Responses of Diatom and Chrysophyte Assemblages in Lake 227 Sediments to Experimental Eutrophication

Responses of Diatom and Chrysoph n Lake 227 Sediments to Experiment

Barbara A. Zeeb, Catherine E. Christie, and John P. Smol Paieoecoiogical Environmental Assessment and Research Laboratory (PEARL), Department of Bioiogy, Queen'$ Universify,

Kingston, ON K7L 3M6, Carsacla

David L. Findlay and Hedy J. Kling Departn-lena of Fisheries and Oceans, Freslrwater Institute, 507 University Goes., k%'inr~ipeg, MB R 3 P 2N6, Candda

and H.).B. Birks Pnleoecologic.ad %nvirorsrnent,~l Assessment and Research Laboratory (PEARL), Deparfrnena of Biology, Queen's University,

Kingston, ON K76 3N6, Car~ad'? and

Botanicad Institute, Universily of Bergen, Allegaten 4 %, N-.i007, Bergen, Norway

Zeeb, B.A., C.E. Christie, J.P. Smol, D.L. Findlay, H.1. Kling, and H.J.B. Birks. 1994. Responses of diatom and chrysophyte assemblages in Lake 227 sediments to experimental eutrophication. Can. J. Fish. Aquat. Sci. 51 : 2300-231 1.

W e examined the diatom and ckrysspkyte assemblages preserved in bake 227 sediments prior to, during, and following the annua9 additions of phosphorus (PI and nitrogen (N) (from 1969-1 989). Premanipulation (1 957-1 968) diatom and ckrysophyte assemblages were dominated by taxa characteristic of acidic, unproductive lake conditions. In 1969, the assemblages immediately shifted in response to increased nutrient availability and/or increased p H values in the epilinanion. Large increases in the relative abundance of Synedra PIRLA 2 and 5. rumpens var. famijiaris, Ma/Bomonas crassisquama, M. doignonii var. tenuicostis, and cysts 1 , 15, 29, 233, and 120 largely replaced the prefertilization assemblages. From 1970-1998, the diatom assemblage was dominated by dlkaliphilic or pH-indifferent taxa. A second ckrysophyte assemblage shift, which coincided with a lowering of the N:P addition ratio in 4975, was chardeteriaed by decreases in M. crassisquama and cysts 1, 15, 29, 233, and 120, and corresponding increases in Syraura sphsgniculs Korskikov scales and cysts 62 and 33. The stratigraphical analyses and numerical rate-of-change analyses clearly showed that diatom and chrysophyte species composition, particularly ckrysophyte cysts, closely tracked short-term changes in lakewater chemistry. The amount of variance in the stratigraphic assemblages explained by lake-water chemical changes was high (68-9O0/0), indicating the close algae-chemistry relationships in Lake 227 from 1 969-1 989.

Nous avons examin6 des restes de diatornees et de chrysophytes contenus dans Ips sediments du lac 227 avant, pendant et apri3s ['addition annuelle de phosphore (P) et d'azote (N) (de 4 969 i?i 1989). Avant la trans- formation du lac (soit de 1957 2 1968), les assemblages 6taient dorninbs par des taxons caractc2ristiques de conditions lacuskres acides et nor? productives. En 1969, i!s ont imrnediaternent r6pondu .h la plus grande disponibilite d'6lements nutritifs et (ou) 2 la hausse du p H en zone epiliminique : l'abondance rel,~tive de Synedra PI RLA 2, de S. ruinpens var. darrsE8Earis, de Mallomonas crassisquama, de M. do ignsn i i var. tenuicc~sfis a 6t6 accrue, e l les spores 7 , 15, 29, 233 et 128 ont largement remplack les groupes qui 6tdient observbs avant le commencement du traitement. De 1976) h 1990, Ies diatornees etaient dominees par des taxons alcalinophiles oke qui sont indifferents au pH. Un second r6equilibrage des assemblages de chrysophytes, yui a co'incid6 avec I'abaissernent du taux N/P de la charge en 1975, 6t6 caract6ris4 par une diminution de M. crassisquama et des spores 1 , 15, 29, 233 et 120, ainsi que par une hausse cor- respondante de Synura sphagnicola, du groupe de Korshiksv er des spores 6 2 et 33. Les analyses stratigraphiques ainsi que celles du taux de changernent ont clsirement montre que Ica composition specifique en diatomkes et en chrysophytes, notarnrnent les spores de chrysophytes, suivaient de pr&s les changements

courte 6ch6anc-e de la chirnie de I'eau, qui expliqusient 68 2 90 % de la variance des assemblages stratigraphiques observ6s dans le lac 227 entre 1969 et 1989.

Received October 29, 7 993 Accepted ApriB 26, 1994 (962P4P)

Regu le 29 octobre 1993 Accept4 le 24 aafril 1994

ew North American lakes provide the opportunity to logical records. Moreover, the important question of how compare long-term historical records of water chem- closely sedimentary diatom and chryssphyte assemblages istry and phytoplankton populatisns with paleslimno- track lakewater changes, s r whether there are significant

lags in response, has rarely been addressed. 'TGS paper is one of a series done in honor s f the 25th annaiver- Located in the Experimental Lakes Area (ELA), nsrth-

sary of the Experimental Lakes Area. western Ontario, Lake 227 is an ideal Iocation for such a

2300 Can. 9. Fish. Aqun~. Sci., Val. 51. I994

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

study because it was the site of a whole-lake addition of phosphorus (B) and nitrogen (N) that has been monitored for 24 yr. Numerous studies have been completed on this lake documenting the chemical (Flett et al. 1980; Levine et al. 1986; Schindler et al. 1987) and biological changes in the primary producers (Schindler and Holmgren 1971; Schindler et al 1971; Schindler and Fee 19'74; SchindIer 1937; Findlay et al. 1994) and zooplankton populations (Batalas 197 1; Malley et al. 1988). Furthemore, Lake 227 is an excel- lent site for a high-resolution paleolirnnological investigation because the water column is strongly stratified; the lake has an anoxic hypolimnion, and seldom mixes below 9 rn (Schindler et al. 1987). This combination of factors has resulted in annually laminated sediments over the last 400 yr (Wolfe et aH. 1994), which provide chronological control.

The purpose of this investigation was to determine how siliceous algal (diatoms and chrysophytes) assemblages preserved in a lake sediment core (representing the period ca. 1957-8 990) tracked limnologlcal changes resulting from the fertilization sf a whole-lake system, and to compare these assemblages with the long-term phytoplankton history and water chemistry that have been recorded for Lake 227 since 1969.

Materials and Methods

A short freeze core was retrieved from the deepest portion of Lake 227 in January 1990 (Leavitt and Findlay 1994). The outermost 5 mm of sediment was removed from the core and the remaining sediment was freeze dried for 24 h (Leavitt et al. 1989). Laminae corresponding to deposition in one year were separated manually (1945-1998) at -8°C within 3 h of freeze-drying the sediments (Leavitt and Findlay 1994). The sediments were subsampled for the analysis of various chemical and biological indicators.

Sediment samples were prepared according to standard techniques (Smol 1983). Briefly, the freeze-dried sediment was digested in polyethylene centrifuge tubes with a mixture of potassium dichrsmate and sulphaaric acid (1 g K,Cr,O, in 20 mL H,SO,). After several days, the material was boiled to complete the digestion and then rinsed eight times with ddas- tilled water. Light microscope (LM) slides were prepared by resuspending the cleaned siliceous material and evapo- rating it onto glass coverslips at 25°C. The dried coverslips were then permanently mounted in Hyrax0 on glass slides. The same slides were counted for each of the three microfossil groups investigated (diatoms, chrysophyte scales, and chrysophyte cysts).

Scanning electron microscopy (SEM) was used to develop a working cyst taxonomy for Lake 227. The same sediment slurries used for LM were evaporated onto a smooth piece of aluminum foil, which was affixed to aluminum SEM stubs. Each sample was then sputter-coated with gold and examined at 2QkV (working distance = 15 mm).

