contribution of ciliated protozoa to the planktonic biomass in a series of ontario lakes:...

Journal of Plankton Research Volume 6 Number 3 1984

Contribution of ciliated protozoa to the planktonic biomass in aseries of Ontario lakes: quantitative estimates and dynamicalrelationships

Michael A.Gates and U.T.Lewg

Department of Zoology, University of Toronto, 25 Harbord Street, Toronto,Ontario M5S 1A1, Canada

(Received March 1983; accepted January 1984)

Abstract. The plankton of nine Ontario lakes spanning several physiographic regions was sampledevery two weeks during the ice-free period of 1981, and one lake was studied in the three previousyears. Phytoplankton, zooplankton, and ciliated protozoa were sampled, counted and sized. The sizedata were converted to biomass estimates to yield quantitative comparisons of the relative allocationof biomass among different functional compartments. This is the first study to look simultaneouslyand quantitatively at the total plankton system of lakes (including dliates, phytoplankton and netzooplankton) over a broad physiographic region. Ciliates constitute - 10<ft of the non-algal biomassand 5% of the total planktonic biomass of these lakes. Ciliate standing crops among lakes are signifi-cantly corrrelated with total organic and total inorganic carbon concentrations in the water column,while the dynamics of ciliate biomass fluctuations are significantly correlated with variations in totalphosphorus concentration, in conductivity, in Kjeldahl nitrogen concentration, and in inorganiccarbon content. There appears to be a significant dynamical relationship between ciliates as a pro-portion of the total planktonic biomass, exclusive of filamentous and large ( >30 pm) spherical algae,and the relative biomass of small algae (2 — 5 /tm) as a fraction of total algal biomass, again exclusiveof filaments and large (>30 /an) algae. The hypothesis is advanced that dliates primarily function asbacterial grazers in planktonic ecosystems and that their primary competitors in this role are rotifers.

Introduction

Ciliated protozoa commonly are present in the plankton of freshwater lakes,often in substantial numbers. Yet they rarely are included in zooplankton studies,even when sampled and adequately preserved (Pace and Orcutt, 1981). Whenthey have been studied at all, limnologists usually have been content to measureabundances and/or biomass by taxonomic categories in a single lake (Bamforth,1958; Bark, 1981; Davis, 1973; Finlay, 1980, 1981; Goulder, 1972; Hecky et al.,1978; Hecky and KHng, 1981; Mamaeva, 1976; Nauwerck, 1963; Pace and Or-cutt, 1981; Pace, 1982; Rigler et al., 1974; Sorokin and Paveljeva, 1972; Taylorand Lean, 1981; Wilbert, 1969). An important exception is a recent study (Beaverand Crisman, 1982) of a series of 20 Florida lakes of varying trophic levels. Thatstudy, however, measured abundance and biomass of ciliates in isolation fromother plankton components. The present study is the first to examine quantitat-ively all planktonic compartments (except bacteria) across a lake set.

Because ciliates potentially are capable of recycling a large percentage of thetotal dissolved phosphorus in plankton communities (Johannes, 1965; Buechlerand Dillon, 1974; Taylor and Lean, 1981), and thus may be important links inaquatic food chains (Porter et al., 1979), it is important to assess quantitatively

© IRL Press Limited, Oxford, England. 443

at Stanford Medical C

enter on October 7, 2012

http://plankt.oxfordjournals.org/D

ownloaded from

http://plankt.oxfordjournals.org/

M.A.Gates and U.T.Lewg

the relative contribution of ciliates, phytoplankton, and zooplankton to plank-tonic biomass.

Here we report the results of a cooperative study of plankton dynamics for ninerelatively oligotrophic Ontario lakes sampled in 1981. For one of these lakes,comparable data are presented for the three previous sampling seasons. Ciliatebiomasses are estimated for these lakes for each sampling period, and these areexamined for correlations both with biomasses in other planktonic compartmentsand with standard limnological parameters.

Methods

Nine lakes in Ontario, from four physiographic regions, were sampled ninetimes at approximately fortnightly intervals (called cycles) during the spring andsummer of 1981 (see Table I). Cycles occurred at comparable calendar dates inseparate years. Simultaneous wateT chemistry, zooplankton, phytoplankton andciliate samples were taken at the deepest point in the major basin of each lake,and a Hydrolab Surveyer was lowered to collect depth profiles of temperatures,pH, conductivity, oxidation reduction potential and dissolved oxygen. A Secchidisk (20 cm diameter) was used to measure water transparency, and a submarinephotometer (Canadian Research Institute model DPMT-100) measured lightpenetration.

