerable variations, the pattern continued throughout most of the records. The maxima became more marked and longer over the years, whcrcas the minima became shorter and less marked (Figs. 2-6). Although developing clearly in all other years, at least for short periods, the winter minimum failed to materialize at all in 1955-56, 1961-62, and 1962-63, and it was only poorly shown in 1959-60. The summer minimum also tended to bc obscured in later years but was always evident, except in some years when there appeared to bc no great increase in fall as compared with summer ( for example, 1963). The records of the Division Avenue Filtration Plant have been utilized twice prcviously in publications dealing with the phytoplankton of Lake Erie. Inasmuch as both references deal with periods for which records are not now available, they are referred to briefly here. Chandler (1944) examined the records for 1941, finding the vernal pulse to last from midMarch to late April and the fall maximum to continue from mid-August to late December. Davis ( 1954) utilized the records only to examine the termination of the phytoplankton maximum in early June 1951 and to check a small maximum that occurred during January of the same year. It is of interest to compare the present results for 1956-57 briefly with results for the same year published previously in an independent study by Davis ( 1962), inas- +. ‘F’M’A C. DAVIS 1935 3. The dance for 1935. record of phytoplankton abun- FIG. 4. The dance for 1946. record of phytoplankton abun- FIG. 5. The dance for 1957. record of phytoplankton abun- FIG. 640C , 6000 1946 M’J’J I 9 2J7 FIG. 2. The record oE phytoplankton abundance for the year 1927. Typical vernal and autumnal maxima arc dcpictcd, separated by winter and summer minima. ETJTROPIIICATION much as one of Davis’ stations lay only about 1 km east of the intake crib used by the Division Avenue Filtration Plant. Davis visited his stations only every 2 weeks, and hence more detail is shown by the present records. Nevertheless, the data dates correspond fairly for particular closely, and differences can be accounted for on the basis of varying collection and counting techniques and a possible patchiDavis was ness of the phytoplankton. unable to visit his stations between midDecember and mid-March. Because his results for mid-March were higher than any others obtained during the entire year, he concluded that he had returned at approximately the peak of the spring maxi@mm. This judgment was incorrect, as indicated by the present records, which show a somewhat obscure winter minimum in December-January, followed by an extensive pulse in February and early March that is much higher than any value reported as late as mid-March (Fig. 5). The most abundant genera were ascertained for each month of each of the years. Thcsc estimates of dominance are based both on the cell counts reported in the records and on an approximate knowledge of relative sizes of cells. They are therefore somewhat subjective. As shown in Table 1, there has been a striking change in the most abundant forms. In the spring pulse (including January and February pulses that occurred during the later years), Asterionella dominated in all of the records up to 1931; in 1932, dominance by Asteriondu was shared part of the time by Synedra. In 1932, dominance was shared by Asterioneh and Melosira. Between 1933 and 1949, Atier~onetla was dominant every year except 1937 (when Melosira and Synedra were of greater importance), but the dominance was shared by Melosirn in 1946 and 1947, and by Cyclotella in 1948. In the records from 1956 to 1963, Asteriondu never dominated the spring pulse, although at times it was common. Instead, Mekwira was dominant during this period every year except 1960 (when its importance was shared by Frag- OF LAKE 279 ERIE 7600’ 6000- ” ‘F’M’A’M’J’J’A’S’O’N’DI Id2 FIG. 6. The dance for 1962. record of phytoplankton abun- ilaria and Tab&ha). In 1958, Fragiluria and Melosira dominated the spring pulse. In carlier years, the autumn maximum (and the large early winter populations, when present), were dominated by Syne&n ( from 1920 to 1923). From 1927 to 1948, Melosiru always dominated, either as the major or as one of the principal forms ( during 1927 and 1928 Synedru remained important as a codominant with Melosira; in 1929, Asterionella was codominant ) . Similarly, dominance was shared by Melosira and Synedrn in 1937, 1945, and 1946.. In 1947, the green alga Pediustrum was a codominant with Melosira; similarly, Asterionella and Melosira were codominants in 1948. After 1948, Lh?eZosirawas among the dominants in some years, but there was a tendency away from this, so that Fragilaria, Peckstrum, Anabaena, and others became more important. Hence, the main tendency in the spring pulses has been a shift from dominance by Asterionella to dominance by Melosira. A corresponding shift in the autumnal pulses: has been from Syneclra to Melosira, and then from Melosira to Fragilariu. In addition, as shown in Table 1, during autumnal pulses there has been a greater tendency during later years (1947, 1949, 1957, 1958,. 