Diatom and chrysophyte remains were enumerated at l00OX with bright-field and Nomarski optics, respectively. In all cases, micrographs were taken, At least 580 diatom valves and 500 chryssphyte scales were counted along par- allel transects; a minimum of 300 chrysophyte cysts were similarly counted.

Diatom taxonomy generally followed Hustedt (1 928 -1966, 1930). Cleve-Euler (195 B -1955), Patrick and Reimer (1966, 1975), Koppen (1975), Nicholls and Camey (1979), Cmburn

et al. (1984-1 98$), and Kram~ner and Lange-Bertalot (1986). The uncited ecological data discussed for some of the diatom taxa are based on the PIRLA database maintained at the Paleoecolsgical Environmental Assessment and Research Laboratory (e.g., Charles et al. 1990; Kingston et al. 1990).

Relatively few cyst inorphotypes have been linked to the taxa that produce them (Smol 1995). In 1986, the Enterna- tional Stagospore Working Group (HSWG) published guidelines for cyst descriptions (Cronberg and Sandgren 1986); this has done much to standardize taxonomic research on cysts (e.g.. Wybak 1987; Rybak et al. 1987, 1991; Duff and Smol 1988, 1989, 1991; Zeeb et al. 1990; DUE et al. 1992; Carney et al. 1992). Our descriptions s f the Lake 227 flora followed the ISWG guidelines and the authorities listed above. Unfortunately, the taxonomic affinities of the dominant cysts recorded in this study have not been determined, but information is available on their ecological optima, based on paleolimnological studies using ISWG guidelines (Duff and Smol 1988, 1989, 1991).

Chrysophyte scale taxonomy followed Asmund and Kristiarasen (1986) and Siver (1991b). The ecological data cited came from phytoplankton collections by Siver (1991k), who calculated the abundance-weighted means (AWM) for pH (i.e., the average of all pH values of lakes in which the taxon occurs, weighted by the taxon's relative abundance in each lake) for chrysophyte taxa referred to in the present study. Chemical and phytoplankton data for Lake 227 came from Schindler et al. (1980) and Leavitt et al, (1994).

The microfossil data obtained from the diatom and chrysophyte (cysts and scales) analyses are presented as relative abundance diagrams. Quantitative (i.e., concentration and accumulation rate) analyses were not done because of lack of material from the master core. We used correction hctsrs to proportionally adjust scale counts to cell counts for indi- vidual chrysophyte species (see Siver 199 1 a).

The computer program RATEPOL (5.M. Line, University of Cambridge, Cambridge, U.K.; and H.J.B. Birks, unpublished data) was used to calculate the biosti-atigraphic rate of change (selaset Grimm and Jacobson 1992) in the three different algal data sets. Chord distance (Prentice 1980) between adjacent samples divided by the time interval between the samples provides a simple and robust estimate of the bio- stratigraphic rate of change per year (Bennett et al. 199%). Estimated rates of change permit comparison of the relative rates of response of the different algal groups to experimental manipulation.

It was useful to compare how total variance in the three algal biostratigraphies for 1969 - 1989 was explained by the known water chemical changes since 1969. Thus, a series of partially constrained ordination models (Borcard et al. 1992) were designed to partition the variance in the three data sets into four statistically independent fractions: ( 1 ) the fraction explained by known water chemical changes independent of any other temporal changes; (2) the fraction explained by water chemical changes that are themselves cova~ying with time and hence are time-structured; (3) the fraction explained by time independent of any water chemical changes; and (4) the fraction unexplained by water chemistry or by time. Bsrcad et al. (1992), Legendhe (1993), and Lotter and Birks (1993) provide further details sf this variance-patiorain procedure. Computations were done using the computer program CANOCO version 3.12 (ter Braak 1987-1990).

Can. J . Fish. Ayuat. Sci., VoI. 51, 1994

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

Can. 9. Fish. Aquar. Sci., VoI. 51, 1994

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

Relative abundance (%) Chad distance (~f-?

FIG. 2. Stratigraphic distributions (expressed as relative (8) abundances) and the rate of change (chord distance (yr-')) of common chrysophycean cysts in the sediments of Lake 223. 1 = start of experimental additions of nitrogen (N) and phosphorus (B) at a N:P of 13:1 (by mass); 2 = start of experimental additions of N and P at a N:P of %:I (by mass).

Results and Discussion There are higher inherent differences in sates of change between adjacent samples in the diatom (Fig. 1) and chrysophyte scale (Fig. 3) assemblages than in the chrysophyte cysts (Fig. 2). The maximum rates of change in the cysts coincide almost precisely with the start of addition of N and P at N:P = 13:1 (by mass) (Fig. 2, line 1) and the switch to an N:P - 5:1 (Fig. 2, line 2), whereas the peaks in the rate of change in the scale assemblages (Fig. 3) were delayed by 1-2 yr after these two manipulations. Relationships between the rates sf change in the diatom assemblages and the experimental manipulations were less clear- The maximum rate of change oceumed -2-3 yr after the 1969 manipulation and was maintained for a further 3 yr until the 1975 manipulation. After the second manipulation, there was a consis- tently high rate of change for -6-7 yr.

General patterns in the rate-of-change profiles suggested different responses by the three groups. Prior to manipulation, the diatoms showed a high rate of change from sample to sample, whereas the cysts showed a low rate of change. After manipulation, lags of 2-3 yr appeared in responses by some of the diatoms and chrysophyte scales, but no Hag was evident in the response by the cyst assemblages.

Diatom valves (Fig. I), chrysophyte cysts (Fig. 2), and chrysophyte scales (Fig. 3) were abundant and well-preserved in all samples. Fourteen diatom taxa showed relative abundances >2% of the fossil sum between 1957 and 1990 (Fig. 1). Forty-five chrysophycean cyst msrphotypes were identified with %EM from the sediments, 33 of which had previously been observed and described by authors from the Pale~cological Environmental Assessment and Research Laboratory. Queen's University (PEARL). Twelve s f the most common ones are presented in Fig. 2. Scales from 16 chrysophyte species and one collective group (encom- passing several small Makionzoraas taxa, designated "Ma/- lomonas small") were identified; the most common 10 taxa are presented in Fig. 3 using two methods of calculation (Siver 199 1 a), which revealed similar trends.

Assemblage Changes

All mierofossil assemblages showed striking changes coin- ciding with the initial input of nutrients into the lake in 1969 (Figs. 1-3). The diatom and chrysophyte assemblages present prior to ca. 1969 are referred to as "premanipulation" assemblages, whereas those occurring after this time are referred to as "postmanipulation" assemblages.

Following an experimental decrease in the N:P ratios from 13: 1 to 5: 1 in 1975 (Leavitt et al. 1994), a second assemblage shift occurred in the cyst and scale stratigra- phies (Figs. 2, 3) . Diatom species composition changed less dramatically during this period, although a brief assemblage shift occurred ca. 1980 (Fig. 1 ) . Both chrysophyte scale and cyst assemblages again revealed some species shifts near the top of the core, ca. 1986 (Figs. 2, 3).

There is considerable variation in the patterns of the estimated rates of change for the three algal groups (Figs. 1-3).

Premanipulation Assemblages (ca. 1957-1968)

There are no water chemistry data available for Lake 227 before 1968, so all environmental reconstructisns before then must be based solely on paleolimno1ogical inference.

