Changes in the zooplankton of Onondaga Lake (NY), 1969–1978

Environmental Pollution (Series A) 23

(1980)131-152

CHANGES IN THE Z O O P L A N K T O N OF O N O N D A G A LAKE (NY), 1969-1978

MICHAEL A. MEYER & STEVEN W. EFFLER

Department of Civil Engineering, Syracuse University, 150 Hinds Hall, Syracuse, NY 13210, USA

ABSTRACT

The zooplankton of polluted, hypereutrophic Onondaga Lake (located in metropolitan Syracuse, NY) were reinvestigated during 1978 to identify changes in the community since 1969. The reduction in large daphnids since 1969 has been attributed to size-selective predation by the obligate planktivore, Alosa pseudoharengus, which has become re-established in the lake. A I0- to 20-fold increase in zooplankton biomass has occurred since 1969, which may have been in response to changes in phytoplankton composition and~or reductions in metal pollution resulting from lake reclamation efforts. Increases in grazing on phytoplankton,phytoplankton turnover rates and nutrient recycling are implied by the elevated levels of zooplankton biomass. These zooplankton-phytoplankton interactions may be critical to future reclamation efforts directed at reducing external nutrient loading and primary productivity.

INTRODUCTION

The zooplankton community is composed of a diverse assemblage of organisms which form a critical intermediate link between the primary producers and the higher consumers. Aquatic ecosystems have frequently been perturbed by the addition of (1) nutrients which stimulate phytoplankton production, (2) toxic substances or (3) exotic fishes. Zooplankton respond quickly to such environmental changes and can thereby be sensitive indicators (Gannon & Stemberger, 1978) and integrators (McNaught & Buzzard, 1973) of subtle changes in water quality and fish predation. In this paper we report on a comprehensive zooplankton study of polluted hypereutrophic Onondaga Lake, New York State, USA, conducted in 1978, 131 Environ. Pollut. Ser. A. 0143-1471/80/0023-0131/$02.25 © Applied Science Publishers Ltd, England, 1980 Printed in Great Britain

132

M I C H A E L A. MEYER, STEVEN W . E F F L E R

particularly in comparison with an earlier (1969) study (Waterman, 1971). Since the 1969 study, substantial changes in the lake's pollutant concentrations and phytoplankton composition have Occurred in response to reclamation efforts. Moreover, the obligate planktivore alewife, A Iosa pseudoharengus, has become reestablished. Changes in the zooplankton since 1969 are evaluated with respect to these perturbing influences and their comparative role in certain aspects of ecosystem dynamics. In addition, the 1978 results serve to establish a new baseline for further zooplankton changes that may occur in response to ongoing reclamation efforts.

D E S C R I P T I O N OF S T U D Y SYSTEM

General Onondaga Lake is located within metropolitan Syracuse, New York. This small (11.7 km 2) lake is one of the most polluted in the northeastern United States, '... so polluted as to make Lake Erie look like an unblemished gem by comparison' (Stewart, 1979). A map of the lake, including significant sources of impact, is shown in Fig. 1. The lake's morphometric features are summarised in Table 1. The lake has

ONONDAGA

Drainage basin area Lake surface area Lake volume Mean depth M a x i m u m depth Shoreline length

TABLE 1 MORPHOMETRIC FEATURES

LAKE

600 km 2 11.7 km 2 1.405 x 10 s m 3 12.0 m 20.5 m 17.9 km

received the domestic effluents and much of the industrial wastes from the metropolitan area for more than a century. A comprehensive baseline limnological survey of the lake was carried out in 1969 (Onondaga County, 1971), with particular emphasis on the assessment of the impact of pollution. The lake was found to be dimictic, although circulation is impeded by the high salt content (Table 2) that occurs as a result of the effluent from a soda ash manufacturer. The lake's most conspicuous problem is hypereutrophy, which manifests itself in a number of ways including (1) extensive periods of anoxia with the hypolimnion, (2) very high standing crops of algae (chlorophyll-a as high as 150/~g/litre), (3) low water transparency (Secchi disc < 1 m), (4) dominance of chlorococcalean green and blue-green algae and (5) high concentrations of algal macronutrients (PO~, NO~-,NH~-,CO2), even during algal blooms (Onondaga County, 1971). Based on the absence of typical time lags between phytoplankton and zooplankton temporal distributions, it was concluded that the interaction between the

LAKE OUTLET

CREEK

Fig. I.

N

20 19 17

METROPOLITAN SYRACUSE SEWAGE TREATMENT PLANT

m

ONONDAGA CREEK

(1) ROUTINE MONITORING SITE I CONTOURS IN METERS

I

" ; ~ HARBOR BROOK DISCHARGE FROM TWO OuTLETE STEEL MANUFACTURING FOR THERMAL DISCHARGE PLANT O F S O D A ASH MANUFACTURING PLANT

SOUTH

LEY CREEK

/ L E Y CREEK /TREATMEN1 PLANT

0.5 km Onondaga Lake, with sampling locations and point source discharges shown.

SODA ASH MANUFACTURING PLANT WASTE B OVERFLOW

NINE MILE CREEK

BROOK

)DY

m

MICHAEL A. MEYER, STEVEN W. EFFLER

134

TABLE 2 SELECTED O N O N D A G A LAKE P O L L U T A N T CONCENTRATIONS

(seasonal averages) Parameter (#g/litre)

1969" Ed

Curot,i

50

CUFiltered

.

CrFiltered

.

Crrotal

ZnrotaI ZnFiltered

Ca ÷ ÷ ( × 103)

1975~ H"

E

40 .

20 .

.

60 .

605

25

23 .

828

5

26 .

3

-.

H

--

--

7"7 (4-11)

345

(2.6-8.1) 39.5 (9-76.5)

-.

426

1400

1700

1250

1500

Na ÷ ( x 103)

555 1700 800

670 2500 1500

373 240 150

446 540 430

PC)+ (as P)

.

E

5

CI- ( × 103)

Pvotal

.

.

60 .

1978" H

.

.

