On the use of carotenoid stratigraphy in lake sediments for detecting past developments of phytoplankton
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1 970 Notes hypothesis and the forms of the visibility parent size as the determinant of prey selection hypothesis for nonopaque cladocerans. by bluegill sunfish (Lepomis macrochiras). Ecology 57: Robert E. &ret1 WARE, D. M Risk of epibenthic prey to predation by rainbow trout (Salmo gairdneri). J. Department of Zoology Fish. Res. Bd. Can. 30: Duke University ZARET, R. E., AND W. C. KERFOOT The Durham, North Carolina shape and swimming technique of Bosmina longirostris. Limnol. Oceanogr. 25: X References ZARET, T. M. The effect of prey motion on planktivore choice. Am. Sot. Limnol. Oceanogr. O'BFUEN, W. J The predator-prey interaction Spec. Symp. 3: of planktivorous fish and zooplankton. Am. Sci. -, AND W. C. KERFOOT Fish predation 67: on Bosmina longirostris: Body size selection -> N. A. SLADE, AND G. VINYARD Apversus visibility selection. Ecology 56: Present address: Dept. Zool., Univ. Rhode Island, Kingston Submitted: 29 July 1980 Accepted: 5 March 1981 Limnol. Oceanogr., 26(5), 1981, by the American Society of Limnology and Oceanography, Inc. On the use of carotenoid stratigraphy in lake sediments for detecting past developments of phytoplankton Abstract-A method is described on onedimensional chromatography with four sequential development steps for the separation of carotenoids in plankton and in lake sediments. Quantitative measurements of various carotenoids in cores of sediments from Swiss lakes allow the composition and development of the phytoplankton over the past years to be worked out and also show the changing trophic condition of the lakes. An example from Lake Zurich shows how the change from oligotrophy to eutrophy, as documented by limnological studies, is reflected in the composition and changing concentration of specific carotenoids. Investigation of the trophic ontogeny of a lake, as manifested in the development of its phytoplankton, can be of great practical importance, because it can provide information about the trophic level and rate of eutrophication before the beginning of any cultural influences, as well as the effects of the latter and prognosis concerning eventual attempts at restoration (e.g. Ziillig 1956; Gorham and Sanger 1976). Stratigraphic investigations of carotenoids in cores of sediments by Ziillig (1961), Griffiths et al. (1969), Griffiths (1978), and Watts et al. (1977) have demonstrated that plankton developments can be detected from the occurrence of characteristic carotenoids in the sediments. Not only do carotenoids preserve well in sediments, but Watts and Maxwell (1977) have detected reduction of double bonds in zeaxanthin and canthaxanthin only in sediments older than 56,000 years, demonstrating the stability of these compounds over long periods. Through the measurement of the concentration of certain carotenoids in cores of sediments and their accumulation rates over time, I have attempted to trace the development of the phytoplankton over the last years in several Swiss lakes that have become eutrophic. As an example of the 10 lakes investigated so far, the results from Lake Zurich are presented and discussed briefly. All these lakes will be treated in greater detail elsewhere. From the recent literature (e.g. Hertzberg et al. 1971: Cyanophyceae; Hager and Stransky 1970: Chlorophyceae; Johansen et al. 1974: Dinophyceae) and my own complementary investigations on
2 Table 1. Various taxa of algae and their characteristic carotenoids. Notes 971 Taxa Characteristic carotenoids Cyanophyta Species of blue-green algae with specific carotenoids: Oscillatoria rubescens Oscillatoria limosa Coelosphaerium Kiitz. Anabaena Anabaena $os-aquae planctonica Chlorophyta (and higher plants) Cryptophyta Chrysophyta Bacillariophyceae Chrysophyceae Pyrrophyta Dinophyceae Euglenophyta I Myxoxanthophyll, echinenone, canthaxanthin Oscillaxanthin Myxol-2 -o-methyl-methylpentoside 4-keto-myxol-2 -methylpentoside Lutein Alloxanthin Fucoxanthin Peridinin Diadinoxanthin (mainly, but not characteristic) phytoplankton, I have selected the principal pigments characteristic of various taxonomic groups of algae, which should enable these groups to be identified from their carotenoids deposited in sediments in past times (Table 1). In selecting these pigments, I took account of the xanthophyll cycle induced by light (Hager and Stransky 197O), which involves reciprocal changes in the violaxanthin, antheraxanthin, and zeaxanthin of the