1961, 1962) for an increased participation: 280 CHARLES ‘~ABLIS 1. Dominant Spring DAVIS phytoplankters during spring and autumn phytoplankton (The dash signifies that there was no pulse) pulse Year Astcrionella Asterionclla Asterionella -Synedra, Asterionella Aaterionella, Melosira Asterionella Aslerionella Asterionella Metosira, Synedra Asterionella Asterionella Asterionella Asterionella, Melosira Melosira, Asterionella Asterionella, Cyclotella Asterionella 2 M elosira LMelosira Fragilaria, Melosira Melosira Fragilaria, Tahellaria Melosira Melosira M elosira * Some T From C. of the included information Chandler’s (1944) report Autumn 1920 1921 1922 1923 1927 1928 1929 1930 1931 1932 1933 1934 1935 1936 1937 1941t 1944 1945 1946 1947 1948 1949 1955 1956 1957 1958 1959 1960 1961 1962 1963 of has the pulse Synedra Synedra Synedra Synedra Melosira, Synedra Synedra, Melosira, Stephanodiscus Asterionella, Melosira M elosira M elosira M elosira Melosira M elosira M elosira Melosira Synedra, Melosira M elosira M elosira Synedra, Melosira hlelosira, Synedra Melosira, Pediastrum Melosi.ra, Asterionella Synedra, Pediastrum Nlelosira Synedra, Melosira Pediastrum, Fragilaria Fragilaria, Melosira, Anabaena Fragilaria M elosira Fragilaria, Melosira, Anabaena Melosira, Anabaena, Oscillatoria Fragilaria, Synedra, Stephanodticus been adapted from an Filtration Plant records on the part of the green and blue-green algae, replacing in part the previous ,dominance by diatoms. There has been a similar change of dominance during the winter phytoplankton minimum, for Stephanodiscus and CycloteZ& were of greatest importance in most years until 1944, whereas Melosira, Fmgila&z, and Asterionellu were most abundant from 1945 to 1949. Since 1956, during a period when little or no winter minimum developed, hlelosiru and Frngilnria continued as the most frequent dominants, so probably the phytoplankton from 1945 to 1949 can be considered as indicating transitional features in the lake, leading to the elimination of winter minima. I)ominance during summer minima, however, showed little indication of a con- pulses, 1920-63” undergraduate for 1941. project written by Mr. John Wolk. sistent change, except for an increased frequency of the chlorophyte Pediustrum and the cyanophyte Anabaena Shifts of dominant species of phytoplankton comparable (though not identical) to these often have been interpreted in other lakes as indications of rapid eutrophica tion ( Hasler 1947 ) . DISCUSSJON The earliest year-round studies of Lake Erie plankton appear to have been those of Vorce ( 1880u,b, 1881, 1882). He gathered his samples from the Cleveland water supply “by tying a muslin bag over the house supply faucet . . . until the pores . . . were clogged with the arrested organisms . . .” (1881, p. 52). Although such a method could give no quantitative EUTROPIIICA’1’ION picture, he reported that from February to May the phytoplankton was dominated by Stephanodiscus and Rhixosolenia, and that Melosira and Tabellaria were the most abundant from May to November, Rhixosole&a eriensis is a small and transparent diatom and was not listed in any of the records under consideration here. There appears, however, to be considerable significance in its apparent abundance in 1880 (Vorce 1881)) and in the fact that subsequent careful observations have indicated it to be less and less common over the years. Thus, Burkholder ( 1960) found it to be occasionally abundant in the central basin in 1929, as did Chandler (1940, 1942, 1944) and Chandler and Weeks t-45) in the western basin in 1939-42. Davis (1954) listed it as a relatively rare winter form in 1950-51, and he did not find it at all in 1956-57 ( Davis 1962 ) . Furthermore, the genus is important in some of the other, more oligotrophic Great Lakes (Putnam and Olson 1961 for Lake Superior; Daily 1938 for Lake Michigan). It is unsafe to draw rigid conclusions regarding other diffcrenccs between the observations reported by Vorce and more recent reports, but it should perhaps be mentioned that there are no recent reports either of Stephanodiscus as a dominating member of the spring pulse or of TabelZaria as a dominant in the summer and fall; the present results similarly support the conclusion that a change has occurred, for these diatom genera have never been dominant in spring or fall. However, we need more reports between 1880 and 1929 before definite conclusions can bc drawn. Burkholder’s publication ( 1960) on the phytoplankton of the central basin in 1929 covers only June to September. Although his study was quantitative, the exact quantities are difficult to ascertain. Thcrc was an autumnal phytoplankton pulse in Scptember, with dominance by AsterioneZZa, Fmgilaria, and Melosira. At the station nearest Cleveland, about 100 phytoplankters/ml are indicated ( Burkholder does not state whether his units are cells or colonies). In the present results, the only OF LAKE ERIE 281 real pulse in 1929 occurred in September, with a maximum of around 600 cells/ml, dominated by AsterioneZZa and Melosira. Hence, the two studies agree rather closely. Metcalf ( 1942) examined the plankton near Cleveland in the summer of 1938 (mainly in August and September, with some results from June), but his methods were nonquantitative. No real pulses were indicated among the few phytoplankters