Zooplankton samples were collected with a metered Wisconsin-style conicaltow net with mesh size 110 /on and fitted with an Auerbach closure. The net waspulled by hand from near-bottom to the surface, and samples were preserved in4% formalin-4% sucrose. Sample aliquots were examined under phase micro-scopy in circular counting chambers, and images of individual plankters wereprojected onto a screen, where they were measured individually with electroniccalipers (Sprules and Knoechel, 1983). Maximal dimensions were used to placeindividual specimens into one of 10 functional size categories. For herbivores,these were: <0.3, 0.3-0.5,0.5-0.85,0.85-1.2, and > 1.2 mm. For carnivores,these were: <0.5, 0.5-0.9, 0.9-1.2, 1.2-1.5, and >1.5 mm. The classificationof taxa into herbivores and carnivores and the rationale for the size class ap-proach are given elsewhere (Sprules and Holtby, 1979; Sprules and Knoechel,1983). Biomass was estimated using regressions of wet-weight on length for eachfunctional size category (Sprules and Knoechel, 1983).

Integrated phytoplankton and ciliate samples were collected from the mixedpool of two hauls of an 8 m-long weighted plastic tube (9 mm diameter), whichwas separated into two compartments at its midpoint. The 0 — 4 m and 4 — 8 msamples were kept and processed separately for phytoplankton and ciliates. Forthese lakes, the epilimnetic boundary fluctuated within the 0 — 8 m zone, andoften lay within the 0—4 m segment (Zimmerman et al., 1983).

Water samples were also collected by the integrated tube sampler. They wereanalyzed by laboratories of the Ontario Ministry of the Environment using stan-dard wet chemical techniques for ligands and atomic absorption spectroscopy formetals (Ontario Ministry of the Environment, 1981). Alkalinities were deter-mined in the field by modified Gran titration (Zimmerman and Harvey, 1979).

Phytoplankton samples of 100 ml volume were preserved in 1% Lugol's iodine

444




ownloaded from


Ciliated protozoa In Ontario lakes

solution and settled with a special chamber (Knoechel and Kalff, 1976) ontomicroscope slides, which were dried and made into permanent preparations.Individual cells and colonies were measured under phase microscopy and placedinto size categories. For spherical cells and colonies, five functional size classeswere used: <2 urn (small blue-green algae and bacteria), 2 - 5 /im, 5-10 /an,10-30 /an and >30 /im. The 5, 10 and 30 fim divisions represent optimal andmaximal size limits for rotifer grazers and the upper availability limit for cla-doceran grazers, respectively (Sprules and Knoechel, 1983). Filamentous algaewere treated separately. Volumes were calculated using geometric formulae andconverted into biomass by assuming neutral buoyancy (i.e., a specific gravity of1.0).

Ciliate samples of 120 ml volume were collected from the mixed integratedtube sample and immediately added to 1 ml of Rodhe's iodine solution in amberflint glass bottles to yield a final concentration of 0.5% iodine. They were storedat 10°C in the dark until 50 ml subsamples were taken (after shaking) and settledovernight in Utermohl chambers. The settled slides were examined under phasemicroscopy with a Zeiss inverted microscope at 500 x total magnification. Asingle observer examined all slides by uniform horizontal transects; each ciliatewas measured for length and maximum body width (excluding the ciliary feedingorganelles: Corliss, 1979). Because most planktonic ciliates are radially symmetri-cal, volumes were estimated by application of the formula for a prolate spheroidand converted to biomass using a directly measured wet-weight conversion con-stant of 0.416 pg nm~3 (Gates et al., 1982).

Ciliate data for lake K6 for the three previous sampling seasons were obtainedby settling 50 ml of each preserved phytoplankton sample. This material hadbeen saved and stored in the dark subsequent to the preparation of permanentphytoplankton slides from sample ah'quots.

All data were entered onto magnetic disk memory and processed on the Univer-sity of Toronto's IBM 3033 system, either with FORTRAN programs or with theSAS program package. Simple regression analyses were performed on the De-partment of Zoology's PDP11 UNIX system, using the S package.

Analysis of duplicate subsamples settled from the same original samples (forK6, sampling cycles 6 and 7) revealed no statistically significant (p>0.05 usingt-tests) differences in numerical density estimates (21.5 and 16.4 ml"1 for0 - 4 m, 36.0 and 34.1 ml"1 for 4 - 8 m, for cycle 6; 46.2 and 48.6 ml"1 for0 - 4 m, 29.4 and 29.8 ml"1 for 4 - 8 m, for cycle 7), but second subsamples con-sistently had lower biomass densities.

In order to test the robustness of the estimation procedure, a special samplingtrip was made to Jack Lake (44° 41' N; 78° 03' W) on 18 August, 1981 to obtaindensity and biomass estimates to compare with those of Taylor and Lean (1981)for the same lake in the previous summer.

