PB84-133008
PCBs (Polychlorinated Piphenyls) in
Saginaw Bay: Development of Functional
Indices to Estimate Inhibition of
Ecosystem Fluxes
State Univ. of New York at Albany
Prepared for
Environmental Research Lab.-Duluth, MN
Jan 84
U.S. Department of Coransf ce
Katzsnal Tecfeac^ ^fonnatkm Service
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EPA-600/3-84-008
January 1984
PCBS IN SAGINAW BAY: DEVELOPMENT OF FUNCTIONAL INDICES TO
ESTIMATE INHIBITION OF ECOSYSTEM FLUXES
by
Donald C. McNaught
David Griesmer
Marlene Buzzard
Michele Kennedy
State University of New York at Albany
Department of Biological Sciences
Albany, New York 12222,
Grant 804573
Program Element
PROJECT OFFICER
William Richardson
Large Lakes Research Station
Grosse lie, Michigan 48138
ENVIRONMENTAL RESEARCH LABORATORY
U.S. ENVIRONMENTAL PROTECTION AGENCY
DULUTH, MINNESOTA 55804
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TECHNICAL REPORT-DATA
rumcnoni an tht rtrmt be/an compUtinf}
REPORT NO.
EPA-600/3-84-OQ8
X RECIPIENT'S ACCESSION NO.
155008
TITLE AND SUBTITLi
PCBs in Saginaw Bay: Development of Function.il
Indices -to Estimate Inhibition of Exosystem Fluxes
S. REPORT OAT«
January 1934
(. PERFORMING ORGANIZATION COD!
AUTMOR(S)
D. C. McNaught, D. Griesmer, M. Buzzard, and
M. Kennedy
I. PERFORMING ORGANIZATION REPORT NO.
. PERFORMING ORGANIZATION NAMI AND ADDRESS
Department of Ecology and Behavioral Biology
University of Minnesota
Minneapolis, Minnesota 55455
10. PROGRAM ELEMENT NO.
11. CONTRACT/GRANT NO.
804573
2. SPONSORING AOENCY NAME AND ADDRESS
U.S. Environmental Protection Agency
ERL-Duluth, Large Lakes Research Station.
9311 Groh Road
Grosse lie, Michigan 48138
IX TYPE Of REPORT AND PERIOD COVERCO
14. SPONSORING AGENCY COOK
EPA/600/03
S. SUPPLEMENTARY NOTES
0. A&STRACT
Saginaw Bay is among the most polluted bays in the Great Lakes. For many years the
Large Lakes Research Station of the US-EPA has examined many aspects of this ecosystem,
from phytoplankton community characteristics to contaminant levels in fishes. As a
result, when it became desirable to determine the impact of an organochlorine
-contaminant-1-ike-PCB, it-was not necessary to-study the -ecosystem-in detail?;~"Phyto-
planktoti species and densities were known, Zooplankton speciec, densities and feeding
habits had been investigated.
This study produced new information on th^ two most basic fluxes in any aquatic system,
.the flow of solar energy into the phy_oplankton, and the flow of solar energy into
the phytoplankton, and the flow of chemical energy inco the zooplankton. The use of
phytoplankton gross photosynthesis to estimate the inhibition by contaminants of the
first flux mentioned was developed for marine communities. In comparison, the use of
zooplankton ingestion rates to estimate the inhibition by contaninants.of carbon flow
into secondary producers is new and developed for this investigation.
17.
KEY WOnOS AND DOCUMENT ANALYSIS
DESCRIPTORS
b. IDENTIFIERS/OPEN ENDED TERMS
e. COSATI Field/Croup
9. DISTRIBUTION STATEMENT
RELEASE TO -PUBLIC
19. SECURi rv CLASS (Thtt Riponj
UNCLASSIFIED
21. NO. OF PAGE*
X. SECURITY
UNCLASSIFIED
42.PRIC*
(PA ftrm 1220-1 (ft**. 4-77) »neviou» IJITION if O«»OLITI
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DISCLAIMER
The Information in this document was funded wholly or in part by the
United States Environmental .Protection Agency-under agreement R-804573
to the State University of New York; it has been subjected to the Agency's
peer and administrative review. The contents .reflect the views and
policies of the agency.