Diatoms

From ea. 1957-1968, the diatom community was dominated (relative abundances > 10%) by Cj9clotelba stell iger~ (CI. and Crun.) V.H. (1957-1969), Tabelkariafloccukosa (Roth) Kiitz. Strain IV sensu Koppen (1965-1966), Aukuco- seira distans var. tenekh (Ny gaard) Florin Simonsen (1 959), Eunstia PHRLA 1 (1 957-1963), and E. zasumireeresis

Can. J . Fish. Aquat. Sci., Vol. 51, 1994 2303

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

Can. J. Fish. Aqlacat. Sci., VoI. 51, 1994

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

(Cab.) Korner (1959). All taxa are characteristic of unproductive, slightly acidic waters. For example, many Eunotia species are restricted to acidic waters (Bourelly 1968). Nicholls and Carney (1979) found the planktonic Eunotici zcasurninensis in unproductive northern Ontario lakes (total P [TP] = 8-25 pg . L-', n = 7 lakes), and poorly buffered lakes with low alkalinity (4-5 mg CaCO, L-I, n = 7 lakes). Eunotia PIRLA 1 is a finely striated planktonic taxon that has a high length to breadth ratio that was documented in the PIRLA iconograph (Camburn et al. 1984 - 1986). Relatively few autecological data are available for this aaxon because Eunotia PIRLA B was present, in low abundance, in only five Adirondack lakes (pH 4.88-7.75)-

Aulciccsseira distans var. tenella is an acidophilic taxon (Camburn and Kingston 1986) that was recorded in 36 Adirondack lakes with a pH range of 4.88-7.7; it occurred at maximum abundance (23.9%) in Rock Pond (pH = 6.85). It was also found in 14 lakes from the PIRLA Northern Great Lakes Region (Kingston et al. 1990; relative abundance = 0.2-26.476) that had pH values ranging from 5.2 1-7.25.

Tabellaria flocculosa Strain IV is an epiphytic taxon (Koppen 1975). Stockner (197 2 ) found it in the littoral zone of ELA lakes in the spring. However, it was dispersed by tur- bulence into the plankton by June. Findlay and Shearer (1992) recorded it as a dominant taxon in 35 unmanipulated ELA lakes, and they classified it as acidophilic. It was also sometimes common (maximum relative abundance = 11.2%) in 48 of 98 PIRLA Adirondack lakes sampled (pH - 4.48-7.39).

Cyclotella stelligera is commonly found in unproductive to moderately productive systems (Schindler and Holmgren 1971; Stoermer et al. 1985; Christie 1993). It appears to be a pH-indifferent taxon (Dixit et al. 1991; Findlay and Shearer 1992). It was found in lakes located on the Canadian Shield (Bixit et al. 1991; Findlay and Shearer 1992), in alkaline lakes from southeastern Ontario (Christie 1993), and in the Laurentian Great Lakes (Stoermer et al. 1985).

cysts Shifts in the relative percentages of chrysophyte cyst mor-

photypes were slight (i.e., 95% change) in the premanipem- lation sediments, presumably indicating fairly stable lake conditions during this time. Cysts 62 and 76 (Duff and Smol 1991), 33 (Duff and Smol 1989), and 1 (Buff and Smol 1988) dominated, collectively accounting for 75% of the premanipulation cyst assemblage.

Cysts 62, 33, and 76 are highly ornamented taxa typical of unproductive systems. Cyst 33 was described originally from an oligotrophic, mid-arctic. lake where it briefly dominated the chrysophyte assemblage (Duff and Smol 1989). Cysts 62 and 76, originally described from Adirondack Park, New York, were also found in oligotrophic and somewhat acidic waters (Duff and Smol 1991).

Cyst 1 is a small, unomamemted cyst lacking a collar- It has been described from a number of temperate and arctic environments (Duff and Smol 1988, 1991; Zeeb et al. 1998; Wybak et al. 1991). It appears to have a wide ecological tolerance and is pH-indifferent (Rybak et al. 1991), but may occur in more productive waters than the previously discussed taxa (Zeeb et al. 1990).

Scales Premanipulation scales were dominated by a relatively

diverse assemblage of Mallomonas. duerrschmidtiae Siver, Hamer and Kling, M . pseudocoronata Prescott, Synura peterse~zii Korshikov, and S. Lkgbzagnicola (Korsh.) Korshikov. Mallosnos~as duerrschmidtiae is found over relatively nar- row environmental gradients, almost exclusively occurring in lakes of pH <7 (AWM = 5.76) that are low in specific conductance and TP (Siver 199 1 b).

Mallomonas pseudocoronata is a more cosmopolitan species. It is found over a wide TP gradient (918 - >35 pg P . L-I), specific conductance (21-170 pS), and pH values (5.75-8.75; AWM = 7.72) (Siver 1991b).

Synura petersenii is an environmental generalist; it is the most commonly reported Synuru species in the world. Synura sphngnicola is reported as occurring predominantly in acidic waters; it has often been found in large populations in acid bog lakes (Kristiansen 1975; Diirrschmidt 1980; Woijackers and Kessels 1986).

Postmanipulation Assemblages 1969-1989)

From 1969 until 1989, annual nutrient additions to Lake 227 resulted in increased annual averages of TP (fmm 1-8 pg L-I

in 1970; up to 14 p g - L-I in 1971) and total N (TN) concentrations (from 245 pg - L-' in 1969 to 2600 pg * L - I in 1970) in the water column. pH values increased (>9.8) in the epilimnion during the ice-free season (Schindler et al. 1988).

Diatoms Numerous lacustrine studies have shown that diatom

assemblages respond to changes in nutrient concentrations (Brugam 1978; Engstrom et al. 1985; Anderson 1989) and to pH and pH-related factors such as alkalinity (Charles et al. 1989). Therefore, it is likely that changes in the postmanipulation diatom assemblages observed in Lake 227 (Fig. 1) may be related to both increased nutrient concentrations and increased pH.

The relative abundances s f acidophilic and generalist diatoms declined after N and P were added in 1969 (Fig. 1). Relative abundances of Cyclatella stelligera and the acidophilic Eunotia PTRLA 1, E. zsesuminensis, Tabellaria $oc- culosa Strain HV, and Aulacoseira distans var. tenella decreased and were either low or zero for the remainder of the core. The decline of the four acidophilic taxa may be related to the increased pH (8-9) in the epilimnion from July 1969 until October 1969 (Schindler et al. 1971). Cyslstellci stslligera is a pH-indifferent taxon that is moderately tolerant of increased nutrient enrichment (Stoermer et al. 1985), which is consistent with its persistence in mod- est numbers following the manipulation.

The acidophilic taxa were replaced by Synedr-a PIRLA 2, S. rumpens var. @miliaris (Kiitz) Hust,, and S. rumgens Kutz following fertilization (Fig, 1). Many researchers have observed increased abundances of Synedra taxa in response to accel- erated mthropogenic nutrient loading (e.g., Lake Washington: Stockner and Benson 1967; Linsley Pond: Brugam 1978; Found Lake: SmoH and Dickman 1981; Little Round Lake: Smol et al. 1983). Increased abundances of Synedra taxa were also observed following liming events, presumably in response to increased pH levels (Loch Fleet: Flower et al. 1990; Lysevatten: Wenberg and Hultberg 1992). Although the taxonomy of Synedra has been in flux, increases in spindle- shaped Syrledra taxa appear to be typical of the early stages of nutrient enrichment or increased pH levels.

Can. J . Fish. Aquat. Scd., V/oL 51, 1994

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

The ecological characteristics of the three dominant Syaee- dra taxa recorded in Lake 227 have been discussed in recent studies. For example, Findlay and Shearer (1992) found S. rumpens in 12 of 36 unmanipulated lakes at the ELA and they classified it as pH indifferent. The PIRLA database showed that Synedm rumpens and S. r~inzpens var. funrhl- iwris were not common at any sites in the Adirondacks or from the northern Great Lake States, so it is difficult to establish pH tolerances for these taxa.

Synedra PIRLA 2 was common in 28 Adirondack lakes that had a pH range sf 5.1-7.47. Its maximum abundance (24.7%) was recorded in Clear Pond, an unproductive lake (TP = 1 pg - L-': chlorophyll a = 0.3 pg . L-') with a pH of 7.05. However, it was also abundant (14.2%) in Mt. Arab Pond, a more productive system (TP = 15.5 kg . L-I) with a pH of 6.94.