Results

The Jack Lake samples yielded estimates for ciliate density of 7.4 and 6.6 ml~ l

for two replicate samples. In view of temporal fluctuations within lakes (seebelow) and average values reported for other lakes worldwide (Gates, 1984), these

445




ownloaded from


iT

able

I.

Mea

n va

lues

of

som

e lim

nolo

gica

l pa

ram

eter

s fo

r a

seri

es o

f O

ntar

io l

akes

dur

ing

the

ice-

free

per

iod

of 1

981.

Nam

e

K6

M2

M4

M5

M6

M8

N4

N5

05

Loc

atio

nL

at.

(°N

)

44°

50'

45°

12'

45°

05'

45°

59'

45°

11'

45°

10'

45°

53'

46°

01

'44

° 4

3'

Lon

g.(°

W)

78°

29'

78°

56'

79°

02'

78°

43

'78

° 50

'79

° 27

'79

° 30

'79

° 3

1'

79°

10'

Mea

nde

pth

(m) 3.72

9.37

8.15

13.4

38.

103.

482.

565.

724.

33

Max

imum

dept

h(m

)

10.4

21.9

23.5

31.4

16.8

11.0 5.8

14.6

10.4

Surf

ace

area

(km

*)

1.75

0.50

0.59

3.19

0.33

9.29

0.29

1.97

0.93

Secc

hide

pth

(m)

4.4

8.4

3.6

7.0

6.3

3.7

3.4

5.6

4.5

Tot

al[P

]

14 9 17 7 14 16 28 14 19

Epi

limne

ticC

hlor

ophy

ll a

b I 8. c H

1.4

0.7

1.3

1.0

0.9

1.1 1.4

1.7

1.4

Tab

le I

. (c

onti

nued

)

Nam

e V

olum

ePH

(km

'x

10"1)

Con

duct

ivit

y(m

s m

"1)

Dis

solv

ed o

xyge

n O

rgan

ic c

arbo

n In

orga

nic

carb

onK

jeld

ahl

nitr

ogen

(mg

l"1)

Tot

al b

iom

ass

G«g

I"1)

Cil

iate

bio

mas

s

(MS

I"1

)

K6

M2

M4

M5

M6

M8

N4

N5

O5

6.5

4.7

4.8

44.2 2.6

32.3 0.7

II.3 4.0

7.73

6.59

5.35

7.08

5.54

6.82

5.17

6.28

8.40

16.9

4.3

4.0

6.8

3.8

10.1

4.2

5.0

23.5

8.2

10.2

9.0

11.2

9.4

13.7 9.7

10.3

9.5

8.3

6.0

4.9

4.5

4.7

4.6

5.1

5.4

6.8

17.1 1.2

0.4

2.6

0.3

2.4

0.4

1.1

22.0

0.33

0.18

0.32

0.21

0.21

0.33

0.33

0.32

0.40

1588

.012

83.4

928.

999

1.4

960.

015

58.0

1523

.199

7.7

2094

.5

140.

639

.926

.936

.176

.730

.747

.270

.889

.2

at Stanford Medical Center on October 7, 2012http://plankt.oxfordjournals.org/Downloaded from


Ciliated protozoa in Ontario lakes

30- n

K6 M2

30-

10-

_•_

J1

ILLN5

40-

30-

20-

10-

11

i r i r

10 20 30 40 50 60 10 20 30 40 50 60 10 20 30 40 50 60LENGTH ((jm)

Fig. 1. Distribution of ciliates by lengths for each lake, pooling all data from 1981.

values compare reasonably well with values (19.0 ml"1 and 8.6 ml"1) from theprevious summer (10 June and 23 September, respectively) collected by differentworkers with different apparatus (Taylor and Lean, 1981). The ciliate biomassdensity at 0 - 4 m in August, 1981 was only 8.1 fig I"1, compared to 52 /ig I"1 at2 m depth in September, 1980; however, Taylor and Lean (1981) deliberatelychose 2 m as one of their sampling depths because of the presence there of largenumbers of one of the largest planktonic ciliates. Thus, their discrete bottlesamples may represent upwardly biased values compared with integrated columnsamples. Nonetheless, the general agreement of our values with theirs is encour-aging and suggests that this estimation methodology is robust.

Table I presents seasonally averaged values for a variety of Umnological andbiomass parameters for the regularly sampled lakes. Temporal variations in thesephysico-chemical parameters are presented in Zimmerman et al. (1983). Most ofthe ciliates found in these Ontario lakes were small, with mean lengths in therange 18-24/tm. Figure 1 shows histograms of body length for all the ciliatesfound during the sampling season. Most lakes have similar histograms, withmodes in the size class centered at 15 fim, but for lakes M2 and N5, more ciliateswere slightly larger, resulting in a modal value of 20 urn. Some lakes had a sub-

447




ownloaded from


M.A.Gates ud U.T.Lewg

- 12-

- 9-

6-

1 9 7 8 1 9 7 9 1 9 8 0 1981

Fig. 2. Mean biovolumes of individual ciliates for lake K6 over four sampling seasons. Cycles corre-spond to comparable day-of-year dates in separate years. Solid lines represent 0—4 m samples; dashedlines are for 4 —8 m samples, which were only taken in 1980 and 1981.

sidiary mode at 35 /an, and one lake (O5), with the largest mean size, had a broadmode in the 32.5—47.5 /tm size range.