520 (400-640) 1150 (800-1500) 487 ---

6"1 (4"4-7"7) 4

(2.5-5.5) 28.9 (7.5-55-5) 665 (580-750) 1550 (1300-1800) 565 ---

a From Onondaga County (1971). bFrom Onondaga County (1976). c From Seeger (1979). a Epilimnion. e Hypolimnion. p h y t o p l a n k t o n a n d the z o o p l a n k t o n was less i m p o r t a n t in d e t e r m i n i n g the a b u n d a n c e o f either g r o u p t h a n were o t h e r e n v i r o n m e n t a l c o n d i t i o n s acting s i m u l t a n e o u s l y on b o t h c o m m u n i t i e s ( W a t e r m a n , 1971; Sze & K i n g s b u r y , 1972). F o l l o w i n g the baseline study, a lake r e c l a m a t i o n p r o g r a m m e was initiated which has included (1) increased sewer m a i n t e n a n c e t h a t resulted in substantial r e d u c t i o n s in d r y w e a t h e r l o a d i n g s f r o m t r i b u t a r y streams (1972), (2) the e s t a b l i s h m e n t o f a regional b a n on high p h o s p h a t e detergents (1972), (3) the r e d u c t i o n o f heavy metal inputs by the c o n s t r u c t i o n o f a t r e a t m e n t p l a n t (1976) to treat the steel mill effluent and (4) the c o n s t r u c t i o n o f a t e r t i a r y sewage t r e a t m e n t p l a n t (1980) that replaced a p r i m a r y t r e a t m e n t p l a n t which h a d been a m a j o r source o f p o l l u t a n t s ( O n o n d a g a C o u n t y , 1979). Onondaga Lake pollutants

T a b l e 2 shows d a t a for selected p o l l u t a n t s within the lake for 1969, 1975 a n d 1978. The high c o n c e n t r a t i o n s o f metals, salts a n d p h o s p h o r u s originate a l m o s t entirely from i n d u s t r i a l a n d d o m e s t i c w a s t e w a t e r p o i n t sources ( O n o n d a g a C o u n t y , 1971, 1979) a n d reflect a grossly p o l l u t e d c o n d i t i o n . S u b s t a n t i a l r e d u c t i o n s in p h o s p h o r u s a n d heavy metal p o l l u t i o n resulted from the d e s c r i b e d r e c l a m a t i o n efforts. T h e p o l l u t e d c o n d i t i o n with respect to the high salt ( C I - , N a ÷ a n d Ca ÷+ ) c o n c e n t r a t i o n s has r e m a i n e d essentially u n c h a n g e d since the baseline study. Since

ZOOPLANKTON OF ONONDAGA LAKE (USA)

135

most of the information on zooplankton tolerance to salts is based on salinity, it is convenient to estimate the lake's salinity by the following expression, based on

[El-I: S%o = 0.030 + 1.86 x 10 -3 [CI-] (APHA, 1975)

(1)

where: S%o = predicted salinity in ppt, [CI-] = chloride ion concentration in mg/litre. During the warm weather stratification period (mid-April to mid-October) the chloride content of the epilimnion varies between 800 and 1500 mg/litre (due to the approximately constant industrial loading combined with the seasonal variability in the lake's flushing rate). This corresponds to a salinity range of 1-5-2.7, which is classified as an oligohaline environment (Remane & Schleeper, 1971). The elevated Ca ++ levels resulting from pollution are largely responsible for the highly supersaturated state of the lake with respect to CaCO3, which results in the formation of'whitings' (calcium carbonate aggregates). The lake remains anaerobic below 10 m for much of the year. Large variations in the dissolved oxygen levels of the epilimnion are typical due to the elevated levels of algal biomass within the system (Field et al., 1979). Night-time dissolved oxygen minima of less than 3mg/litre are common (Field et al., 1979). In addition, dramatic algae die-offs occasionally occur (Sze, 1975) which reduce surface dissolved oxygen levels to as low as 0.5 mg/litre.

Phytoplankton assemblages and the alewife, 1969 and 1978 The phytoplankton assemblages of 1969 and 1978 are summarised in Table 3 and Fig. 2. The most conspicuous change since 1969 has been the loss of blue-green (particularly the N2-fixing ) forms, which was apparently in response to reduced phosphorus loadings associated with a ban on high phosphate detergents in 1972 (Murphy, 1973; Sze, 1975). Similar losses of N2-fixing blue-green algae have been observed for other systems following increases in the nitrogen/phosphorus ratio (Schindler, 1977; Gelin & Ripl, 1978). Since 1972, the phytoplankton of Onondaga Lake have become more diverse, although the total phytoplankton biomass has not changed significantly since 1969 (Meyer, 1979). Certain blue-green algae common to Onondaga Lake in 1969, including Microcystis aeruginosa, Anabaenaflos-aqua and Aphanizomenon flos-aqua, and the green alga, Chlorella vulgaris, are among some of the most prominent freshwater algae capable of eliciting toxic responses from aquatic organisms under bloom conditions (Hughes et al., 1958; Gorham, 1960, 1964; Gentile & Maloney, 1969). Only Chlorella vulgaris remained common to the lake in 1978 (Onondaga County, 1979). Previous to the baseline study, Dence (1956) noted that the alewife was common to Onondaga Lake. However, a rather extensive fish survey, conducted as part of the baseline study (Onondaga County, 1971), found it to be absent. Later less extensive surveys by the New York State Department of Environmental Conservation (pers.

136

MICHAEL A. MEYER, STEVEN W. EFFLER TABLE 3 ONONDAGALAKEPHYTOPLANKTON, 1969 AND 1978 1969

1978

Cyanophyta Myxophyceae Microcystis aeroginosa Aphanizomenon flos-aqua Anabaena flos-aqua" Anabaena circinalis a

Chrysophyta Bacillariophyceae Cyclotella glomerata Cyclotella spp. Diatoma tenue a Synedra spp. Asterionella formosa" Amphipora alata ° Nitzschia palea a

Chrysophyta Bacillariophyceae Diatoma tenue Melosira granulata Chlorophyta Chlorophyceae Chlamydomonas sp. Chlorella vulgaris Scenedesmus obliquus Scenedesmus quadricauda

Chlorophyta Chlorophyceae Chlamydomonas spp. Schroederia setigera" Pediastrum duplex ° Chlorella oulgaris Oocystis parva Ankistrodesmus falcatus Scenedesmus obliquus Scenedesmus quadricauda Actinastrum hantzschii ° Cryptophyceae Cryptomonas sp. Chromonas sp. Euglenophyta Euglena proxima °

Cryptophyceae Cryptomonas sp.

° Rare species.

comm.) and personal observations by the second author of high mortality periods for the alewife (typical of the alewife in freshwaters (Dence, 1956)) in the period 1976-1979, indicate that the alewife has again become common to the lake.

METHODS

To facilitate comparative evaluations, the sampling procedures used in 1978 were designed to duplicate the sampling scheme of 1969 (Waterman, 1971). Zooplankton were sampled two to three times a week, depending on the general productivity level, from ice out in April to autumn turnover in late October. Only weekly data are shown as results, except where the higher frequency information depicts additional

ZOOPLANKTONOF ONONDAGALAKE(USA)

'oo I

137

1

901 -

~o r 2Ol,oF APR

MAY

~°°1

1~

i ca-

f#j~

9o I -

JUNE

JULY 1969

AUG

SEPT

OCT

I-'---] GREENS DIATOMS BLUE-GREENS W

CRYPTOMONADS

84ota 5 0 y 20-

'° I APR

MAY

,~2'ol ,bzb L ,;io I ,;~01 ,;I JUNE

JULY 1978

AUG

SEPT

OCT

Fig. 2. Phytoplanktonassemblagesfor OnondagaLake, 1969and 1978,per centcontributionby cell volume.

trends. Vertical net hauls were taken from 10 m to the surface, with a 12 cm diameter No. 20 mesh Wisconsin-style plankton net, at the deepest sites of the north and south basins (Fig. 1). For most of the sampling period this depth interval included the oxygenated layers, and at times as much as 2 m of the anoxic zone. Samples were preserved with 4 % formalin. The zooplankton were enumerated at 30 x , using a Bogarov counting tray (Gannon, 1971). At least 200 individuals of the major forms were counted in each sample. The zooplankton were identified to species using keys by Edmondson (1959) and Brooks (1957), with reference to Pennak (1953) and Gannon (1970). Due to the lack of significant differences between the north and south sites (Meyer, 1979) the average of the two sites is presented. In addition, a number of intermediate (1970-1975) net haul samples, obtained in a similar fashion by other investigators, were qualitatively reviewed.