From 1978-1 988, the sedimentary diatom assemblage continued to be dominated by Synedra rumpens var. farnil- iceris; however, increased abundances of benthic tam, such as Frwgdlcerka virescens Ralfs, Hil construens var. venter (Ehrenb.) Grun., Achnanthes minutissiraaa Kiitz, and Ntzschia gracikis Hust., were also observed (Fig. 1). The relative abundance of H;. pinnata Ehrenb. also increased in 1974. These benthic diatoms were clearly more competitive following the 1969 manipulation, which elevated nutrient and pH levels. These taxa would have been tolerant of the increased pH that characterized Lake 227 during the grow- ing seasons following fertilization, and they have often been classified as circumneutral taxa (Achnanbhes rninuti.rsimw: Findlay and Shearer 1992) or alkaliphilic taxa (E construeas var. venter: Brugarm 1983; E pinnata: Findlay and Shearer 1992).

cys ts Between 1969-1975, cysts 42, 33, 76, and 161 (Zeeb and

Smol 1993) decreased in relative abundance, whereas cysts 1, 15 (Duff and Smol 1988), 29 (Duff and Srnol 1989), 233 (this paper), 120 (Duff and Smol, in Duff et al. 1992), and 11 1 (Zeeb et al. 1990) increased. Also, cyst 72 (Duff and Smol 1991) was observed for the first time in the core.

The increase in cyst 1 (from <I 0% in 1968 to >15% in 1970) coincided with the I969 nutrient additions to Lake 227, and is consistent with its increase in Little Round Lake, Ontario, following eutrophication after land clearance (Zeeb et al. 1998). Cyst 1 is similar to those produced by Para- ghysomonas spa. (Preisig and Hibberd 1982, 1983), taxa that are common in the eutrophic waters of Lake Tystrup, Denmark (Kristiansen H 985).

Cysts 15 and 29, which also increased in abundance ca. 1969-1970, are morphologically similar to cyst 1; cyst 15 is about three times larger in diameter, and cyst 29 is distinguished by a shallow conical pore. Both cysts have been observed in arctic (Buff and Smol 1988) and temperate (Zeeb et aB. 1990; Zeeb and Smol 1993) regions. Cyst 29 was found in the early postglacial sediments of Elk Lake, Minnesota. but peaked in abundance near the top of that core when nutrient conditions and temperatures were higher (Zeeb and Smol 1993).

Cyst 233, described for the first time in Appendix I , increased from premanipulation values of ca. 4% to postmanipulation values of 18%. Morphologically, it is most similar to cyst 41, described from a mid-arctic lake (Duff a d Smol 1989), and cyst 78 from Adirondack Park (Duff and

Smol 1991). Cysts 41, 78, and 233 are spherical with a hooked collar, which is typical of the cyst produced by Disrobryon cylindricurn tmhof (Sandgren l98Oa, 1983; Donaldson and Stein 1984). Cysts with hooked collars are often recorded in cyst assemblages (e.g., Adam and Mahood (1979) type 56; cysfa curvicollis Nygaard (Rybak 8986); Wybak et al. (1987) cyst 3; Sandgren and Carney (1983) cyst 9), and are us~aaHBy associated with oligotrophic to mildly eutrophic conditions (Rybak 1986; Rybak et al. 1987; Carney and Sandgren 1983).

Cyst 120 is a larger form of cyst 29 and was described from high-arctic ponds (Duff et al. 1992). It has previously been found in circumneutral to alkaline waters of low productivity (Duff et al. 1992; Zeeb and Smol 1993; Rybak et al. 1987). This study suggests that cyst 120 is also present in high productivity environments.

Cyst 161 peaked in abundance ca. 1978, but then dropped to lower values for the next five years. It is probably produced by Dinoh)-yon diver-gens Imhof (Sheath et al. 1975; Sandgren 1988b), which is a pH-indifferent to alkaliphilis species that thrives in mesotrophic to eutrophic waters (Eloranta 1989).

Cyst 11 1 increased from trace levels in the premanipulation assemblage to ca. 4% in 1971. This cyst is produced by Sginiferomonus trkoralis Takahashi, which is a cosmopolitan species found across a wide range of environmental conditions (e.g., Diirrschmidt 1980; Nicholls 198 1 ; Roijackers and Kessels 1981 ; Croome and Tyler 1988; Siver 1988). It is predominantly a spring-blooming taxon (Diirrschmidt 1980; Kristiansen 1988), and cyst formation occurs during, or prior to, spring ice break-up (Skogstad 1986). Previous paleslimnslogicai reports have linked this cyst with eutrophic conditions (Nygaard 1956; Rybak 1986; Carney and Smdgren 1983; Zeeb et al. 1990), which is consistent with our obser- vations in Lake 224.

Scales Immediately following the 1969 lake manipulation, Ma/-

komonas crassisquama (Asmund) Fott increased dramatically (from 4 0 % to >80% abundance). M C A ~ ~ ~ ~ B P I Z O ~ U S cras- sisgi~arnu is an environmental generalist found over wide ranges of pH, specific conductance, TP, and temperature (Siver 199Ib). A less striking increase occurred with M. dofgnonii var. telaraicostis Asmund and Cronberg, but it had declined by 1972. Very few ecological data are available for M- doignonii, but it is believed to be a cold-water srgan- ism, tentatively classified as acidophilic, and usually present in habitats with specific conductance Bevels 4 3 pS (Siver 1991b). Increased abundances of the above two taxa were mirrored by decreased abundances of M. d~aerrschmidtiae, Synurde petersendi, small Mcrbkomonas species, and M. caudata Ivanov. The ecologicaH requirements of M. caudatw are similar to those of hd. CF-ass isq~ama (Siver 1991b).

Postmanipulation Change in the N:B Ratio (1976-1990)

The second major chrysophyte assemblage shlft occurred ca. 1946, which followed the experimental change in N:P ratios from 13:1 to 5:k by mass in 1975 (Figs. 2, 3). During 11975, N additions were reduced, and N,-fixing cyanobacteria increased in abundance and largely replaced the ehlorophytes (Leavitt and Findlay 1994). During this period, total dissolved nitrogen (TBN) continued to rise (up to 750 pg . L-' in B 989); total dissolved phosphorus (TBP) remained fairly steady (1 983: 13 kg . L- ; 1985: 1 1 pg - L-I)

Can. 9. Fish. Aquaa. Sci.. Vol. 51, 1994

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

% abundance

% abundance

96 abundance FIG. 4. Percent abundances and number of cells counted of selected phytoplankton species in Lake 227 (from field records). (A) Diatoms. (B) Chrysophytes. ( C ) Scaled chrysophytes.

but peaked at 29 pg . L1 in 1984. Following the change similar, although the latter was more diverse; both assem- in N:P ratios in 19'75, relative abundance of cysts 62 and blages were dominated by highly ornamented taxa. Unlike 33 increased to almost premanipulation levels. Relative chryssphyte assemblages, diatom communities showed little abundances sf cysts 72 and 88 (Duff and Smol 1991) d s o response to the change in the N:P ratio. increased, whereas cysts 1, 15, 29, 233, and 120 declined. A less striking shift in cyst assemblage occurred ca. 1985. The premanipulation and post-1975 cyst assemblages were The relative abundance of cyst 62 was unaffected, but cyst

Can. 9. Fish. Aquas. Sci., Vol. 51, 1894 2307

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

33 decreased from >20% to <%%, a d was replaced by cysts 76 and 1%. This shift may have been linked to a sudden increase in TDP (from 14 yg . L-' in 1983 to 29 pg . L-' in 1984) (D.L. Findlay and H.J. Kling, unpublished data).

The sealed chrysophytes also shifted with the change in nutrient ratios ca. 1976. Relative abundances of M . crassisquama and M . doignonii var. teazuict~stis scales decreased, whereas those of S Y I Z U ~ ~ sphag~zicoka increased (Fig. 3). However, M. crassisquama and M. doignonii var. fenuicostis eventually recovered to premanipulation values (Fig. 3).