Chlorophyceae, and in the diadinoxanthin and diatoxanthin among the Xanthophyceae, Euglenaceae, and Bacillariophyceae. No quantitative significance can be ascribed to those carotenoids that undergo such reciprocal transformation. I thank C. Eugster and R. Buchecker for valuable advice, S. Liaaen- Jensen, H. Kjosen, F. Leuenberger, and P. Schudel for furnishing certain test preparations, and D. G. Frey for help with the English translation. Cores of sediments up to 1 m long and about 34 mm in diameter were collected with a gravity corer (Ztillig 1953; modified in 1977), containing a Plexiglas tube provided with a sealed, removable cover. The core was prepared while in the collection tube by removing the cover and cutting it in half longitudinally with a 0.5 mm-thick Plexiglas plate. To prevent disturbance and loss of the often very fluid sediments at the surface, I positioned a tightly fitting piston at the surface of the sediments while the sampling tube was still in a vertical position. Sometimes the surficial sediments and the overlying several centimeters of water were immobilized by the addition of liquid agar before removal of samples. Short segments of sediments, consisting of only one or several annual laminae, were separated from one another in the core by inserting thin, circular Plexiglas plates (Fig. 1). Before extraction of pigments, the wet samples were weighed and after extraction the filter residues were dried at 80 C and reweighed, enabling calculation of water content, the dry weight factor, and dry weight. I avoided the customary drying temperature of 100 C because this is the approximate temperature at which clay minerals start to dewater (Iberg 1954) and organic compounds to volatilize. Pigments were extracted from either freshly procured samples of sediments or deep-frozen pure cultures of algae in 15 ml of a 1: 1 mixture of acetone and ethanol for 5-6 h in the dark and in an atmosphere of nitrogen. On the basis of measurements made at
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4 Notes 973 Table 3. Approximate Rf values of carotenoids. Carotenoid Carotene Echinenone 0.81 Canthaxanthin 0.65 Rhodoxanthin* 0.54 Astaxanthin 0.48 Lutein 0.46 Zeaxanthin (+diadinoxanthin) 0.42 Alloxanthin 0.40 Fucoxanthin 0.37 Violaxanthin 0.35 Peridinin 0.33 Neoxanthin 0.28 Fucoxanthin degradation product 1 (trace) 0.25 Myxol-2 -o-methyl-methylpentoside 0.24 Fucoxanthin degradation product keto-myxol-2 -methylpentoside 0.14 Myxoxanthophyll 2t 0.10 Myxoxanthophyll 1 or aphanizophyllt Oscillaxanthin 0.03 * Rhodoxanthin was observed in TLC of sediment extractions when the sediment probes contained FeS. Rhodoxanthin was not quantitatively determined. t Myxoxanthophyll 1 and 2 give the same absorbance values in visible light area after acetylation. Myxoxanthophyll was obtained from extracts of Oscillatoria rubescens and Aphanizomenon jlosaquae. era1 minutes with nitrogen, 100 ml of developer were added, and after about 30 min the plate was inserted with the layered side 4 cm from the blotting paper. Development proceeds in the dark. Immediately after development the pigments that had migrated were scraped off in dim light, and the pigments still remaining on the plate were scraped off with a glass plate, then eluted with ethanol. Approximate R, values were determined (Table 3) and from Eq. 2 the quantities of the individual carotenoids were calculated. If the procedure specified is followed exactly, it is possible to recover and measure about 90% of the pigments present, Carotenoids E;lOV (2) (mg) = E IV0 I cm where E, is optical density in l-cm layer measured at x nm, V is volume (ml), and Elvo 1 cm is extinction coefficient for carotenoid X (oscillaxanthin Elyo 1 cm = 1,450 : Griffiths 1978; myxol-2 -o-methylmethylpentoside E l% 1 cm = 2,200 approx calculated; 4-keto-myxol-2 -methyl- Rf pentoside E l% 1 cm = 2,200 approx calculated; others according to Davies 1976). The results can be expressed as percentages of dry weight, but because of the variable concentrations in the sediments of clay, carbonates, and other admixed materials, such percentages give a false idea of the annual contributions of carotenoids. Accordingly, I have used the annual accumulation rate of the individual carotenoids, calculated according to the following equations, to compare different lakes and different times. Specific annual quantity of sediment = SAQS: SAQS = h-1 cm2-df-s~1,000 mg (3) where h is thickness of the annual layer of sediment (cm), D, is dry weight factor, and s is specific weight (conveniently taken as 