138

MICHAELA. MEYER, STEVENW. EFFLER RESULTS

Data from the 1969 study (Waterman, 1971) are presented with the 1978 results to illustrate the changes which have occurred in that period. Little change in microcrustacean occurrence has been evident since 1969 (Table 4). Waterman (1971) had originally noted the occurrence of D a p h n i a similis, but re-examination of available samples from 1970 indicates that this form was almost certainly misidentified D a p h n i a p u l e x . Comparison of rotifer occurrence for the two years is difficult because of incomplete speciation of these forms performed in 1969 (Waterman, 1971). TABLE4 ZOOPLANKTONOCCURRENCEIN ONONDAGALAKE,1969 AND 1978 1969 °

Cladocera Bosmina Iongirostris ~ Ceriodaphnia quadrangula Chydorus sphaericus b Daphnia pulex

Copepoda Cyclops bisucpidatus thomasi Cyclops vernalis Diaptomus sicilis b Mesocyclops edax b

Rotifera Asplanchna sp) Brachionus sp. Filinia Iongiseta b Keratella cochlearis b Keratella hiemalis Polyarthra sp.

Unidentified rotiferb

1978

Cladocera Aloha affinis b Bosmina Iongirostris b Ceriodaphnia quadrangula Chydorus sphaericus b Daphnia pulex

Copepoda Cyclops bicuspidatus thomasi Cyclops vernalis Diaptomus sicilis b

Rotifera Asplanchna sp. Brachionus sp. Brachionus calyciflorus Brachionus pl&atilis b Filinia longiseta b Keratella hienalis Keratella quadrata Keratella valga b Polyarthra sp. Synchaeta sp.

Unidentified Bdelloidea

aFrom Waterman (1971). bRare forms. The changes in the populations of individual crustaceans from 1969 are dramatic (Fig. 3). The number of large daphnids (D. p u l e x ) has decreased substantially since 1969. In 1969 the average number ofD. p u l e x (including the misidentified D. similis) per 100 litres was more than 1000 in the summer and autumn while, in 1978, their number was less than 100 per 100 litres, for the same time period. Qualitative inspection of intermediate net hauls indicates that the average size of D. p u l e x has

Z O O P L A N K T O N OF O N O N D A G A

LAKE (USA)

139

9

:t °

t

b

75

_-

,978

72 69 66 63 60 57 54 51 48

~ 45 ~

42 39

r

,

'

i

33 3o c3 27 24 21 18 15 12 9 6 3

APRIL

MAY

JUNE

JULY

AUG.

SEPT

OCI

Fig. 3. Seasonal epilimnetic populations of Ceriodaphnia quadrangula (-O-C)-) and Cyclops vernalis adults and copepodids ( - A - A - ) in Onondaga Lake: (a) 1969, and (b) 1978; (c) Large daphnids in epilimnion of Onondaga Lake, 1969 and 1978.

140

MICHAEL A. MEYER,STEVEN W. EFFLER

3.0

-,,e- LARGE DAPHNIDS1969 LARGE DAPHNIDS 1978

tC ~

--~

~ I~

|

2.0

"f

~ ~.o

i o.o ,~ 2b I ,'o~o'~-,~o~o -'r' I ,b2b J ,b~o ~ f ,; ~o I ,b APRIL

MAY

JUNE

JULY

AUG

SEPT

OCT

Fig. 3. --contd.

decreased since the early 1970s and that the trend has been progressive. The dramatic increases exhibited in the populations of the smaller crustaceans, Cyclops vernalis and Ceriodaphnia quadrangula (Fig. 3) since 1969 are particularly striking. The great increase in these two forms has resulted in an estimated ten- to twenty-fold increase in total zooplankton biomass (Fig. 4), based on individual weights obtained from the literature (Table 5). Although rotifers were common smaller zooplankters in both 1969 and 1978, they contributed significantly to total zooplankton biomass only in the early spring of both years. DISCUSSION A large number of ecosystem conditions can affect zooplankton composition and biomass. Several notable ecosystem changes have occurred since 1969 which potentially influenced the dramatic changes in the lake's zooplankton population, including (1) reductions in water column copper and chromium concentrations, (2) loss of the blue-green algae as major components of the phytoplankton and (3) reestablishment of the alewife. The following discussion will address (1) possible relationships between the above ecosystem changes and the parallel zooplankton changes, (2) some features of the lake's continuing polluted condition as they may affect zooplankton occurrence and condition and (3) several potential implications of the greatly increased zooplankton biomass with respect to the primary productivity of the lake. Zooplankton response to ecosystem changes since 1969 Heavy metals in both the cationic (Biesinger & Christensen, 1972) and soluble complex form (Andrews et al., 1977) can be toxic to, or inhibit, zooplankton.

141

ZOOPLANKTON OF ONONDAGA LAKE (USA)

1969

"~

b

0 . 9 -

0.8

(36

0.5

0.4

0.3

0.2

0.1

~-~i

~

I

'

I

tO 20 MAY

Fig. 4.

'

,

r'

l

f I0 20 CLAD JUNE

rT

'

1

I

'

I ~

I0 20 JULY 1978

•

I

'

t

I0 20 AUG,

1

- ~ l - ' -

I0 20 SEPT

1

10 20 OCT

Estimated seasonal epilimnetic zooplankton biomass in Onondaga Lake. (a) 1969 and (b) 1978.

Unfortunately, the information on the toxicity of various heavy metal forms to specific zooplankton species is very limited. The lack of segregation between total and dissolved (filtered, 0.45/~m) heavy metal fractions in earlier analyses on Onondaga Lake (Table 2) further confounds interpretations concerning the possible effect decreases in total heavy metal concentrations may have had on the noted changes in zooplankton. Acute and chronic toxicity, and reproductive impairment data for Daphina magna due to selected cations (note chromium ion(s) were not

MICHAEL A. MEYER, STEVEN W. EFFLER

142

TABLE 5 A V E R A G E D R Y WEIGHI?S F O R T H E C O M M O N Z O O P L A N K T O N O F O N O N D A G A LAKE

Organism

Dry weight

Reference

(~g)

15.41 6.4 8.6 6.8 3.0 1.0 x 10 -2 3.0 5.7 x 10- l 5.0 x 10 -3 5.0 x 10-3 3-0 x 10 - l I-0 x 10-1

Daphnia pulex Ceriodaphnia quadrangula Cyclops vernalis Cyclops bicuspidatus thomasi Cyclopoid copepodids Cyciopoid nauplii Asplanchna sp. Brachionus calycifloris Keratella hiemalis Keratella quadrata Synchaeta sp. Polyartha sp.