Variance Partitioning of the Algal Groups

The stratigraphic changes in algal assemblages described above were related to changes in water chemistry by using a series of partially constrained ordinatiora models. The overall amount s f variation explained by water chemistry and time was 79.1%, 7%.0%, and 95.7% for diatoms, scales, and cysts, respectively. Chemical changes independent of time explained 60.5%, 66.3%, and 50.0% of the variation, whereas the time data independent of water chemistry explained only 6.396, 5.9%, and %.I% of the variation. The small amount of total variation accounted for by time alone indicated that no fundamental, temporally structured, environmental process had been missed. Moreover, the analyses indicated that there was a strong relationship between changes in water chemistry and the algal assemblages. Fur- thermore, the low incidence of unexplained variation in chrysophyte cysts (4.3%) suggested that there was a very close relationship between cysts and water chemistry in Lake 227 between 1969 and 1989.

Comparison of Fossil and Planktonic Diatoms and Chrysophytes

Diatoms The planktonic diatom assemblage was dominated (i.e., rel-

ative abundance >20%) by either Synedra rumpens (1970-1972; 1974-1978; 1983-1987), Cyclotella ssellig- era (1973; 1979-1982; 1985), Rhkzosolenia eriensis H.L. Smith (1973-1974; 1978; 1982- B983), or Synedra cf. rumpens vat-. familaroides Grun. (1987-1989), or a combination of these taxa in different years from 1970 until 1988 (Fig. 4A). Synedra ruinpens probably represented a group- ing of the three main Synedra taxa that were detected in the sediment core (i.e., Synedra rumpens, S. rumpens var. ,fa~niliaris, and Synedra PIRLA 2; Fig. I). Hn fact, S. cf. rumpens var. familardaides, observed in 1988 (Fig. 4A), was probably synonymous with Synedra PIRLA 2 recorded from the sediment core (Fig. 1).

The relative abundance of Cyc8otekla stelligera increased in the phytoplankton assemblage (Fig. 4A), whereas it decreased in the sediment core (Fig. 1). The decline may be the result of an influx of benthic taxa that were both tolerant of the increased pH and capable of using the increased nutrients available following fertilization (as discussed above). These benthic taxa would not have been collected in the water samples analyzed for phytoplankton, but they would be observed in the integrated sediment samples.

Rhizosolenia erkensis was common in the phytoplankton assemblage (Fig. 4A). However, its valves were probably destroyed during the sediment analyses by the W2SO4 used to prepare the samples (Yung et al. 1988).

Chrysophytes Thirty chsysophyte species, six genera, and two collective

groups (i.e., "small" and "large" chrysophytes) were dif- ferentiated in the phytoplankton counts from Lake 227 (D.L. Findlay and H.9. Kling, unpublished data). Only two of our common sedimentary cyst morphstypes could be linked to chryssphyte species. Cyst 1 I H (Spinifemmonm triorakis) was present throughout the sediment core, but started to increase in abundance ca. 1969 and peaked ca. 1973 (Fig. 2). Phytoplankton records showed a similar trend; maximum numbers of this species were observed in 1973 (ca. 0.8% abundance), but it was absent in the phytoplankton samples from 1986 onwards (Fig. 4B).

Cyst B 61 (probably Dinobryon divergens) was also present throughout the sediment core. It peaked ca. 1970 and was more abundant in the upper part of the core (1976-1990) than in the lower part (Fig. 2). This species was only recorded in the phytoplankton in 1988 in very low abundances (4.0%; Fig. 4B).

Mallomonas crassisquama iM. pseu696Pcoronata were abundant in the phytoplankton in 1970, and numbers remained high until ca. 1975 (Fig. 4C). These two taxa were always lumped together with M . duerrschmidtiae in the phytoplankton counts because the three taxa were not separated taxonomically until 1990 (Siver et al. 1990). Unfortunately, although Me crassisquama and M. pseudocoronata have similar ecological tolerances (except the former has a wider pH range), M. duerrschmidtiae has very different nutrient and pH optima (Siver 1991 b). Important ecological information was, therefore, lost by lumping the thee taxa together.

Mallomoreas doignonii var. tenuicostis, another dominant species in the sediment chrysophyte assemblage (Fig. 3), was either not identified in the phytoplankton counts or it was lumped into the '6Mallomonas spp." category (Fig. 4C). The presence of h4. caudata and the increased abundance of Synekra spkagizkcola from ca. 1978-1988 in the sediment core (Fig. 3) was reflected in the phytoplankton records (Fig. 4C).

It is difficult to compare the paleoliannological data to the annual phytoplankton records for Lake 227 because of taxonomic inconsistencies. For example, phytoplankton samples were fixed with Lugol's solution and counted using a modified Uterrnohl method (Nauwerck 1963). The identification of the diatom taxa in these samples probably is reli- able only to the genus level because specific or subspecific identification of many taxa depends upon ornamentation of the cell wall, which often requires high-resolution microscopy. Furthermore, it is important to note that the phytoplankton collections represent discrete samples, whereas lake sediments record algal assemblages integrated over time (365 days of the year) and space (from the entire water column and from various habitats).

In view of the fact that no water chemistry data were collected before manipulation, the paleolimnological data provide important baseline information for Lake 227. The lake was unproductive (pH -6) before nutrient addition, as evi- denced by the dominant taxa in the premanipulation diatom assemblage: Cyclotella stelligera, Tabellaria! flocculosa Strain IV, Aulacoseira distans var. tenella, Eunstia PIRLA 1, and E* zasuminensis. Chuysophyte cyst and scale assemblages were

Can. J. Fish. Aquat. Sci., VQI. 54, 1994

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

FIG. Al. Stomatocyst 233 (%eb and Smol), a common cyst morphotype found in the sediments of Lake 227. (A) Scanning electron micrograph. (B) Light micrograph, Scale bars = 2 pm.

diverse and relatively constant during this period. Although Acknowledgments there were some subtle species changes before 1969, these natural fluctuations were insignificant compared with the s&ik- This work was supported by a National Sciences and Engi- ing changes that occurred after fertilization started. neering Research Council of Canada grant to J.P.S. P. Leavitt

Stratigraphic changes in diatom and chrysophyte assem- provided sediment samples and background information for

blages were clearly related to increased nutrient availability Lake 224. The comments of S. Guildford, R. Hecky, D. Rosenberg, and two anonymous reviewers improved the quality of the and/or increased pH resulting from lake fertilization. More- manuscript.

over, there was no significant lag period between initial lake manipulation and when changes were first observed in sedimentary algal assemblages.

The increase in epilimnetic nutrient concentrations and pH after I969 coincided with decreased relative abundance of the premanipulation assemblage, in conjunction with large increases in the relative abundances of Synedra PIKLA 2, S. rumpens var. jamiliaris, Mallomonas crassisquama, and cysts 1, H 5, 29, 128, and 233. From 1940 until the present, the diatom assemblage has continued to be dominated by alkaliphilic or pH-indifferent taxa. Chrysophyte populations had a second large assemblage shift ca. 1976, immediately following the change in N:P ratio, characterized by a decrease in Wawllomsnas crassisquama, an increase in Synura sphag- nkcola, and a return of dominant premanipulation cysts.

It was difficult to compare the paleolimnological data with the annual phytoplankton records that have been maintained for Lake 224, primarily because of taxonomic problems. Furthermore, more diatom and chrysophyte taxa were recorded in the sediment core than in the plankton samples. For example, scaled chrysophytes were rare in the overall phytoplankton records, but showed a striking response to nutrient addition in the sedimentary profiles.

In summary, the paleo8imnological data presented in this study complement the annual phytoplankton records presently available and provide additional information describing the spatial and temporal responses of diatom and chrysophyte assemblages to whsle-lake fertilization. The data also provide insights into the relative responsiveness of different algal groups to major environmental perturbations.

Appendix

Description of a new Chrysophyte Cyst

Following the International Statospore Working Group (HSWG) guidelines (Cronberg and Sandgren 19861, we describe a new cyst morphotype that was common in the Lake 224 sediments. The number in parentheses following the authors' names indicates the number of scanning electron microscope (SEM) micrographs on which the description is based. The negative number, locality information, and first figure refer to the characteristic SEM specimen. Cyst numbering follows consecutively from Duff and Smol (1994).