11
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CONTENTS
Disclaimer • ii
Abstract. iv
r Figures vii
Acknowledgement. i*
1, Introduction. 1
2. Conclusions 5
3. Recommendat ions 8
3.1 Recommendations for water quality criteria on PCB's...'.". 9
3.2 Recotnnendations for future reseaurch 10
4. Experimental Procedures
4.1 Methods for determining effects of PCB's on Saginaw
Bay ecosystem................ 12
4.2 Methods for determining effects of PCB's upon
carbon fixation ' _.iv ..".. ..»15
4.3 Methods for determining effects of chronic exposure "''.
to PCB's , ....-...-.,-...,.. .16-
4.4 Methods for assessing zooplankton grazing .^®"
4.5 Location of experiments... i... — .20
5. Results and Disci"?'-ion .........;.. •. .23"
5.1 Effects c^ i'CB's up-;, carbon flow in the Saginaw
Bay ecosy- -_em ^..._23-
5^2 -Inhibition-of natural phytoplankton photosynthesis at
environmental concentrations of PCB's and metabolites.39
5.3 Chronic effects of dichlorobiphenyl upon the survival
of the crustacean Diaptomus. ..'.'...... 66
5.4 Inhibition of grazing as an algal control 74
References 92
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Abstract: Aquatic ecosystems of the Great Lakes are threatened by
approximately 50,000 chemicals of commerce from the United States and
Canada; at least 2000 may have adverse biological effects and only 200 have
been studied (IOC Annual Report. 1982). Contaminants as chlorinated
hydrocarbons are especially prone to concentration in food chains because of
their partitioning into lipids of lower organisms, and later food chain
concentration by apex predators. Waters of the Great Lakes contain 2 to 300
ng f* PCB; this major contaminant is concentrated about 1 million-times-ln
apex predators. Generally the mode of action of PCBs is to inhibit
organisinic as well as ecosystem metabolism, and thus ecosystem productivity.
Since the complex food webs of Lake Huron involve hundreds of phytoplankton
taxa and tens of zooplankton taxa, we utilized and developed two ecosystem
functional -ind.ices-measur_ing contaminant inhibition. These were measures of
the inhibition (and sometimes stimulation) of algal photosynthesis and of
zooplankton g-azing.
Methodologically *4C-bicarbonate was used to measure phytoplankton
gross photosynthesis. PCB concentrations of 5-500 ng jf* above control
levels were injected into experimental test samples of phytoplankton
incubated-at-depth—of coMectioni Intvibition of photosynthesis was
expressed as a percentage decrease relative to control values. This simple
test is a functional (rate impacted) index of ecosystem-inhibition^-at
trophic level one (phytoplankton). In a similar- treatment, *4C tagged
ilgae, fractionated into nannoplankton and netplankton size ranges (<20 urn
and >20 pm dia.), were fed to zooplankton and filtering rates were
calculated. Then similar tests were performed where experimental containers
ilso contained PCBs. Thus the relative depression of grazing by PCBs was
iv
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measured for all major taxa of zooplankton.
Eight important conclusions were reached with regard to the Saginaw Bay
ecosystem. With regard to phytoplankton photosynthesis, dichJorobiphenyl
was selectively more, toxic to nannoplankton-than—netplankton. This is an
important conclusion, since Great Lakes food chains are based on sma-Tl
nannoplankton algae. Secondly, dichlorobiphenyl metabolites (unspecified!
were more toxic to phytoplankton than the parent isomer. This finding
suggested problems similar to those encountered for other man-made organics.
"In addition to selective toxicity by phytoplankton size, we found that PCBs
inhibited photosynthesis of diatoms and green algae more than-blue-green
algae; unfortunately diatoms and small greens-are the most grazed components
in this ecosystem. Zooplankton grazing -was-.'also inhibited by FCB
metabolites, and especially when detritus was present, as in most productive
waters of the Great Lakes. The above_find.iags-were based on-exposures-to-
PCBs above normal environmental levels encountered in Lake Huron.
Inhibition of algal photosynthesis by ambient levels of PCBs was
examined for dichlorobiphenyl and hexachlorobiphenyl and purified
metabolites, including hydroxylated PCS and furans. Ambient levels of PCBs
inhibited nannoplankton productivity. In the hexachlorobiphenyl series-the-
hydroxylated PCB and furan were more inhibitory to photosynthesis than the
partnt isomer, with a seasonal range of inhibition of -2 to -93%. At depth
these same contaminants stimulated gross photosynthesis, probably by
increasing algal respiration and net production. This was a totally new
result. In the dichlorobiphenyl series the metabolic products inhibited
photosynthesis 1n surface waters from -6 to -22%, much less than by the
higher chlorinated compound.