Dumont et al. (1975) Dumont et al. (1975) Hall et al. (1975) Dumont et al. (1975) Hall et al. (1970) Hall et al. (1970) Nauwerck (1963) Comita (1972) Hall et al. (1970) Hall et al. (1970) Dumont et al. (1975) Comita (1972)

included), are shown in T a b l e 6 (Biesinger & Christensen, 1972). A s s u m i n g that the sensitivity o f O n o n d a g a L a k e z o o p l a n k t o n m a t c h e s t h a t o f Daphnia m a g n a , c o p p e r i m p a c t in 1969 c a n n o t be ruled out. M c I n t o s h & K e v e r n (1974) r e p o r t a 96-h TI_~ value o f 0.096 mg/litre filtered c o p p e r for D a p h n i a p u l e x . C y c l o p o i d c o p e p o d s , including C y c l o p s vernalis, were f o u n d to be s u b s t a n t i a l l y m o r e t o l e r a n t t h a n the c l a d o c e r a n s to c o p p e r ( M c I n t o s h & K e v e r n , 1974). Based on the relative success o f the c l a d o c e r a n s in 1969, a n d the t e n d e n c y o f c o p p e r to b e c o m e i n o r g a n i c a l l y (Syiva, 1976) a n d o r g a n i c a l l y ( S h u m a n & W o o d w a r d , 1977) b o u n d in n o n - t o x i c forms, it is unlikely that acute o r c h r o n i c toxicity w o u l d result f r o m the levels o f total c o p p e r f o u n d in the lake in 1969. M o r e p r o b a b l e w o u l d be subtle negative i m p a c t s such as the i m p a i r m e n t o f r e p r o d u c t i v e processes, a s s o c i a t e d with lower levels o f a v a i l a b l e c o p p e r . The lack o f previous studies d e s c r i b i n g c h r o m i u m toxicity to z o o p l a n k t o n prevents the e v a l u a t i o n o f the effect r e d u c t i o n s o f this p o t e n t i a l toxin m a y have had. T h e b l u e - g r e e n algae m a y have influenced the relatively lower z o o p l a n k t o n p o p u l a t i o n observed in 1969, d u r i n g the p e r i o d in which they were c o - d o m i n a n t (Fig. 2), b y eliciting i n h i b i t o r y responses, o r d u e to their u n s u i t a b i l i t y as f o o d .

TOXICITY TO

Ions (lag/litre)

Cu +2 Zn +2 Ca +2 Fe +3 Pb +2 Hg +2 Cd +2

TABLE 6 Daphnia magna F R O M

Acute (48 h < LCso )

VARIOUS CATIONSa

16 % reproduction impairment

60 280 464000 9600 45 ° 5 65

a From Biesinger & Christensen (1972).

22 70 116000 4380 30 3"4 0"17

Chronic (3 wk < LCso )

44 ! 58 330000 5900 300 13 5

ZOOPLANKTON OF ONONDAGA LAKE (USA)

143

Gentile & Maloney (1969) found a wide range of sensitivity for microcrustaceans exposed to the toxin released from Aphanizomenon flos-aqua, although their experimental concentrations of A.flos-aqua exceeded those observed in Onondaga Lake (Sze & Kingsbury, 1972) by an order of magnitude. Arnold (1971) found that several species of blue-green algae showed some toxicity or inhibition to Daphnia pulex. Non-toxigenic strains of algal species identified as capable of eliciting toxicity generally exist (Gorham, 1960). A number of investigators have found blue-green algae to be of little or no food value to herbivorous planktivores (Edmondson, 1965; Schindler, 1968; Sorokin, 1968; Arnold, 1971 ; InFante, 1978). Zooplankton-blue-green algae interactions have been ignored (i.e. assumed no food value derived from blue-greens by zooplankton) in a number of successful mechanistic mathematical models of lake primary productivity, while interactions with other algal forms were found to be critical to the effective prediction of phytoplankton growth and standing crop (Bierman, 1976; Canale et al., 1976; DePinto et al., 1976). The alewife, a size-selective planktivore, first selects large daphnids, then large copepods (Brooks & Dodson, 1965; Brooks, 1968). As the larger zooplankton become depleted, the alewife often consumes progressively smaller zooplankton (Brooks & Dodson, 1965; Brooks, 1968; O'Brien, 1979). This size selectivity has been demonstrated in a number of lakes (Brooks & Dodson, 1965; Wells, 1970; Hutchinson, 1971 ; Gannon, 1976). Most of the egg-producing individuals of the two co-dominant microcrustaceans of Onondaga Lake were in a size range ( < 1.0 mm) generally not pressured by the alewife (Brooks & Dodson, 1965; Wells, 1970). Moderate successes in avoidance by Cyclops vernalis (O'Brien, 1979) may also contribute to the overall success of this form in Onondaga Lake. In a successful mathematical model of alewife-zooplankton interactions in Lake Michigan, Canale et al. (1976) demonstrated that alewife predation not only caused a decline in the larger forms of zooplankton, but also enhanced the small herbivorous forms. The continued presence of small numbers of D. pulex in Onondaga Lake in 1978 is probably in part due to its decrease in size at maturity since alewife re-establishment. Wells (1970) reports a similar strategy for D. pulex in Lake Michigan. Despite the lack of specific information concerning the magnitude of the alewife population and the date of re-establishment, it appears probable that this sizeselective planktivore caused the noted reduction in D. pulex in Onondaga Lake since 1969. It remains largely supposition as to the extent to which the change in phytoplankton composition and/or reductions in metal pollution affected the dramatic increase in zooplankton biomass in the lake since 1969.