Stomatocyst 233, Zeeb and Smol (6) Negative No.: J.P. Smol 586, Plate 1 Locality: Experimental Lakes Area Lake 227, Ontario, varve

No. 17

This is a large, spherical stomatocyst (diam. 12.3-14.4 km). The collar has a conical base with a gradual basal margin, and a hooked apical portion (basal d im . ca. 3.6 wm; apical ddiam. 1.6-2.6 pm; height to flexure 2.8-3.2 pm; length to 5.5 pm). The collar is radially striated. The entire cyst surface is densely scabrate with occasional smooth patches. The scabrae may be elongated (diam. 8.2-8.4 km; height 0.2-0.3 pem) and extend up the length of the collar. 'This stomatocyst is very similar to one produced by Dlnobryon cylindricum Hmhof (Donaldson and Stein 1984; Sandgren 1980a, 1983, 1989),

Can. J. Fish. Aquat. Sci., Vol. 51, 1994

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

although scabrate forms have not been recorded. With %EM and light microscopy, stomatocyst 233 can be distinguished from stomatocyst 41 (Duff and Smol 1989) by the presence sf scabrae, and from stomatocyst 78 (Buff and Smol 1991) by the absence sf a bipartite collar and the lack s f venrucae.

References ADAM, D.P., AND A.D. MAHOOD. 1979. Modern and Holocene chrysom-

monad cysts from Alta Morris Lake, Eldorado County, California. US Geol. Surv. Open-File Rep. 70-1461. 13 p.

ANDERSON, N.J. 1989. A whole-basin diatom accumulatisn rate for a small eutrophic lake in northern Ireland and its palaeoecological implications. J. Ecol. l I : 926-946.

ASMUND, B., AND J. KRISTIANSEN. 1986. The genus MaEEomolz~.s (Chryso- phyceae). Opera Bot. 85: 128 p.

BENNETT, K.D., %. BBREHAM, M.J. SHARP, A N D V.R. SWITSUR. 1992. Holocene history of environment, vegetation and human settlement on Catta Ness, Lunnastung, Shetland. J. Ecol. 80: 241-273.

BORCARD, D., P. LEGENDRE, AND P. DRAPEAU. 1992. Partialling out the spatial component of ecological variation. Ecology, 73: 1045 -1055.

BOURELI,Y, P. 2968. Les algues d'eau douce. Tome It. Les algues jaunes et brunes. N. Boubee et Cie, Paris.

BRUGAM, R.B. 1978. Human disturbance and the historical development of Linsley Pond. Ecology, 59: 19-36.

BRUGAM, R.B. 1983. The relationship between fossil diatom assemblages and limnological conditions. Hydrobiologia, 98: 223-235.

CAMBURN, K.B., AND J.C. KINGSTON. 1986. The genus Mebsira from soft- water lakes with special reference to northern Michigan, Wisconsin and Minnesota, p. 17-34. In J.P. Smol et al. led.] Diatoms and lake acidity. Dr. W. Junk Publishers, Bordrecht, The Netherlands.

CAMBURN, K.E., J.C. KINGSTON, AND D.F. CHARLES [ed.]. 1984-1986. PIRLA diatom iconograph. PIRLA Unpubl. Rep. Ser. 3. Indiana Uni- versity, Bloomington, IN.

CARNEY, H.J., AND C.D. SANDGREN. 1983. Chrysophycean cysts: indicators of eutrophication in the recent sediments of Frains Lake, Michigan, U.S.A. Hydrobiologia, 101: 195 -202.

CARNEY, H.J., M.C. WHITING, K.E. DUFF, AND D.R. WHITEHEAD. 1992. Chrysophycean cysts in Sierra Nevada (California) lake sediments: paleoecological potential. I. Baieolimnol. 7: 73 -94.

CHARLES, D.F., R.W. BATTARBEE, I. RENBEWG, H. VAN DAM, AND J.P. SMOL. 1989. Paleoecological analyses of lake acidification trends in North America and Europe using diatoms and chrysophykes. p. 207-270. In S.A. Norton, S.E. Lindberg, and A.L. Page Led.] Acidic precipitation volume 4: soils, aquatic processes and lake acidification. Springer- Verlag, Stuttgart.

CHARLES, D.F., M.W. BINFORD, E.T. FURLONG, R.A. HITES, M.J. MITCHELL, S.A. NORTON, F. OLDFIELD, M.J. PATERSON, J.P. SMBL, A.J. UUTALA, J.R, WHITE, B.R. WHITEHEAD, AND R.J. WISE. 1990. Paleoecological investigation of recent lake acidification in the Adirondack Mountains, N.Y. J. Paleslimnol. 3: 195 -241.

CHRISTIE, C. 1993. Paleoecological reconstruction of lake trophic status: the effect of human activity on lake conditions in southeastern Ontario in the recent (ca. 200 years) past. Ph.D. thesis, Queens University, Kingston, Ont. 21 1 p.

CLEVE-EULER, A. 1951-1955. Die Diatomeen von Schweden und Finnland. Kungl. Svenska Vetenskapsakademiens Handlingar. Fjarde Serien Band 2(1), Band 3(3), Band 4(5). (Republished by J. Cramer, Berlin, as Bibl. Phycol. 5, 1968).

CRONBERG, G., AND C.D. SANMREN. 1986. A proposal for the deveiop- ment of standardized nomenclature and terminology for chrysophycean statospores. p. 317-328. In J. Kristiansen and R.A. Andersen [ed.] Chrysophytes: aspects and problems. Cambridge University Press, Cambridge, MA.

CROOME, R.L., AND P.A. TYLER. 1988. Phytsflagellates and their ecology in Tasmanian polyhumic lakes. Hydrobiologia, 161: 245-253.

DIXIT, S.S., A.S. DIXBT, AND J,P. SMOL. 1991. Multivxiable environmental inferences based on diatom assemblages from Suetbury (Canada) lakes. Freshwater Biol. 26: 25 1-266.

DONALDSON, D.W., AND J.R. STEIN. 1984. Identification of planktonic Mar- lomonadaceae and other Chrysophyceae from selected Bakes in the lower Fraser Valley, British Columbia, Canada. Can. J. Bot. 67: 525-539.

DLTFF, K.E., AND J.P. SMOL. 1988. Chrysophycean stomatocysts from the postglacial sediments of a High Arctic lake. Can. J. Bot. 66: 11 17-1 128.

DUFF, K.E., AND J.P. SMOL. 1989. Cbryscsphyceaaa stomatocysts from the post-

glacial sediments of Tasikutaaq Lake, Baffin Island, N.W.T. Can. J. Bot. 67: 1649-1656.

DUFF, K.E., AND J.P. SMOL. 1991. Morphological descriptions and stratigraphic distributions of the chqssphycean stomatocysts from a recently acidified lake (Adirondack Park, N.Y .). J. PaHeolimncsl. 5: 73- 1 13.

D u F ~ , K.E., AND J.P. SMOL. 1994. Chrysophycean cyst flora from British Columbia (Canada) lakes. Nova Hedwigia, 58: 353-389.

DUFF, K.E., M.S.V. DOUGLAS, AND J.P. SMOL. 1992. Chrysophyte cysts in 36 Canadian high arctic ponds. Nord. J. Bot. 12: 471-499.

DURRSCHMIDT, M. 1980. Studies on the Chryssphyceae from Rio Cruces, Prov. Valdivia, south Chile by scanning and transmission inicroscopy. Nova Medwigia 33: 353-388.

ELORANTA, P. 1989. On the ecology of the genus Dinobryon in Finnish lakes. Beih. Nova Hedwigia, 95: 99-109.

ENGSTROM. D.R., E.B. SWAIN, AND J.C. KINGSTON. 1985. A paleolimnological record of human disturbance from Harvey's Lake, Vermont: g e e chemistry, pigments and diatoms. Freshwater Biol. 15: 261-288.