Lake K6 had the largest average ciliate biomass in 1981 (Table I), and this wasthe lake for which data were obtained from previous sampling seasons. Figure 2illustrates the changes in size (here expressed as mean biovolumes) that occurredthrough the sampling seasons for K6. There are no consistent trends in size fluc-tuations: in 1978 and 1979, the largest ciliates were found early in the summer,while in 1981 they were found later. In both 1979 and 1981, there were two peakperiods; in 1980, a peak in mean size occurred only in the 4 — 8 m sample. Thedata for 1981 suggest that there may be a consistent late summer biovolume peakat this depth, but further sampling will be required to verify whether in factciliates in this zone of K6 tend to be large only late in the summer. Similar latesummer biovolume peaks at 4 —8 m occurred in lakes M5, M8 and N5, while inlake M6, the peak occurred earlier in the summer (sampling cycle 3).

For lake K6, Figure 3 shows the temporal fluctuations in the relative contri-bution of mean ciliate biomass to the total planktonic biomass, which has beenbroken into four components: ciliates, edible phytoplankton, traditional zoo-plankton and inedible phytoplankton (the last is not plotted since it can be calcu-lated from the other three). This graph also illustrates trends which were seen inthe 1981 sampling season for all the lakes. First of all, ciliates can constitute anappreciable proportion of the total biomass. Although an unusually high numberof ciliates was found during 1981 in lake K6, ciliates usually constitute > 2 - 3 %of the total biomass throughout the summer, even in years of low ciliate density.Secondly, ciliate biomass densities fluctuate through the summer, usually show-ing two peak periods, one early in the sampling season, and one late. However,these fluctuations apparently are not directly related to fluctuations in the otherthree components: there are few consistencies in pattern with zooplankton andonly a slight tendency for edible phytoplankton and ciliates to peak at the same

448




ownloaded from


Ciliated protozoa In Ontario lakes

60

I 40o

20-

•vaWo

a ZOO

C I L

1 9 7 8 1 9 7 9 1 9 8 0 1981

Fig. 3. Mean relative biomass densities for lake K6 over four sampling seasons. The relative densitiesof the three illustrated components, plus the inedible phytoplankton, sum to 1.0. Edible phytoplank-ton (ED) is denoted by ovals; zooplankton (ZOO), by squares; and ciliates (CIL), by circles.

time. Furthermore, there are no consistent trends across these years in the phyto-plankton and zooplankton components themselves, either considered in isolationor together. Each year apparently is unique. Nonetheless, there is a good corre-spondence, in lake K6, between the total analytic concentration of phosphorus at0 —4 m and various measures of ciliate biomass in the same depth stratum:r2 = 0. 248, F1M = 6.6, p <0.05, for total ciliate biomass; r2 = 0.390, F120 =12.77, p <0.01, for ciliates as a proportion of the total planktonic biomass; andr2 = 0.237, FlK = 6.2, p <0.05, for ciliates as a proportion of non-inedibleplanktonic biomass (wherein the filamentous and largest spherical algal size classare excluded). In this lake, there also is a low but significant correlation (r2 =0.161, FliQ = 5.75, p <0.05) between ciliates as a fraction of the non-inedibleplanktonic biomass and the relative biomass proportion of edible algae (<30 /imsize classes) which are in the 2 — 5 /*m size class.

The temporal fluctuations in mean ciliate biomass density for all the lakes in1981 are shown in Figure 4. Although there is a fairly good correspondence be-tween the 0 — 4 m and the 4 — 8 m depth samples within each lake, this is far frombeing close — except for M2, which showed a decline in ciliate biomassthroughout the summmer, with only a weak peak late in the season. The lakes inthis study show an early peak in ciliate biomass; K6 is an exception, although ittoo sometimes has an early increase in ciliates (Figure 3). Several lakes had a sub-sidiary peak in late summer.

By averaging the temporal variations across the sampling season, the lakes maybe arranged in order of increasing mean ciliate biomass density. This is done inFigure 5, where the mean ciliate numerical densities are also given. This figuredemonstrates that there is no necessary correspondence between average numeri-cal and biomass densities, despite the relatively restricted size range of the ciliates.Although K6 had both the largest numbers and the largest biomass, lake M6, with

449




ownloaded from



100-

K6 M6 N 5 0 5

Fig. 4. Ciliate biomass densities in 1981. Solid lines indicate 0 - 4 m samples; dashed lines indicate4 - 8 m samples.