1978 Onondaga Lake conditions and zooplankton Despite the reported improvements in the lake, the continuing elevated salinity, frequent low dissolved oxygen tensions and high concentrations of inert particles exert selective pressure and result in potentially stressful conditions for the

144

MICHAEL A. MEYER, STEVEN W. EFFLER

zooplankton. Whilst the majority of Cladocera and Copepoda are restricted to fresh waters of less than 1%o salinity, the salinity tolerances of the zooplankton of Onondaga Lake reported in the literature (Table 7) place them in the less common oligohaline-tolerant group. The particular species of Cyclops, C. vernalis, a codominant of the zooplankton of Onondaga Lake, has not previously been identified with oligohaline or more saline systems. The majority of freshwater rotifers are euryhaline and can inhabit waters of salinities between 0%0 and 3%0 (Remane & Schleeper, 1971). TABLE 7 SALINITY TOLERANCESOF THE ONONDAGALAKEZOOPLANKTON(1978)° Rotifers

Brachionus calyciflorus Brachionus plicatilis Keratella quadrata Keratella hiemalis Asplanchna hiemalis Synchaeta sp.b Filinia sp. b Bdelloidea

Up Up Up Up Up Up Up Up

to to to to to to to to

5%0 S 7%0 S 8%0 S 5%0 S 5~ooS 5~/ooS 8YooS 5%° S

Up Up Up Up

to to to to

4-5%0 S 4-5~/oo S 4-5%0 S 4-5%0 S

Cladocerans

Ceriodaphnia quadrangula Daphnia pulex Aloha affinis Chydorus spaericusb Copepods

Cyclops vernalis Cyclops bicuspidatus thomasi Diaptomus sp.~

No limit found Up to 10%o S Intolerant of salt water

* From Remane & Schleeper (1971). ~Rare species.

The Ca ÷ ÷ levels have remained at levels which exceed the reported acute and chronic LCso levels for Daphnia magna (Table 6), a zooplankter whose response to toxins has been described as generally representative of most freshwater microfauna (Anderson, 1950; Biesinger & Christensen, 1972). Anderson (1950) reported a toxicity threshold of CaCI 2 to C. vernalis of 1730 mg/litre, substantially less than Onondaga Lake concentrations. The 'whitings' common tothe lake (Meyer, 1979) probably stress zooplankton populations, or at least reduce their feeding efficiency (Eadie, 1979). The impact of such relatively inert particles is greatest on the cladocerans since rejection of unsatisfactory particles includes a complex behaviour pattern involving the use of their postabdominal claws to dislodge the particles whereas rejection by the copepods and rotifers is accomplished through simple release or expulsion (Starkweather, 1979). A number of the zooplankton of Onondaga Lake, including the co-dominants,

ZOOPLANKTON OF ONONDAGA LAKE (USA)

145

Ceriodaphnia quadrangula and Cyclops vernalis, are typical of eutrophic systems (Gannon, 1972; Gannon & Stemberger, 1978) and the temporal dissolved oxygen variations common to them. Low oxygen levels may also interact with other stress conditions to lower threshold values (Fairchild, 1955). Implications of increased zooplankton biomass The grazing of zooplankton contributes to phytoplankton losses from the water column. Phytoplankton losses are generally conceived to be of three components, as shown below:

Dp = Rp + s~ + e~

(2)

where: Dp = phytoplankton loss rate (day- 1), Rp = phytoplankton respiration rate (day-1), Sp = phytoplankton settling rate (day-1), pp = grazing rate (day-1). In a qualitative sense, the major increase in zooplankton biomass (and presumably grazing) since 1969 without substantial changes in phytoplankton biomass, respiration and settling rates, implies that a higher phytoplankton turnover rate was required in 1978 to maintain the observed phytoplankton standing crop. The relative increase in this turnover rate can be estimated by assessing the approximate contributions of grazing in 1969 and 1978 to the overall loss rates. Two components of the grazing (P~) term are required to estimate predation by the non-selective filter feeding Ceriodaphnia quadrangula (Ppl) and the raptorial feeding omnivore Cyclops vernalis (Fryer, 1957; Canale et al., 1976) (Pp2)The loss due to non-selective filter feeding can be estimated by the following expression (DiToro et al., 1971; O'Connor et al., 1975; Thomann et al., 1975; Simons, 1976).

(3) i

where: Ppl = predation rate by non-selective filter feeders (day-1), Cg, = gazing rate of non-selective filter feeder i (litre day =1 mg -1) (dry weight), Z i = concentration of zooplankter i (mg (dry weight) litre-1), Kmp = MichaelisMenton half-saturation constant for zooplankton (#g chlorophyll litre-1), p = phytoplankton concentration (as pg chlorophyll a litre- 1), ~i(T ) = temperature correction term for zooplankter i (unitless). Although C. vernalis is known to feed on Ceriodaphnia (Brandl & Fernando, 1974), their comparatively great numbers and parallel temporal trends (Fig. 3) with C. quadrangula imply substantial phytoplankton based food sources. Fryer (1957) found that C. vernalis digests a number of algae. The following expression, modified from Canale et al. (1976), was used to estimate phytoplankton losses from the raptorial feeding of C. vernalis.

146

MICHAEL A. MEYER, STEVEN W. EFFLER

\ / E, ci Pv: =feR • Sn~E,C i + ~-~-OODR)~b,(T)

(4)

where: Pv2 = predation rate by raptorial feeders (day-1), fPR = phytoplankton fraction of total food carbon available (mg phytoplankton C mg food C-1), Sn = 'snatching' rate (mg food C mg Zoo. C- 1 day- 1), Ci = sum of all concentrations of all states i that can serve as food for raptor, mg food C litre- 1. KFOODR = food level half-saturation constant for raptor (mg food C litre-1). The sources of food are assumed to be other zooplankters and the phytoplankton. A further, undocumented, simplifying assumption is that the losses to raptorial feeding are proportional to the fraction of the total food contributed by the phytoplankton. The observation that cyclopoid species do not pursue their prey, but seize it only after a collision or very close approach, partially supports this assumption (Fryer, 1957; Brandl & Fernando, 1974). Equation (2) can now be recast in a more quantitative form, with the above estimator expressions for grazing losses to give: W

~/'

Kmp

"~

D v = R v + ~ + Cg,Li|Km p \ + P)d&(T) +fvR.

Sn(E "

Z, Ci Ci + kT-OOD,)4~'(T)

(5) where: W/H = Sp, W = settling velocity (m day- 1) and H = depth of settling out

(m). The above expression has been used to evaluate the relative phytoplankton loss rates under the conditions of 1969 and 1978, particularly as they are affected by the respective zooplankton populations. Specified conditions and appropriate literature information concerning the organisms, kinetic constants and lake characteristics are summarised in Table 8. Estimates of the fractional phytoplankton loss rates, for periods of maximum (spring) and minimum (late summer) zooplankton biomass, for both 1969 and 1978, are presented in Table 9. The increased zooplankton biomass of 1978 is estimated to have caused an approximate doubling (1 •9-2•4) in phytoplankton loss rate from the lake's water column. In the light of the essentially unchanged phytoplankton biomass level in 1978, increases in phytoplankton turnover rate of similar magnitude are implied compared with 1969. A number of investigators have indicated that the grazing of herbivores can stimulate primary productivity (Slobodkin, 1964; Cooper, 1973; Gliwicz, 1975)• Zooplankton are known to actively participate in the nutrient dynamics of aquatic systems (Lean, 1973), not only by their consumption of nutrient-rich particles, but by the excretion of nutrients associated with digestive processes (Pomeroy et al., 1963; Barlow & Bishop, 1965; Gnaf & Rlazka, 1974). The dramatic increase in zooplankton biomass implies similar increases in secondary