FINDLAY, D.L., AND J.A. SHEARER. 1992. Relationships between sedimentary diatom assemblages and lakewater pH values in the Experimental Lakes Area. J. Paleolimnol. 7: 145-156.

FINDLAY, D.L., W.E. HECKY, L.L. HENDZEL, M.P. STAINTON, A N D

G.W. WECEHR. 1994. Relationship between N,-fixation and hetero- cyst abundance and its relevance t s the nitrogen budget of Lake 227. Can. J. Fish. Aquat. Sci. 51: 2254-2266.

FLETT, R.J., D.W. SCHINDLER, R.D. HAMILTON, AND N.E.R. CAMPBELL. 1980. Nitrogen fixation in Canadian Precambrian Shield lakes. Can. J. Fish. Aquat. Sci. 37: 494-505.

FLOWER, R.J., N.G. CAMERON, N. ROSE, S.C. FRITZ, R. HARRIMAN, AND A.C. STEVENSON. 1990. Post-1970 water chemistry changes and pale- olimnslogy of several acidified upland lakes in the U.K. Philos. Trms. R. Soc. Lond. B. Biol. Scii. 327: 427-433.

GRIMM, E.C., AND G.L. JACoBsoN. 1992. Fossil-pollen evidence for abrupt climate changes during the past 18 008 years in eastern North America. Clirn. Dyn. 6: 179-1 84.

HUSTEDT, F. 1928-1966. Die Kieselagen Deutschlands, ~s ter re ichs und der Schweiz unter Beriicksichtigung der Ubrigen Lgnder Buropas sowie der angrenzenden Meeresgebiete. In Dr. L. Wabenhorst's Krypts- gamenflora von Deutschland, osterreich und der Schweiz, parts 1-3. (Reprinted by Koeltz, Konigstein, Germany, 1977).

HUSTEDT, F. 1930. Bacillariophyta (Diatomaceae). In A. Pascher led.] Die SiiBwasserflora Mitteleuropas, Heft 10. Gustav Fischer Verlag, Jena.

KINGSTON, J.C., R.B. COOK, W.G. KWEIS, JR., K.E. CAMBURN, S.A. NORTON, P.R. SWEETS, M.W. BINFORD, M.J. MITCHELL, S.C. SCHINDLER, L.C.K. SHANE, AND G.A. KLNG. 1990. Paleoecological investigation of recent lake acidification in the northern Great Lakes states. J. Pale- olimnoi. 4: 153-201.

KOPPEN, J.D. 1975. Morphological and taxonomic considerations of Tabellaria (Bacillariophyceae) from the worth central United States. J. Phycol. 2: 236-244.

KRAMMER, K., AND H. LANGE-BERTALOT. 1986. Naviculaceae. Neue unwenig bekannte Taxa, neue Kombination un Synonyme Sswie Bermerkungen zu einigen Gattungen. J. Cramer, Berlin.

KWISTIANSEN, J. 1975. On the occurrence of the species of Synura (Chrys- ophyceae). Int. Ver. Theor. Angew. Limnol. Verh. 19: 2709-2715.

KRISTIANSEN, J. 1985. Occurrence of scale-bearing Chrysophyceae in a eutrophic Danish lake. Bnt. Ver. Theor. Angew. Limnol. Verh. 22: 2826-2829.

KRISTHANSEN, J. 1988. Seasonal occurrence of silica-scaled chrysophytes under eutrophic conditions. Hydrobiologia, 161: 171-1 84.

LEAVBTT, P.R., AND D.L. FINDLAY. 1994. Comparison of fossil pigments with 20 years of phytoplankton data from eutrophic Lake 227, Exper- imental Lakes Area, Ontario. Can. J. Fish. Aquat. Sci. 51: 2286-2299.

LEAVITT, P.R., B.J. HANN, J.P. SMOL, B.A. ZEEB, C.E. CHRISTIE, B. WOLFE, AND H.J. KLING. 1994. Analysis of whole-lake experiments: an overview of results from Experimental Lakes Area Lake 227. Can. J. Fish. Aquat. Sci. 51: 2322-2332.

LEAVITT, P.R., S. CARPENTER, AND J.F. KHTCHELL. 1989. Whole-lake experiments: the annual record of fossil pigments and zooplankton. Lim- nol. Bceanogr. 34: 700-717.

LEGENDRE, P. 1993. Spatial autoccsrrelation: trouble or new paradigm? Ecology, 73: 1659-1673.

LEVINE, S.N., M.P. STAINTON, AND D.W. SCKINDLER. 1986 A radiotracer study of phosphorus cycling in a eutrophic Canadian Shield lake. Lake 227, northwestern Ontario. Canira. J. Fish. Aquat. Sci. 43: 366-378.

LOTTER, A.F., AND H.J.B. BIRKS. 1993. The impact of the Laacher See Tephra on terrestrial and aquatic ecosystems in the Black Forest (Southern Germany). J. Quat. Sci. 8: 263-276.

Can. J . FFish. Aquat. Sci., Vok. 51, 1994

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

MALLEY, D.F., P.S.S. CHANG, D.L. FINDLAY, A N D G.A. LINSEY. 1988. Extreme perturbation of the zooplankton community of a small Pre- cambrian Shield lake by the addition of nutrients. Int. Ver. Theor. Angew. Limnol. Verh. 23: 2237-2247.

NALJWERCK, A. 1963. Die Beziehungen zwischen Zooplankton und Phyto- plankton irn See Erken. Symb. Bot. Ups. 17(5B: 163 p.

NICHOLLS. K.H. 1981. Chrysococcusfurca~us (Dolg.) comb. nov.: a new name for Chrysastrellu furcara (Dolg.) Defl. based on the discovery of the vegetative stage. Phycslogia 20: 16-21.

NICHOLI.~, K.H., AND E.C. CARNEY. 1979. The rare planktonic diatom Euno~iu zusurninensis in Canada. Can. J. Bot. 57: 1150-1 154.

NYCAARD, G. 1956. Ancient and recent flora of diatoms and Chrysophyceae in Lake Grabs@. Folia Limnol. Scand. 8: 32-262.

PAIALAS, K. 1971. Crustacean plankton communities in 45 lakes in the Experirnental Lakes Area, northwestern Ontario. J. Fish. Res. Board Can. 28: 23 1-244.

PATRICK R.. AND C.W. Rb1h.f~~ 1966. The diatoms of the United States exclusive of Alaska and Hawaii. Vol. 1. Livingston Publishing Co., Philadelphia, Penn.

PATRICK R., AND C.W. REIMLR. 1975. The diatoms of the United States exclusive of Alaska and Hawaii. Vol. 2. Livingston Publishing Co., Philadelphia, Penn.

PREISIG, H.R., AND D.J. HBBBERD. 1982. Ultrastructure and taxonomy of Pur~1physo?raunas. (Chrysophyceae) and related genera: 2. Nord. J. Boe. 2: 601-438.

Pw~rs~o , H.W., AND D.J. HIBBERD. 1983. Ultrastructure and taxonomy of Paraprhp.so~nonas (Chrysophyceae) and related genera: 3. Nord. J. Bot. 3: 695-723.

PRENTICE, I.C. 1980. Multidimensional scaling as a research tool in Quaternary palynology: a review of theory and methods. Rev. Palaeobot. Palynol. 31: 71-104.

RENBERG, I.. AND PI. HL~LTBERG. 1992. A paleolimnological assessment of acidification and liming effects on diatom assemblages in a Swedish lake. Can. J. Fish. Aquat. Sci. 49: 65-72.

ROIJACKERS, R.M.M., AND W. KESSELS. 1081. Chrysophyceae fmm freshwater localities near Nijmegen, The Netherlands. 11. Bydrobiologia, 88: 23 1-239.

ROIJACKERS, R.M.M., AND H. KESSEI~S. 1986. Ecological characteristics of scale-bearing Chrysophyceae from the Netherlands. Nnrd. J. Bot. 6: 373-385.