C I L I A T E s / m50 30 10

B I O M A S S («o 120 tao

Fig. 5. Mean numerical and biomass densities of ciliates in 1981. The standard errors of the means arealso indicated. The lakes are arranged from top to bottom in order of increasing mean ciliate biomassdensity.

a large amount of ciliate biomass, had one of the lower numerical densities. Overall the cycles throughout the sampling season in these lakes, however, there is ageneral and significant correspondence between numerical and biomass densities(r2 = 0.203, Fl1t = 29.97, p <0.001).

Using this same arrangement of the lakes, by mean ciliate biomass, Figure 6illustrates the relative contributions of the ciliates, edible and inedible phyto-

450




ownloaded from



I 50-O

30-

INEO

CARH

HERB

ED I iiI i i

i

IM8 M5 M2 N5 H6 0 5 K6

Fig. 6. Mean proportional allocation of planktonic biomass during 1981 for five compartments: CIL,ciliates; ED, edible phytoplankton; HERB, herbivorous zooplankton; CARN, carnivorous zooplank-ton; INED, inedible phytoplankton. The lakes are arranged from left to right in order of increasingmean ciliate biomass density.

plankton, and herbivorous and carnivorous zooplankton to the total planktonicbiomass. The general correspondence between increased absolute biomass andpercent relative contribution of ciliates is not uniform, and lake O5 is an import-ant exception; this lake had the second largest mean ciliate biomass (89.2 /tg 1~1),but ciliates constitute only 4.3% of the total, whereas in lake M4, for example,ciliates have their lowest absolute mean abundance (26.9 fig 1~*) and still contrib-ute 2.9% of the total. Mean ciliate contributions range from 2.0% in M8 to 8.9%inK6.

It is clear from Figure 6 that there is little correspondence between the relativecontributions of the different plankton components across the set of lakes, exceptthat the proportion of carnivorous zooplankton seems to be inversely related tothe proportion of edible phytoplankton. There is apparently no relation betweenedible and inedible phytoplankton, nor between herbivorous and carnivorous zo-plankton, and ciliates are not related strongly to any of the other components,except as noted above with respect to the 2 - 5 fim size class of algae.

Regression analyses of ciliate numerical and biomass densities against thecycle-by-cycle limnological parameters, of which the yearly means are shown inTable I, showed significant but weakly linear relationships with conductivity (r2

= 0.019, F176 = 9.30, p <0.01, for numbers; r2 = 0.131, Fl7S = 11.42, p<0.01, for biomass), and with the analytical concentrations of inorganic carbon(r2 = 0.115, F1>76 = 9.86, p <0.01, for numbers; r2 = 0.0146, F176 = 12.99,/?<0.001, for biomass), of Kjeldahl nitrogen (r2 = 0.056, F176 = 4.55, p <0.05,for biomass), and of phosphorus (r2 = 0.218, Fl 49 = 13.69, p <0.001, fornumbers; r2 = 0.086, F149 = 4.62, p <0.04, for biomass).

The differences among the lakes in their standing crop of ciliates in 1981 (TableI) are most strongly related to total analytic concentrations of inorganic (r2 =0.534, Fxj = 8.02, p <0.05) and organic {r* = 0.713, F1>7 = 17.46, p <0.01)carbon. There is no significant relationship, on a lake-by-lake comparison, withphosphorus concentration or with conductivity.

451




ownloaded from



Discussion

This is the first study to look simultaneously at planktonic ciliates, other zoo-plankton and phytoplankton. Previous work has been either taxonomic in scopeor restricted to a single lake, and none has quantitatively partitioned the biomassof the total plankton (excluding bacteria). There is only one other comparativestudy of ciliate biomass in a series of lakes (Beaver and Crisman, 1982). Further,there is only one study (based on a single lake) of relative biomass allocationamong plankton compartments, and in that study phytoplankton were excluded(Pace and Orcutt, 1981).

Beaver and Crisman (1982), in their study of 20 Florida lakes spanning a rangeof trophic levels, review previously published data on ciliates in lakes. The datafor Ontario lakes reported here generally agree (after taking into account differ-ing methods of estimation) with published values for ciliate numerical densitiesfor other temperate oligotrophic lakes (Gates, 1984) and for the oligotrophic sub-set of the Florida lakes. With total chlorophyll a concentrations in the epilimnionof 0.7 — 1.7 fig I"1 and phosphorus concentrations of 7 — 28 /tg I"1, and withmean Secchi depths of 3.4 — 8.4 m, the Ontario set of lakes span trophic state in-dices ([TSI(Chl)] of Carlson, 1977, used in Beaver and Crisman, 1982) of 27 to36. Use of phosphorus or Secchi depth in the index gives slightly higher values, upto 50, and quite different orderings of the lakes. Perhaps, therefore, some ofthese lakes can be considered somewhat mesotrophic (Carlson, 1977). But bysurveying the average values of the limnological parameters given in Table I, it isclear that these lakes would fit under the broad umbrella of oligotrophy.