147

ZOOPLANKTON OF ONONDAGA LAKE (USA) TABLE 8 VALUES AND SOURCES USED IN ESTIMATION OF PHYTOPLANKTON LOSS RATES a

Value

Parameter

Units

Source

Cgi

4.6 for C. quadrangula

Kmp T tpi(T) P

50 20 (invoked) 1 (for T = 20°C) 50

KFOOD R Sn

0.2 0.43 (for Cyclops)

Rp W

0.1 0.4 Greens/Diatoms 0.15 Blue-greens

m g food C litre- 1 m g food C (mg zoo C ) - t d a y - 1 day- t 0.4 m d a y - t 0.15 m d a y - 1

H

5 (for Onondaga Lake)

m

Millilitre per animal per day #g chloro litre-t °C Unitless #g chloro litre - t

Haney (1973) O'Connor et al. (1975) -Canale et al. (1976) Average value O n o n d a g a Lake, unpublished data Canale et al. (1976) Canale et al. (1976) O'Connor et aL (1975) Bierman (1976) Bierman (1976) Meyer (1979) Onondaga County (1971)

° The necessary individuals weights for Ceriodaphnia quadrangula and Cyclops vernalis are given in Table 3. TABLE 9 ESTIMATED PHYTOPLANKTON LOSS RATES FOR ONONDAGA LAKE, 1 9 6 9 AND

Case

Rr (day - l )

Sp (day - l )

Pp, (day - l )

Pp, (da[ ,'-I )

Dv (d[/y -I )

Pp/Dp

1969 spring

0.1

0.08

0.22

0.05

0.45

0.60

11. 1978 spring

0.1

0-08

0-63

0-25

1-06

0.83

111. 1969 late summer

0.1

0.06

0.09

0.00

0.25

0.36

IV. 1978 late summer

0.1

0.08

0.10

0.11

0-47

0.62

I.

1978

Dp 11

Dew

Dp 1V /)pill

-2.4

- 1.9

productivity and the associated excretion of nutrients. A number of investigators have demonstrated that excretion increases logarithmically as body weight decreases (Barlow & Bishop, 1965; Hargrave & Green, 1968; Peters & Rigler, 1973; Gnaf & Blazka, 1974). Thus, a shift to smaller zooplankton associated with the presence of an obligate planktivore, the alewife, even if constant total zooplankton biomass were maintained, would result in increased nutrient regeneration within the water column. The major increase in zooplankton biomass, which has also occurred since 1969, of course translates into a major increase in predicted nutrient regneration (Table 10). A number of expressions exist to predict regeneration per individual (reviewed by Peters & Rigler, 1973). We have selected the following

148

M I C H A E L A. MEYER, STEYEN W . EFFLER

T A B L E 10 EXTERNAL PHOSPHORUS LOADINGS AND ESTIMATED PHOSPHORUS EXCRETION BY ZOOPLANKTON, ONONDAGA LAKE

Year

1969" 1978 b 1980"

Pomt source P Ioadings(kg/day) TP POI - P 4980 745 620'

1460 490 --

Excreted reactwe P (kg/day) Late June Early September 32 369 --

7 107 --

" O n o n d a g a C o u n t y (1971). b O n o n d a g a C o u n t y (1979). c B a s e d o n 85 ~ r e m o v a l o f P a n t i c i p a t e d at t h e n e w t e r t i a r y s e w a g e t r e a t m e n t p l a n t .

relationship by Bishop & Barlow (1975) for the estimation of the rate of reactive (i.e. mostly available) phosphorus excretion per individual zooplankter: Ri = 144 x W -°'69

(6)

where: R~ = rate of reactive phosphorus excretion per individual zooplankter i (#g p g - 1 h-1), W~ = dry weight of individual zooplankter i (#g), since it was obtained from a lake in the same region (50 km) for which two of the four dominant zooplankton genera were Ceriodaphnia and Cyclops. The total rate of excretion (Rr) is then given by:

R r = Vn ~ Z , R ,

(7)

where: Vn=volume of Onondaga Lake (5-5 x 107m 3) containing active zooplankton. The estimated phosphorus excretion rates within the upper mixed layer (10 m) of Onondaga Lake are compared with the average external point source loading, for two different periods of both 1969 and 1978, in Table 10. The two periods were selected to demonstrate the range of impact of excretion for the respective years. The estimated excretion is probably conservative since assimilation of ingested food by zooplankton decreases under the algal bloom conditions (Barlow & Bishop, 1965) typical of Onondaga Lake. Apparently, this internal source of phosphorus was insignificant in 1969 whilst in 1978 its contribution was significant. Ganf & Blazka (1974) estimated the ratio of annual zooplankton to external loading of phosphorus to Lake George (Uganda) to be 2-7. Barlow & Bishop (1965) found that the regeneration of phosphorus by zooplankton in the epilimnion of Cayuga Lake (New York, USA) was sufficient to supply the requirements of the phytoplankton for that period. Concentrations of macronutrients in Onondaga Lake for 1978 (epilimnetic minima; 48/ag. PO~ - P, 260 #g/litre N O~ - N, 400 #g NH~" - N) indicate that the system was nutrient-saturated (Bannister, 1974). Thus, nutrients recycled by the zooplankton may not have been critical to primary productivity, and thereby not necessarily related to the previously implied higher phytoplankton turnover rates

ZOOPLANKTON OF ONONDAGA LAKE (USA)

149

since 1969. This additional interaction with the lake's primary productivity may become more important following the future reductions (1980) in phosphorus loading that are anticipated (Table 10). SUMMARY

The concurrent change in several potential influences in the interval, 1969-1978, complicates the identification and interpretation of cause and effects relationships which explain the observed changes in the zooplankton of Onondaga Lake for that period. It is probable that the re-establishment of the alewife caused the reduction in the large daphnids, despite the major overall increase in zooplankton biomass and concentration. Based on the small sizes of dominant microcrustaceans and their probablehigh turnover rates in such a eutrophic system, it appears unlikely that the alewife significantly influenced the zooplankton standing crop of the lake. The most dramatic aspect of the change in the lake's zooplankton since 1969, the ten- to twenty-fold increase in biomass, may be in response to reclamation efforts which have resulted in substantial changes in phytoplankton composition and reductions in water column pollutant concentrations. Despite the noted improvements in the lake since 1969, current salt, intert pariicle and dissolved oxygen conditions present a rather extreme environment and sources of selective pressure for the zooplankton. The increased zooplankton biomass implies increased grazing on phytoplankton, phytoplankton turnover rates and nutrient recycling, within the upper waters of the lake. These zooplankton-phytoplankton interactions may act to delay or resist further reclamation efforts directed at primary productivity.