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Lastly, we compared grazing in western Lake Erie to that in Saginaw
Bay. In Lake Erie, grazing as a control on algal populations was almost as
effective as in oligotrophic Lake Huron,,_whereas. gr.azJng_was-gr.eat.ly-
dept essed in Saginaw Bay. Apparently the Lake Erie ecosystem is in much
better condition than Saginaw Bay.
We conclude that functional ecosystem irhibition by toxic chemicals as
PCBs is a most serious problem. Our results clearly indicate that levels of
PCBs must be held below 5 ng a"1 and we suggest that level as an appropriate
water quality objective to the IJC. In addition, we suggest more attention
be paid to the effects of PCS metabolites on natural communities. We also
imply that the lack of zooplankton grazing in..an ecosystem like Saginaw.. Bay.
is related to unknown inhibitory-compounds—w-i-th-a-mode-of—ae-t-ion^s-in+1-ar^-OF-
identical to PCBs.
VI
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FIGURES
Number "Page
1 Location of studies on Saginaw Bay, Lake Huron--~ ^ . -. '21
2 Location of studies on Western Lake Erie 22
3 Ecdsystera impact of experimental addition of 25 jjg 1"1
(iichlorobiphenyl, including inhibition of carbon
flow (right column) and accumulation of PCB with
trophic levels (left column) 34
4A Simulated route of transfer of dichlorobiphenyl to
dichlorodibenzofuran (di- series). ..... ^_
4B Simulated route of transfer of hexachlorobiphenyl to
its furan (hexa- series) 46
5 Relative nannoplankton (o) and netplankton (o) pro-
ductivify-on-10-June—1978~at~0.5 nr~depth upon expo-
sure to 5,_ 100 and 500 eg I"1 hexachlorobiphenyl and
100 ng 1-1 pent^chlorcbiphenylol (OH-PCB) and-
occachlorodiber£ofuran (CDBF) 49
6 Relative nannoplankton (o) and netplankton (o) pro-
ductivity on 9 July 1978 when exposed to he.xa-
series at 0.5 m depth 50
7 Estimated relative inhibition of productivity (o)
relative to actual productivity (o) and PCB levels
(ng 1-1) _ , .. , -52
8 Relative nannoplankton (o) and netplankton_(o-)-pro-
ductivity at 0.5 m depth on 16 August 1979 when
exposed to dichlorobiphenyl series . 55
9 Inhibition (hatched) and stimulation of netplankton
carbon fixation by hexa- series (100 ng I"1) during
1978 . 56
10 Inhibition (hatched) and stimulation of nannoplankton
carbon fixation by di- series (100 ng I"-1) during
1979 58
vii
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Number Pa§
11 Stimulation/inhibition of carbon fixation by PCB's
and metabolites relative to degree of chlorination . 61
-121 Stimulation/inhibition of carbon fixation by 100 ng
I-1 hexachlorobiphenyl (o) and its hydroxylated
product (o) relative to light intensity : 62
I
, -Stimulation/inhibition of carbon fixation by di- and I
!13 hexachlorobiphenyl and metabolites relative to their!
I lipid-water partition coefficients |65
14 Number of surviving Diaptomus in controls and experi-
mental exposures (3.4 and 20.0 ng 1~*) over time
(days), in flow-through experiments
15 A-D. Ingestion-concentration curves for Eubosmina
(o), Chydorus (o), Diaptomus adults (A) and nauplii
(A) in Saginaw Bay (dashed line), as compared to the
same ingestion rates as identical concentrations in
the open waters oi Lake Huron (solid line) ..... 78
16 Model for inhibition of ingestion (I); symbols in-
text ............ ....... ..... 80
17 Relative composition (by volume) of phytoplankton
community of Saginaw Bay, including diatoms (D),
green (G) and blue-green (BG) algae ......... 81
18 Percentage inhibition by Eubosmina (o), Chydorus (o),
and Diaptomus (A) as a function of the percentage
composition of blue-green algae in Saginaw Bay - . . 84
19 A-D. Ingestion-concentration curves for Eubosmina
(o), Chydorus (o); Diaptomus adults (A) and nauplii
(A) in Western Lake Erie (dashed line) compared to
the same ingestion rates at identical concentrations
in the open waters of Lake Huron (solid line). . . ... 87
Vlll
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ACKNOWLEDGMENTS
Many helpful people were Involved with this study; in addition
"to those listed on the title page Nelson Ti.omas, William Richardson,
and Wayland Swain were.-involved in boti- planning-and-execution. Ryland
Loos prepared the many figures in his usual high quality fashion, Steven
Eisenreich provided critical comments. And the study even led to a more
permanent relationship for two of the participants. Thanks to all of you.