Our biomass estimates are lower than for Beaver and Crisman's (1982) mostcomparable lakes, primarily because we have used an improved value for thevolume to wet-weight conversion constant that, at worst, underestimates trueciliate biomass. Beaver and Crisman (1982) use a specific gravity of 1.025, whilewe use 0.416, based on direct measurements for the ciliate Tetrahymena (Gates etal., 1982). Also, their method of volume estimation was based on unspecifiedgeometric formulae that yielded a table of estimated volumes for each taxonexamined. Their samples were scored for taxa, and the resulting abundances weremultiplied by the values for the volumes of the respective taxa. We have directlymeasured every ciliate and used a uniform geometric formula (for a prolate sphe-roid) throughout.

Our numerical densities (mean 23.5 ml"1) are higher than for their oligo-trophic subset of lakes (mean 10.8 ml"1) and fall in the range found in theirmesotrophic lakes (mean 27.5 ml"1). However, they are much lower than theirreported values for eutrophic lakes (mean 55.5 ml"1). The Florida lakes are, ofcourse, subtropical while these are northern temperate lakes. Furthermore, theirdata represent mean annual data from 12 months of sampling, while these datacorrespond only to the growing season.

All of the lakes are dominated by the smaller size classes (12- 17 /ig length),but here the modal lengths are less than those of the Florida lakes, which weredominated by ciliates of the size class 20-30/im. Also, we do not find, as Beaverand Crisman (1982) did, that large ciliates (40-50 /an) made a greater contri-

452




ownloaded from



bution to the more oligotrophic lakes. Using their trophic state index, the mostmesotrophic lakes (K6, N4, N5, O5) have the largest ciliates, and conversely, themost oligotrophic lakes (M2, M4, M5, M6) have ciliates with the smallest meansize (Table I and Figure 1).

Our results provide little evidence on the question of whether or not resourceoverlap exists between ciliates and large zooplankton (Crisman et ah, 1981;Beaver and Crisman, 1982). As shown in Figures 3 and 6, there are few consistenttrends, either within one lake over time or across lakes, with respect to the relativeallocation of biomass among phytoplankton, zooplankton and ciliates. We wereunable to find any dynamical relationship, based on biomass allocation, betweenciliates and zooplankton, either totally or any size classes that would be potentialpredators. This is in contrast to the situation with phytoplankton, where thereappears to be a significant correspondence between the relative amounts of small(2 -5 /tm) algal biomass (in the total edible algae) and the biomass of ciliates inthe total planktonic biomass. This size fraction presumably includes flagellates,which can constitute an important part of the diet of many planktonic ciliates(Corliss, 1979); the phytoplankton samples included both zooflagellates andphytoflagellates. In addition, we do have preliminary evidence that there is aninverse relationship between the biomass of the generally small, and presumablyprimarily bactivorous, ciliates and bacterial biomass for a subset of lakes thatwere monitored for bacteria (Dalziel and Gates, in preparation).

Although there is a general and significant correspondence between ciliates(numbers or biomass) and certain nutrient-related parameters such as conduc-tivity and the concentrations of inorganic carbon and phosphorus, as well ascertain biomass indicators such as organic carbon and organic nitrogen, thatcorrespondence is not strongly linear. Furthermore, inspection of the detailedtemporal patterns for each lake reveals that this pattern is also not directly causal,even in lake K6, where there is a strong relationship between phosphorus concen-tration and ciliate biomass. The lack of linearity in the relationship is not surpris-ing, in view of the small absolute contribution of ciliates to planktonic biomass.

The only comparable quantitative study of relative biomass allocation is that ofPace and Orcutt (1981), which was based on a man-made eutrophic lake inGeorgia, and which did not consider phytoplankton. They found that ciliates andamoebae together comprised 15 — 62% of the summer zooplankton biomass. Inthis set of relatively oligotrophic Ontario lakes, ciliates comprise 5 — 22% (meanacross lakes, 11.2%) of the total zooplankton biomass (including ciliates), aver-aged over the ice-free period.

Our quantitative estimates of the contribution of ciliated protozoa to the totalplankton system of lakes are based on a series of Ontario lakes spanning severalphysiographic regions. We suggest, therefore, that ciliates constitute a quantitat-ively important component of the plankton of freshwater ecosystems. In this lakeset ciliates comprise, on average, ~ 10% of the non-algal biomass and ~ 5 % ofthe total planktonic biomass (excluding bacteria). Fluctuations in ciliate biomassare significantly related across lakes to total carbon content of the water column,but within lakes to seasonal variations in conductivity and in total phosphorusand inorganic carbon concentrations.