REFERENCES AMERICAN PUBLIC HEALTH ASSOCIATION, AMERICAN WATER WORKS ASSOCIATION, AND WATER POLLUTION CONTROL FEDERATION (1975). Standard methods for the examination of water and wastewater, 14th edn. Washington, DC. ANDERSON, B. G. (1950). The apparent thresholds of toxicity to Daphnia magna for chlorides of various metals when added to Lake Erie water. Trans. Am. Fish. Soc., 78, 96-113. ANDREWS,R. W., BIESlNGER,K. E. & GLASS,G. E. (1977). Effects of inorganic complexing on the toxicity of Copper to Daphnia magna. Water Res., 11, 309-15. ARNOLD, D. R. (1971). Ingestion, assimilation, survival and reproduction by Daphnia pulex fed seven species of blue-green algae. Limnol. Oceanogr., 16, 906-20. BANNISTER, T. T. (1974). Quantitative description of steady-state nutrient saturated algal growth, including adaptation. Limnol. Oceanogr., 24, 79-96. BARLOW,J. P. & BISHOP,J. W. (1965). Phosphate regeneration by zooplankton in Cayuga Lake. L imnol. Oceanogr., 10 (suppl.), R15-R24. BIERMAN,V. J. (1976). Mathematical model of the selective enhancement of blue-green algae by nutrient enrichment. In Modeling biochemicalprocesses in aquatic ecosystems, ed. by R. P. Canale, 1-32. Ann Arbor, Michigan, Ann Arbor Science, Inc. BIESINGER, K. E. & CHR1STENSEN,-G. i . (1972). Effects of various metals on survival, growth, reproduction, and metabolism of Daphnia magna. J. Fish. Res. Bd Can., 29, 1691-700.

150

MICHAEL A. MEYER, STEVEN W. EFFLER

BISHOP, J. W. & BARLOW, J. P. (1975). Phosphorus release by zooplankton (comment). Limnol. Oceanogr., 20, 148-9. BRANDL, Z. & FERNANDO, C. H. (1974). Feeding of the copepod Acanthocyclops vernalis on the cladoceran Ceriodaphnia reticulata under laboratory conditions. Can. J. Zool., 52, 99-105. BROOKS,J. L. (1957). The systematics of North American Daphnia. Memoirs of the Connecticut Academy of Arts and Science, 8. BROOKS,J. L. & DODSON, S. I. (1965). Predation, body size and composition of plankton. Science, N.Y., 150, 28-35. BROOKS, J. L. (1968). The effects of prey-size selection by lake planktivores. Syst. Zool., 17, 272-91. CANALE, R. P., DEPALMA, L. M. & VOGEL,A. H. (1976). A plankton-based food web model for Lake Michigan. In Modeling biochemicalprocesses in aquatic ecosystems, ed. by R. P. Canale, 33-7. Ann Arbor, Michigan, Ann Arbor Science, Inc. COMITA,G. W. (1972). The seasonal zooplankton cycles, production and transformation of energy in Severson Lake, Minnesota. Arch. Hydrobiol., 70, 14-66. COOPER, D. C. (1973). Enhancement of net primary productivity by herbivore grazing in aquatic laboratory microcosms. Limnol. Oceanogr., 18, 31-7. DENCE, W. A. (1956). Concretions of the alewife, Pomolobus pseudoharengus (Wilson), at Onondaga Lake, New York, Copeia, 3, 155-8. DEPINTO, J. V., BIERMAN, V. J. & VERHOFF,F. H. (1976). Seasonal phytoplankton succession as a function of species composition for phosphorus and nitrogen. In Modeling biochemicalprocesses in aquatic ecosystems, ed. by R. P. Canale, 141-70. Ann Arbor, Michigan, Ann Arbor Science, Inc. DIToRo, D. M., O'CONNOR, D. J. & THOMANN, R. V. (1971). A dynamic model of the phytoplankton population in the Sacramento-San Joaquin Delta. Adv. Chem. Ser., 106. DUMONT, H. J., VAN DEVELDE,I. & DUMONT,S. (1975). The dry weight estimate of biomass in a selection of Cladocera, Copepoda, and Rotifera from the plankton, periphyton and benthos of continental waters. Oceologia (Berl.), 19, 75-97. EAglE, B. J. (1979). The cycle ofa CaCO 3 in the Great Lakes. Paperpresentedat the 42ndAnnual Meeting, American Society of Limnology and Oceanography, Marine Sciences Research Center, S UNY Stony Brook, New York. EDMONDSON, W. T. (ed.) (1959). Fresh water biology. New York, Wiley and Sons, Inc. EDMONDSON, W. T. (1965). Reproductive rate of planktivore rotifers as related to food and temperature in nature. Ecol. Monogr., 35, 61-111. FAIRCmLD, E. J. (1955). Low dissolved oxygen: Effect upon the toxicity of certain organic salts to the aquatic invertebrate, Daphnia magna. In Proc. A. Water Syrup., 4th, 22-23 March, 1955, Baton Rouge, LA, Eng. Exp. Station, Bull. No. 51, 95-102. FIELD, S. D., EFFLER,S. W. & RAND, M. C. (1979). Diurnal dissolved oxygen variation in hypereutrophic Onondaga Lake, Syracuse, N.Y. Paper presented at the 42rid Annual Meeting, American Society of Limnology and Oceanography, Marine Sciences Research Center, S UNY Stony Brook, New York. FRYER, G. (1957). The food of some freshwater cyclopoid copepods and its ecological significance. J. Anita. Ecol., 26, 263-86. GANNOI~,J. E. (1970). An artificial key to the common zooplankton Crustacea,of Lake Michigan, exclusive of Green Bay. Milwaukee, Center for Great Lakes Studies, University of Wisconsin. GANNON, J. E. ( 1971). Two counting cells for the enumeration of zooplankton micro-crustacea. Trans. Am. Microsc. Soc., 90, 486-90. GANNON, J. E. (1972). Effects of eutrophication and fish predation on recent changes in zooplankton crustacea species composition in Lake Michigan. Trans. Am. Micros. Soc., 91, 82-4. GANNON, J. E. (1976). The effects of differential digestion rates of zooplankton by alewife, Alosa pseudoharengus on determination of selective feeding. Trans. Am. Fish. Soc., 105, 89-95. GANNON, J. E. & STEMBERGER,R. S. (1978). Zooplankton (especially crustaceans and rotifers) as indicators of water quality. Trans. Am. Microsc. Soc., 97, 16-35. GEmN & RIPL (1978). Nutrient decrease and response of various phytoplankton size fractions, following the restoration of Lake Trammen, Sweden. Arch. Hydrobiol., 51,339-67. GENTILE, J. H. & MALOtqEV, T. E. (1969). Toxicity and environmental requirements of a strain of Aphanizomenon flos-aquae (L). Can. J. Microbiol., 15, 165-73. GLIWICZ, Z. M. (1975). Effect of zooplankton grazing on photosynthetic activity and composition of phytoplankton. Verb. int. Verein. theor, angew. Limnol., 19, 1490-7. GNAF, G. G. & BLAZKA,P. (I 974). Oxygen uptake, ammonia and phosphate excretion by zooplankton of a shallow equatorial lake (Lake George, Uganda). Limnol. Oceanogr., 19, 313-25. GORnAM, P. R. (1960). Toxic water blooms of blue-green algae. Can. Vet. J., 9, 235-45. GORHAM, P. R. (1964). Toxic algae. In Algae and man, ed. by D. F. Jackson, 307-36. New York, Plenum Press.