2.8). Specific annual accumulation of carotenoid X = SAAC: SAAC = % carotenoid X * SAQS * mg 100 (4) Some Swiss lakes, especially Lake Ziirich, show clear annual laminae, from which h can be measured for every year (see discussion of Lake Ztirich below). In the absence of annual laminae, the rate of sedimentation was determined by radioisotopic methods on the basis of 137Cs distribution. In addition to measurements of carotenoids, the frustules of centric and pennate diatoms were counted. A portion of the filter residue from the pigment extraction was suspended in water and then boiled in hydrochloric acid and hydrogen peroxide. Diatoms form a large part of the plankton of most of the Swiss lakes; their quantitative relationships, therefore, can be regarded as an indication of the level of eutrophication. The counts reflect previous developments of diatoms and can be used to corroborate the development of the phytoplankton as indicated by the carotenoids. The developmental history of Lake Ziirich over the past 80 years, which encompasses its transformation from oligotrophy to eutrophy, is documented by many chemical and biological investigations, such as those of Minder (1943), Marki
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6 Notes 975 ning of winter. Through the accumulation of organic materials from dead and sedimented plankton, the oxygen on the bottom of the lake is completely consumed, hydrogen sulfide is formed, and this leads to the precipitation of black iron sulfide. During spring and summer a light-colored layer of allochthonous clay is deposited on the black layer of the previous year. The sediments deposited before 1890 are predominantly light colored, interrupted irregularly by thin black layers containing washed-in plant remains. Schriiter (1897) reported scattered blooms of blue-green algae and sparse concentrations of other phytoplankters. Oscillatoria rubescens, which in later years became very abundant, was absent. Except for oscillaxanthin, all pigments that later became abundant in the sediments were already present in trace quantities in these presettlement sediments. The first sign of eutrophication occurred in 1896, when the diatom Tabel- Zaria fenestrata became very abundant in the plankton, and massive quantities of its frustules were deposited in the layer of sediment deriving from that year. Parallel to this, the appropriate carotenoids fucoxanthin and diadinoxanthin (+zeaxanthin) occur in the 1896 layer in substantial quantities (Fig. 2). In 1899 a massive development of 0. rubescens displaced the diatoms and resulted in the highest annual accumulation rates of oscillaxanthin and myxoxanthophyll in the sediments. Later there was a wavelike development of the plankton, clearly dominated by diatoms and 0. rubescens. The crude carotenoids show that after the first maximum toward the end of the last century there was a second in , which continued up to 1945, and a third one around During this period the oxygen content in summer at a depth of about 100 m was always less than the value measured in 1910 (Minder 1943; Thomas 1971). Up to the end of the 19th century, Lake Zurich was little affected by cultural influences, but thereafter the dense development of the near-lake re- gion for residences and industry changed the condition of the lake from oligotrophy to eutrophy in three pulses; we do not have a clear explanation as to the specific factors controlling these. Oscillatoria and its associated oscillaxanthin in the sediments had a last maximum about 1960; since 1970 oscillaxanthin has declined to the limit of detection. Other pigments, however, are still present-myxoxanthophyll, echinenone, can- thaxanthin, 4-keto-myxol-2 -methylpentoside, lutein, fucoxanthin, and peridinin -indicating that other blue-green algae are still present along with green algae, dinoflagellates, and diatoms, although there has been an overall progressive decline in algal production. This behavior of the carotenoids is the consequence of an oligotrophication, described by Thomas (1971). The mechanical-biological treatment of sewage and the concurrent elimination of phos- phate inputs from most of the watershed of Lake Ziirich has produced effects detectable in general limnological studies. After an extreme hypolimnetic oxygen minimum in 1945, very low levels of dissolved oxygen were last observed in 1963 and Since 1967 there has been a strong increase in hypolimnetic oxygen (despite the continued formation of annual couplets in the sediments). The transparency has increased, and the phosphate concentration has decreased. In concert with these changes, 0. rubes- tens disappeared from the lake, although it reappeared in A comparable disappearance of oscillaxanthin from Lake Washington following the diversion of effluents from secondary sewage treatment plants is mentioned by Griffiths and Edmondson (1975). Hans ZiiZZig Brendenweg 9 CH-9424 Rheineck, Switzerland References DAVIES, B. H Carotenoids, p Zn T. W. Goodwin led.], Chemistry and biochemistry of plant pigments, v. 2. Academic. GORHAM, E., AND J. E. SANGER Fossilized pigments as stratigraphic indicators of cultural