453




ownloaded from


M.A.Gates and U.T.Ltwg

Most planktonic ciliates are particle feeders, grazing on bacteria and smallplankters such as algae, zooflagellates and blooms of smaller ciliates. Little isknown of the predation to which they themselves are subject (Robertson, 1983) orif they are an essential component of the planktonic ecosystem (Banse, 1982).However, their universal presence and not insignificant contribution to plank-tonic biomass suggests that they may indeed fulfill the crucial role that theirpotential nutrient-recycling ability indicates.

The significant relationship between ciliate biomass across lakes (and, ingeneral, total planktonic biomass, Gates et al., 1983) and an overall productivitymeasure (total carbon), as well as the significant correlation within lakes betweenciliate dynamics and the dynamics of other productivity measures (total phos-phorus, total inorganic carbon), and the general relationship between lake eu-trophication and bacterial production, all suggest that ciliates may be moststrongly responding to bacterial prey densities. Therefore, it may be of value toadvance the hypothesis that the primary role of ciliates in the plankton is as con-sumers of bacteria. Their major competitors in this function probably arerotifers, which possess a similar size range and similar trophic apparati. Bothciliates and rotifers are most probably prey for the larger zooplankters which arecommonly detected in 'plankton nets' whose relatively large mesh the ciliates androtifers themselves passively elude.

Tests of this hypothesis require assessment of the relative quantitative contri-butions of bacteria and nannoplankters to ciliate diets, competition studies be-tween ciliates and rotifers for planktonic bacterial prey species, and comparativepredation studies of zooplankton feeding on bacteria, algae, rotifers and ciliates.As well, there remain the difficult problems of estimating bacterial and ciliateproductivity in the field and determining their relationships to each other asfunctions of limnological parameters.

Acknowledgements

We thank Rob Graham for competent technical assistance, and Bill Taylor forunpublished data, much advice, and encouragement. R.Knoechel provided thephytoplankton data; W.G.SpruIes, the zooplankton data; and A.P.Zimmerman,the water chemistry and general limnological data. We are grateful to A.P.Zim-merman for helpful comments. This study was supported by the Natural Sciencesand Engineering Research Council of Canada, through grant U0090 to M.Gatesand by a subgrant from a Cooperative grant to J.E.Paloheimo, N.C.Collins,H.H.Harvey, R.Knoechel, H.A.Regier, W.G.SpruIes, and A.P.Zimmerman.

References

Bamforth.S.: 1958, 'Ecological studies on the planktonic protozoa of a small artificial pond', Limnol.Oceanogr., 3, 398-412.

Banse.K.: 1982, 'Cell volumes, maximal growth rates of unicellular algae and ciliates, and the role ofciliates in the marine pelagjaT, Limnol. Oceanogr., 27, 1059-1071.

Bark,A.W.: 1981, "The temporal and spatial distribution of planktonic and benthic protozoan com-munities in a small productive lake', Hydrobiologia, 85, 239-255.

Beaver,J.R. and Crisman.T.L.: 1982, 'The trophic response of ciliated protozoans in freshwaterlakes', Limnol. Oceanogr., 27, 246-253.

454




ownloaded from



Buechler.D.G. and Dillon.R.D.: 1974, 'Phosphorus regeneration in freshwater Paramecia', J. Proto-zool., 21, 339-343.

Carlson,R.E.: 1977, 'A trophic state index for lakes', Limnol. Oceanogr., 22, 361-369.Corliss.J.O.: 1979, 'The ciliated Protozoa: characterization, classification, and guide to the litera-

ture', 2nd edition, published by PeTgamon Press, London, UK, 455 pp.Crisman.T.L., Beaver.J.R. and Bays.J.S.: 1981, 'Examination of the relative impact of micro-

zooplankton and macrozooplankton on bacteria in Florida lakes'. Int. Ver. Theor. Angew.Limnol. Verh., 21, 359-362.

Davis,C.C.: 1973, 'A seasonal quantitative study of the plankton of Bauline Long Pond, a New-foundland lake', Naturaliste Can., 100, 85-105.

Finlay.B. J.: 1980, 'Temporal and vertical distribution of ciliophoran communities in the benthos of asmall eutrophic loch with particular reference to the redox profile', Freshwat. Biol., 9, 45-53.

Finlay.B. J.: 1981, 'Oxygen availability and seasonal migrations of ciliated protozoa in a freshwaterlake', J. Gen. Microbiol., 123, 173-178.