ZOOPLANKTON OF ONONDAGA LAKE (USA)

151

HALL, D. J., COOPER, W. E. & WERNER, E. E. (1970). An experimental approach to the production dynamics and structure of freshwater animal communities. Limnol. Oceanogr., 15, 839-928. HANEY, J. F. (1973). An in situ examination of the grazing activities of natural zooplankton communities. Arch. Hydrobiol., 72, 3%132. HARGRAVE,B. T. & GREEN, G. H. (1968). Phosphate excretion by zooplankton. Limnol. Oceanogr., 13, 332-43. HUGHES, E. O., GORHAM, P. R. & ZCHNDAR, A. (1958). Toxicity of a unialgal culture of Microcyctis aeruginosa. Can. J. Mierobiol., 4, 225-36. HUTCHINSON, B. P. (1971). The effect offish predation on the zooplankton of ten Adirondack lakes, with particular reference to the alewife, Alosa pseudoharengus on determinations of selective feeding. Trans. Am. Fish. Sot., 105, 8%95. I NFANTE,AIDA DE(1978). Natural food of herbivorous zooplankton of Lake Valencia (Venezuela). Arch. Hydrobiol., 62, 34%58~ LEAN, D. R. S. (1973). Phosphorus dynamics in lake water. Science, N.Y., 179, 678-80. MCINTOSH, A. W. & KEVERN, N. P. (1974). Toxicity of Copper to zooplankton. J. environ. Quality, 3, 166-70. MCNAUGHT, D. C. & BUZZARD, M. (1973). Changes in zooplankton populations in Lake Ontario (1939-1972). Proc. ConJ~ Great'Lakes Res., 16th, 78-86. International Association of Great Lakes Research. MEYER, M. A. (1979). The temporal and spatial distribution of the limnetie zooplankton in Onondaga Lake, Syracuse, N.Y. Masters thesis, Department of Civil Engineering, Syracuse University, Syracuse, NY. MURPHY, C. B. (1973). Effect of restricted use of phosphate based detergents on Onondaga Lake. Science, N.Y., 182, 379-81. NAUWERCK,A. (1963). Die Beziehungen zwisehen Zooplankton und Phytoplankton in See Erken. Symb. bot. upsal., 17, 94-100. O'BRIEN, J. W. (1979). The predator-prey interaction of planktivorous fish and zooplankton. Am. Scient., 67, 572 81. O'CONNOR, D. J., DIToRO, D. M. & THOMANN,R. V. (1975). Phytoplankton models and eutrophication problems. In Ecological modeling in a resource management framework, ed. by C. S. Russell. Proceedings of symposium sponsored by NOAA and Resources. ONONDAGACOUNTY( 1971). Onondaga~Lake Study. Project No. 11060, FAE 4/71. Water Quality Office, Environmental Protection Agency, Onondaga County, Syracuse, New York. ONONDAGA COtmTV (1976). Onondaga Lake Monitoring Program. Jan. 1975-Dee. 1975. O'Brien and Gere Engineers, Inc., Syracuse, New York. ONONDAGA COUNTY (1979). Onondaga Lake Monitoring Program. Jan. 1978-Dee. 1979. Cazenovia, NY, Stearns and Wheler, Civil and Sanitary Engineers. PENNACK, R. W. (1953). Fresh-water invertebrates of the United States. New York, Ronald Press Co. PETERS, R. H. & RIGLER, F. H. (1973). Phosphorus release by Daphnia. Limnol. Oceanogr., 18, 821-39. POMEROY, L. R., MATHEWS, H. M. & MIN, H. S. (1963). Excretion of phosphate and soluble organic phosphorus compounds by zooplankton. LimnoL Oceanogr., 8, 50-5. REMANE, A. & SCHLEEPER, C. (1971). The biology of brackish water. New York, Wiley and Sons, Inc. SEEGER,E. (1979). The fate of heavy metals in Onondaga Lake. Masters thesis, Department of Civil and Environmental Engineering, Clarkson College, Potsdam, N.Y. SCI-IINDLER,D. W. (1968). Feeding, assimilation and respiration rates of Dahpnia magna under various environmental conditions and their relation to production estimates. J. Anita. Ecol., 37, 36%85. SCHINDLER, D. W. (1977). Evolution of phosphorus limitation in lakes. Science, N.Y., 195, 260-2. SHUMAN, M. S. & WOODWARD, G. P. (1977). Stability constant of carbon-copper-organic chelates in aquatic samples. Environ. Sci. & Technol., 11, 809-13. SIMONS, T. T. (1976). Continuous dynamical computations of water transport in Lake Erie for 1970. J. Fish. Res. Bd Can., 33, 371-84. SLOBODKIN,L. B. (1964). Growth and regulation ofanimalpopulations, New York, Holt, Rinehart and Winston. SOROKIN, J. J. (1968). The use of 14C in the study of the nutrition of aquatic animals. Mitt. int. Verein. theor, angew. Limnol., 16. STARKWEATHER, P. L. (1979). Morphological and behavioral aspects of selective feeding by nonpredatory freshwater zooplankton. Paper presented at the 42nd Annual Meeting~ American Society of Limnology and Oceanography, Marine Sciences Research Center, SUNY, Stony Brook, New York. STEWART,K. M. (1979). Book review of: Lakes of New York State. Am. Scient., 67, 480-1.

152

MICHAEL A. MEYER, STEVEN W. EFFLER

SYLVA,R. N. (1976). The environmental chemistry of copper (II) in aquatic systems. Wat. Res., 10, 789-92. SZE, P. & K INGSBURV,J. M. (1972). Distribution of phytoplankton in a polluted saline lake, Onondaga Lake, New York, J. Phyeol., 8, 25-37. SzE, P. 0975). Possible effect of lower phosphorus concentrations on the phytoplankton in Onondaga Lake, New York. Phycologia, 14, 197-203. THOMANN,R. V., DITORO,D. M. & O'CONNOR,D. J. (1975). Mathematicalmodeling ofphytoplankton in Lake Ontario. Grosse Ile Laboratory, National Environmental Research Center, Grosse lie, Michigan. WATERMAN,G. (1971). Onondaga Lake zooplankton. 361-84. In Onondaga Lake Study. Project No. i 1060, FAE 4/71. Water Quality Office, Environmental Protection Agency, Onondaga County, Syracuse, New York. WELLS,L. (1970). Effects of alewife predation on zooplankton populations in Lake Michigan. Limnol. Oceanogr., 15, 556-65.