7 eutrophication in Shagawa Lake, northeastern Minnesota. Geol. Sot. Am. Bull. 87: GRIFFITHS, M Specific blue-green algal carotenoids in sediments of Esthwaite Water. Limnol. Oceanogr. 23: , AND W. T. EDMONDSON Burial of oscillaxanthin in the sediment of Lake Washington. Limnol. Oceanogr. 20: , P. S. PERROT, AND W. T. EDMONDSON Oscillaxanthin in the sediments of Lake Washington. Limnol. Oceanogr. 14: HAGER, A., AND H. STRANSKY Das Carotinoidmuster und die Verbreitung des lichtinduzierten Xanthophyll-Cyclus in verschiedenen Algenklassen, III Griinanlagen. Arch. Mikrobiol. 72: HERTZBERG,S.,S.LIAAEN-JENSEN,AND H. W. SIE- GELMANN The carotenoids of bluegreen algae. Phytochemistry 10: IBERG, R Beitrag zur Kenntnis von Tonmineralien einiger Schweizer Boden. Diss. Eidg. Tech. Hochschule Zurich Prom. No JOHANSEN, J. E., W. A. SVEC, S. LIAAEN-JENSEN, AND F. T. HAXO Carotenoids of the Dinophyceae. Phytochemistry 13: MWRKI, E Unser Ziirichsee ist in der Agonie. Wasser Energiewirtsch. 10: MINDER, L Der Ziirichsee im Lichte der Seetypenlehre. Neujahrsblatt Naturforsch. Gesellsch., Zurich, p. l-83. NIPKOW, F Vorlaufige Mitteilungen iiber Untersuchungen des Schlammabsatzes im Ziirichsee. Schweiz. Z. Hydrol. 1: PAVONI, M Die Bedeutung des Nannoplanktons im Vergleich zum Netzplankton. Schweiz. Z. Hydrol. 25: SCHR~TER, C Die Schwebeflora unserer Seen. Neujahrsblatt Naturforsch. Gesellsch., Zurich, p STAHL, E Diinnschicht-Chromatographic, Ein Laboratoriumshandbuch. Springer. THOMAS, E. A. 1956/57. Der Ziirichsee, sein Wasser und sein Boden. Jahrb. Zurichsee 17: Druck Th. Gut, Stafa/Ziirich Oligotrophierung des Zurichsees. Vierteljahres. Naturforsch. Gesellsch., Zurich 116( 1): , AND E. MARKI Der heutige Zustand des Ziirichsees. Int. Ver. Theor. Angew. Limnol. Verh. 10: WATTS, D. C., AND J. R. MAXWELL Carotenoid diagenesis in a marine sediment. Geochim. Cosmochim. Acta 41: ,-,AND H. KJOSEN The potential of carotenoids as environmental indicators. Adv. Org. Geochem., p Proc. 7th Int. Meeting Org. Geochem. Madrid Pergamon. ZSCHEILE, F. P., J. W. WHITE, JR., B. W. BEADLE, AND J. R. ROACH The preparation and absorption spectra of five pure carotenoid pigments. Plant Physiol. 17: Z~LLIG, H Ein neues Lot zur Untersuchung der obersten Schlammschichten. Schweiz. Z. Hydrol. 15: Sedimente als Ausdruck des Zustandes eines Gewassers. Schweiz. Z. Hydrol. 18: Die Bestimmung von Myxoxanthophyll in Bohrprofilen zum Nachweis vergangener Blaualgenentaltungen. Int. Ver. Theor. Angew. Limnol. Verh. 14: Submitted: 24 February 1980 Accepted: 14 January 1981 Limnol. Oceanogr., 26(5), 1981, A method for preparing permanent mounts of phytoplankton for critical microscopy and cell counting1 Abstract-A method is described for preparing permanent mounts of phytoplankton for critical microscopy and cell counting. Preserved phytoplankton are settled onto cover glasses (or slides), dehydrated by ethanol vapor substitution, and mounted in one of several ethanol-soluble resins. The resulting slides are permanent, quantitative, and of excellent optical quality. Resolution is very good and, with the appropriate resin, contrast is high enough to eliminate the need for phase shift or other contrast enhancement. The inverted microscope - -_ technique of TT u termijhl (1958), which allows quantitar This study was supported by the U.S. DOE (EY- tive analyses of even the most delicate 75-S , COO ) and the National Science Foundation (BMS ). A contribution microplankton, has become the standard of the W. K. Kellogg Biological Station of Michigan by which other techniques are judged. It State University. has, however, a number of shortcomings,
A method for preparing permanent mounts of phytoplankton for critical microscopy and cell counting1
eutrophication in Shagawa Lake, northeastern Minnesota. Geol. Sot. Am. Bull. 87: 1638-1642. GRIFFITHS, M. 1978. Specific blue-green algal carotenoids in sediments of Esthwaite Water. Limnol. Oceanogr.
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