Gates,M.A.: 1984, 'Quantitative importance of ciliates in the planktonic biomass of lake ecosystems',Hydrobiologia, 108, 233-238.

Gates,M.A., Rogerson.A. and Berger.J.: 1982, 'Dry to wet weight biomass conversion constant forTetrahymena elliottC, Oecologia, 55, 145-148.

Gates,M.A., Zimmerman,A.P., Sprules.W.G. and Knoechel.R.: 1983, 'Planktonic biomasstrajectories in lake ecosystems', Can. J. Fish. Aquat. Sci., 40, 1752-1760.

Goulder.R.: 1972, 'The vertical distribution of some ciliated Protozoa in the plankton of a eutrophicpond during summer stratification', Freshwat. Biol., 2, 163-176.

Hecky.R.E. and Kling.H.J.: 1981, 'The phytoplankton and protozooplankton of the euphotic zoneof Lake Tanganyika: species composition, biomass, chlorophyll content, and spatio-temporal dis-tribution', Limnol. Oceanogr., 26, 548-564.

Hecky.R.E., Fee.E.J., Kling.H. and Rudd.J.W.: 1978, 'Studies on the planktonic ecology of LakeTanganyika', Can. Fish. Mar. Sen*. Tech. Rep., 816, 51pp.

Johannes,R.E.: 1965, 'Influence of marine Protozoa on nutrient regeneration', Limnol. Oceanogr.,10, 434-442.

Knoechel.R. and Kalff.J.: 1976, 'Track autoradiography: a method for the determination of phyto-plankton species productivity', Limnol. Oceanogr., 21, 590-596.

Mamaeva.N.V.: 1976, 'Planktonic ciliates in the Ivan'kovsky Water Reservoir', Zool. Zh., 55, 657-664.

Nauwerck.A.: 1963, 'Die Beziehungen zwischen Zooplankton und Phytoplankton im See Erken',Symb. Bot. Upsal., 17, 163 pp.

Ontario Ministry of the Environment: 1981, 'Outlines of Analytical Methods', Ontario Ministry ofthe Environment, Toronto, Canada, 246 pp.

Pace.M.L.: 1982, 'Planktonic ciliates: their distribution, abundance and relationship to microbial re-sources in a monomictic lake', Can. J. Fish. Aquat. Sci., 39, 1106-1116.

Pace.M.L. and Orcutt.J.D., Jr.: 1981, 'The relative importance of protozoans, rotifers and crus-taceans in a freshwater zooplankton community', Limnol. Oceanogr., 26, 822-830.

Porter.K.G., Pace.M.L. and Battey.J.F.: 1979, 'Ciliate protozoans as links in freshwater planktonicfood chains', Nature, TH, 563-565.

Rigler.F.H., MacCallum.M.E. and Roff.J.C: 1974, 'Production of zooplankton in Char Lake, J.Fish. Res. Board Can., 31, 637-646.

Robertson,J.R.: 1983, 'Predation by estuarine zooplankton on tintinnid ciliates', Estuar. Coast. ShelfSci., 16, 27-36.

Sorokin.Y.I. and Paveljeva.E.B.: 1972, 'On the quantitative characteristics of the pelagic ecosystemof Dalnee Lake (Kamchatka)', Hydrobiologia, 40, 519-552.

Sprules.G.W. and Holtby.L.B.: 1979, 'Body size and feeding ecology as alternatives to taxonomy forthe study of limnetic zooplankton community structure', J. Fish. Res. Board. Can., 36, 1354-1363.

Sprules.G.W. and Knocchel.R.: 1983, 'Lake ecosystem dynamics based on functional representationof trophic components', in Myers.D.G. and Strickler, J.R. (eds.), Trophic dynamics of aquatic eco-systems, American Association of Advanced Science, Washington, DC, USA, in press.

Taylor,W.D. and Lean.D.R.S.: 1981, 'Radiotracer experiments on phosphorus uptake and release bylimnetic microzooplankton'. Can. J. Fish. Aquat. Sci., 38, 1316-1321.

Wilbert.N.: 1969, 'Okologische untersuchung der Aufwuchs- und Plankton-ciliaten eines eutrophen

455




ownloaded from



Weihers', Arch. Hydrobiol. Suppl., 35, 411-518.Zimmerman.A.P. and Harvey,H.H.: 1979, 'Sensitivity of the waters of Ontario to acidification',

Final report to Ontario Hydro, Toronto, Canada, 114 pp.Zimmerman.A.P., Noble.K.M., Gates,M.A. and Paloheimo.J.E.: 1983, 'Physico-chemical ty-

pologies of south-central Ontario lakes', Can. J. Fish. Aquat. Sci., 40, 1788-1803.

456




ownloaded from


contribution of ciliated protozoa to the planktonic biomass in a series of ontario lakes:...

Documents