he reported ( Asterionella, Anabaena, Ceratium, and Dinobryon.) . As mentioned, Chandler (1944) briefly described the now missing records for 1941 from the Division Avenue Filtration Plant for the purpose of general comparison with his own more detailed results from the western basin. Dominants listed by Chandler are given in Table 1. The only other studies from the Cleveland area are those of Davis ( 1954, 1962) for 1950-51 and 1956-57, rcspectivcly. The 1950-51 records of the filtration plant are at present lacking, so that no comparisons can be made. The year was characterized by distinct vernal and autumnal maxima, dominated in the autumn of 1950 by Melosira spp., Fragilaria crotonensis, and Pediastrum simplex, in the spring of 1951 by CycZofeZZa and Melosira, and in the autumn of 1951 by Melosira spp., Pediastrum simplex, and Fragilaria crotonensk These results fit reasonably well into the pattern shown for the preceding and following years. In the 1956-57 study, the autumnal phytoplankton of 1956 was dominated by Microcystis spp., and the early winter plankton was characterized by an abundance of Stephanodiscus niagarae. Melosira spp. were most important during the main portion of the vernal pulse of 1957, and unidentified phytoflagellates dominated the summer minimum. The late summer and autumnal phytoplankton communities were dominated by a succession of green algae, first Pediastrum duplex, then OBcystis spp. and Coelustrum sp., and finally Pediastrum simplex. It must be emphasized that Davis’ methods of collec- 282 Cm4RLES C. DAVIS tion and preservation differed greatly from those used at the filtration plant and that he reported his results as volumes of the phytoplankters per liter of lake water rather than as cells per milliliter. Consequently, close comparisons are not feasible. The differing methods undoubtedly contribute to the discrepancies between his results for 1956-57 and those reported for the same period from the filtration plant. In addition, taxonomic differences also are apparent, for example, in the lack of recognition of the genera Microcystis and O&y&is in the records of the filtration plant during 195&57, whereas Davis found the genus Microcystis to be dominant in September 1956 and Oiicystis to be the most important genus in August 1957. The results surveyed in the present paper show that 1) the phytoplankton has consistently increased in quantity between 1920 and 1963, 2) the intensity and length of the maxima have increased, 3) the minima have become shorter and less pronounced, and 4) the winter minimum has failed to materialize in some of the later definite qualitative years. Furthermore, changes have occurred. All of these results appear to indicate an increased and rapid eutrophication of the waters of Lake Erie, as has been suggested by studies of the bottom fauna, ichthyofauna, and water chemistry as summarized by Beeton (1961, 1964). REFERENCES 1961. Environmental changes BEETON, A. M. Trans. Am. Fishcrics Sot., in Lake Erie. 90: 153-159. 1964. The eutrophication of the Great -. Lakes. ( Unpublished manuscript. > The crustacean zooBHAUSHAW, A. S. 1964. plankton picture : Lake Erie 1939-49-59; Vcrhandl. Intern. Ver. Cayuga 1910-51-61. Limnol., 15: 700-708. BRITT, N. W. 1955a. Stratification in wcstcrn Lake Erie in summer of 1953: effects on Hexageniu (Ephcmeroptcra) population. Ecology, 36 : 239-244. -. ( Ephcmeroptera ) 1955b. E-Iexccg&n recovery in western Lake Eric following the Ecology, 36 : 520-522. I953 catastrophe. Some changes in the bottom -. 1963. f auna of the island area of western Lake Erie in the decade 1953-1963, with special reference to the aquatic insects. ( Abstr. ) Proc. Conf. Great Lakes Res. 6th: 268. BUHKHOLDER, P. R. 1960. A survey of the microplankton of Lake Eric. In. Limnological survey of eastern and central Lake Erie, 1928-192,9. U.S. Fish Wildlife Serv. Spcc. Sci. Rept., Fisheries, 334: 123-144. CAM, J. F., AND J. K. IIILTUNEN. 1963. 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H. 1942. The attraction of fishes by disposal plant effluent in a frcshwater lake. Ohio J. Sci., 42: 191-197. EUTROI’HICA’ITON R. W. 1946. The dynamics of frcshwater plankton populations. Ecol. Monographs, 16: 340-355. PUTNAM, H. D., AND T. A. OLSON. 1961. Studies on the productivity and plankton of Lake Superior. Univ. Minnesota School Public Health. ( Multigraphcd. ) 24 p. VERDUIN, J. 1964. Changes in western Lake Erie during the period 1948-1962. Verhandl. Intern. Ver. Limnol., 15: 639-644. VORCE, c. M. 188Oa. The minute forms of life in the waters of the lakes. Am. J, Microscopy Pop. Sci., 5: 263-265. -. 1880b. Some observations on the mi- PENNAK, OF LAKE ERIX 283 nutc forms of life in the waters of the lakes. A paper read before the Kirtland Society of Natural Sciences of Cleveland, Ohio. J. B. Snvagc, Cleveland, Ohio. P. 3-7. -. Forms observed in water of 1881, Lake Erie. Proc. Am. Sot. Microscopists, 4: 51-90. -. 1882. Microscopic forms observed in water of Lake Eric. Proc. Am. Sot. Microscopists, 5: 187-196. \VHIPPLE, G. c., G. M. FAIR, AND M. c. WHIPThe microscopy of drinking PLE. 1927. water. 4th ed., 5th printing ( 1948). Wiley, New York. 585 p.
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