WYBAK, M. 1986. The chrysophycean paleocyst flora of the bottom sediments of Kortowskie Lake (Poland) and its ecological significance. Hydro- biologia, 140: 67-84.

RYBAK, M. 1987. Fossil chrysophycean cyst floa-a of Racze Lake, Wolin Island (Poland) in relation to paleoenvironmental conditions. Hydro- biologia, 150: 257-272.

RYBAK, M., I. RYBAK, AND M. DICKMAN. 1987. Fossil chsyssphycean cyst flora in a small meromictic lake in southern Ontario, and its paleoecological interpretation. Can. J. Bot. 65: 2425-2440.

WYBAK, M., I. RYBAK, AND K. NHCHOLI,~. 1991. Sedimentary chrysophycean cyst assemblages as paleoindicators in acid sensitive lakes. J. Pale- olimnol. 5: 19-72.

SANDGREN. C.D. 1980a. An ultrastructural investigation of resting cyst formation in Dinobryon cylindricurn Imhof (Chrysophyceae, Chsys- opkycota). Protistologica, 16: 259 -275.

SANDGREN. C.D. 1980b. Resting cyst formation in selected chrysophyte flagellates: an ultrastructural survey including a proposal for the phy- logenetic significance of interspecific variations in the encystment process. Protistologica, 16: 289-303.

SANDGREN, C.B. 1983. Survival strategies of chrysophycean flagellates: reproduction and the formation of resistant resting cysts, p. 23-48. %rm G.A. Fryxell Led.] Survival strategies of the algae. Cambridge Uni- versity Press, Cambridge, Mass.

SANDGREN, C.D. 1989. SEM investigations of statospore (stomatocyst) development in diverse members of the Chrysophyceae and Synuri- phyceae. Beih. Nova Hedwigia, 95: 45-69.

SANDGWEN, C.D., AND H.J. CARNEY. 1983. A flora of fossil Chrysophycean cysts from the recent sediments of Frains Lake, Michigan, USA. Nova Hedwigia, 38: 129-163.

SCWINDLER, D.W. 1977. Evolution of phosphorus limitation in lakes. Science (Wash., D.C.), 195: 260-262.

SCHINDI-ER, D.W., AND E.J. FEE. 1974. The Experimental Lakes Area:

whole-lake experiments in eutrophication. J. Fish. Wes. Board Can. 31: 937-953.

SCHBNDLER, D.W., F.A.J. ARMSTRONG, S.K. HOLMGREN, AND G.J. BRUNSKILL. 1971. Eutrophication of Lake 227, Experimental Lakes Area, nsrth- western Ontario by addition of phosphate and nitrate. J . Fish. Res. Board Can. 28: 1763-1782.

SC'HINDLFR, D.W., AND S.K. HOLMGREN. 1971. Primary production and phytoplankton in the Experimental Lakes Area QELA) northwestern Ontario and other low-carbonate waters and a liquid scintillation method for determining I4c activity in photosynthesis. J. Fish. Res. Board Can. 28: 189 -201.

SCHINDE-ER, D.W., R.H. HESSLEIN, AND M.A. TURNER. 1987. Exchange of nutrients between sediments and water after 15 years of experimental eutrophication. Can. J. Fish. Aquat. Sci. 44(Suppl. 1): 6-25.

SCMINDI,ER, D.W., R.W. NEWBUKY, K . G . BEATY, J. PROKOPOWICH, T. R u s z c z ~ ~ s ~ i , AND J.A. DALTON. 1980. Effects of a windstorm and forest fire on chemical losses from forested watersheds and on the quality of receiving streams. Can. J. Fish. Aquat. Sci. 37: 328-334.

SHEATH. R.G., J.A. HELLEBUST, AND T. SAWA. 1975. The statospore of Dinobryo~z divergens Imhof: formation and germination in a subarctic Lake. J. Phycol. 11: 131-138.

SIVER. P.A. 1988. The distribution and ecology of Spiniferomonas (Chays- ophyceae) in Connecticut (USA). Nord. J. Bot. 8: 205-212.

SIVER, P.A. 1991a. Implications for improving paleolimnological inference models utilizing scale-bearing siliceous algae: transforming scale counts to sell counts. J. Paleolimnol. 5: 219-225.

Savs~ , P.A. 1991b. The biology of Mullomonas: morphology, taxonomy and ecology. Kluwer Academic Publishers, Boston.

SIVER, P.A.. J.S. HAMER, AND H. KLHNG. 1990. The separation of Mul- lornunas sl'uerrschidtiue sp. nov. from h4. crussisquum~ and M. pseudo- curonata: implications for paleoBimnologica~ research. J. Phycol. 26: 728 -740.

SKOGSTAD, A. 1986. Chromophysomoncls (Chrysophyceae) from twenty- seven localities in the Oslo area, p. 259-269. In J. Kristiansen and W.A. Andersen (ed.] Chrysophytes: aspects and problems. Cambridge University Press, Cambridge, Mass.

SMOL, 9.P. 1983. Paleophycology of a high arctic lake near Cape Herschel, Ellesmere Island. Can. J. Bot. 61: 2195 -2204.

SMOL. J.P. 1995. Application of chrysophytes to problems in paleoecology. In C. Sandgren, J.P. Smol, and J. Kristiansen [ed.] Chrysophyte algae: ecology, phylogeny and development. Cambridge University Press, Cambridge, Mass. pp. 303-329.

SMOL. J.P., AND M.D. DICKMAN. 1981. The recent histories sf three Cana- dian Shield lakes: a paleolimnological experiment. Arch. Hydrobiol. 93: 83 -108.

SAIOL, J.P., S.R. BROWN, AND R.N. MCNEELY. 1983. Cultural disturbances and trophic history of a small meromictic lake from central Canada. Hydrobiologia, 103: 125 -1 30.

STOCKNER, J.G. 197 1. Preliminary characterization of lakes in the Experi- mental Lakes Area, northwestern Ontario, using diatom occurrences in sediments. J. Fish. Res. Board Can. 28: 265-275.

STOCKNER, J.G., AND W.W. BENSON. 1967. The succession of diatom assemblages in the recent sediments of Lake Washington. Limnol. Oceanogr. 5: 195-211.

S'FOEWM~R, E.F., J.A. WOLIN, C.L. SCHELSKE, AND D.J. CONLEY. 1985. An assessment s f ecological changes during the recent history of Lake Ontario based on siliceous algal microfossils preserved in the sediments. J. Phycol. 21: 257-276.

TER BRAAK, C.J.F. 1987-1 990. CANOCB-a FORTRAN program for CANOnical Community Ordination. Microcomputer Power, Ithaca, N.Y.

WOLFE, B., H.J. KL~ING, G.J. BRITNSKILL, AND P. WI~KINSON. 1994. Multi- ple dating of a freeze core from Lake 227, an experimentally fertilized lake with varved sediments. Can. J. Fish. Aquat. Sci. 51: 2274-2285.

YUNC,, Ye-K., K.H. NICHOLLS, AND A.G. CHENG. 1988. The detection of Whizosoletaiu (Bacillariophyceae) in sediment of Ontario lakes and implications for paleoecology. J. Paleolimnol. 1 : 6 1-69.

ZEER, B.A., AND J.P. SMOL. 1993. Chrysophycean stomatocyst flora sf Elk Lake, Clearwater County, Minnesota. Can. J. Bot. 71: 737-756.

ZEEB, B.A., K.E. DUFF, AND J.P. SMBI,. 1990. Morphological descriptions and stratigraphic profiles of chrysophycean stomatocysts from the recent sediments of Little Round Lake, Ontario. Nova Hedwigia, 51: 361-380.

Can. J . Fish. Aquae. Sci., Vul. 51, 1994

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

om w

ww

.nrc

rese

arch

pres

s.co

m b

y U

NIV

CH

ICA

GO

on

11/1

2/14

For

pers

onal

use

onl

y.

Documents

Responses of Diatom and Chrysophyte Assemblages in Lake 227 Sediments to Experimental Eutrophication