IX
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SECTION 1
INTRODUCTION
Aquatic ecosystems are by nature sensitive to contaminants which concen-
trate in food chains. The mechanisms involved in accumulation of polychlorin-
ated biphenyls (PCB's) include physical concentration, equilibrium partition-
ing with lipoid materials (Pavlou and Dexter, 1977) , and bioconcentration by
higher organisms (many authors). These mechanissm take PCB's found in lake-
water at concentrations in ppt (ng 1~ ) and concentrate them until fishes often
contain concentrations of ppm (mg 1~ ).
The-waters of the Great Lakes all contain about the same concentration of
PCB's, with Lake Superior at about 2 ng 1 (Eisenreich, unpub.). Lake Michi-
gan at 10- ng 1~* offshore ?~X 100 ng 1 near shore (Veith, 1975), Lake Huron
t
-1 *
at 5-316 ng 1 in Saginaw"E_/ (Richardson, pers. coitm.). Lake Erie at 27 ng
1 and I-ake Ontario at 30 ng 1 (Glooshenko et_ al., 1975). Thus concentra-
tions in Great Lake waters generally fall within the same range and bear lit-
tle resemblance to the degree of industrialization of surrounding countryside.
"However, Saginaw Bay, downriver from major industrial activity, is the largest
input to Lake Huron (Frank et al., 1979). Dry deposition from the atmosphere
accounts for a significant input of PCB's to the Great Lakes, along with the
more obvious industrial dumping. Industrial manufacture of PCB's has been
discontinued since 1972, but utilization of PCB's continues in liininted quan-
tities. Aerosols containing PCB's may travel hundreds of kilometers (McClure,
1976) and constitute the principal input for lakes like Superior (Eisenreich
I
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and Hollod, 1979), whose shores are not industrialized. Following dry deposi-
tion, PCB's may be concentrated in surface slicks or monolayers of lipoid ma-
terials (Duce e_t al^ , 1972). At the same time, losses of PCB's from surface
-slicks-occurs through~volatinzation_(Southworth, 1979). Thus PCB's may be
concentrated at the surface of the lakes, where biological uptake is most
probable.
Phytoplankton accumulate PCB's, likely through equilibrium partitioning
between water and lipid materials, although dead algae also concentrate them
(Urey et al. , 197 ). Equilibrium between algae and water occurs within two
hours (Harding e_t al., 1978). Commonly literature values for. the inhibition
of carbon fixation by phytoplankton suggest a lower' threshold of 10 yg 1 PCB
(Harding, 1976; Powers e_t ajU , 1977) ^.although Glooschenko et_ al_. (1975) found
1 yg 1 inhibited photosynthesis—in—L^~0ntario.——T-hi-s—repoEt-wi43^-J.ower. t-.hese^.
thresholds considerably further.
Zooplankton reproduction (Daphnia) was affected by Aroclor (industrial
PCB mixture) levels of 1.3 yg 1~ (Nebeker and Puglisi, 1974). PCB's are com-
monly in equilibrium between the water and zooplankton lipids (Ware and Adde-
son, 1973; Pavlou and Dexter, 1977). Thus PCB's may be concentrated in marine
zooplankton at levels of 0.3 to 260 yg g (P-Lsebrough et al., 1972). Gener-
ally it has been concluded that ecological magnification increases with the
degree of chlorination of the biphenyl (Metcalf, 1975).
PCB's aru common in the fishes of Lake Huron, especially in^herbivious
alewivos and predaceous walleyes and channel catfish (Reinert, 1970). Penta-
and hexachlorobiohe.iyls are the most commonly found isomers in fishes (Ball-
schniter et^ a_l^., 1978). Recently (Frank et^ al. , 1978) PCB's were found in
excess of 2 yg g~ in bloaters, splake, and cisco in Lake Huron. The white
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sucker, an underutilized species of potential importance, contains 6-43 pg g~*
in Lake Huron (Zabik e£ aJU, 1978).
At the top of the food chain, PCB's have been found in mother's blood at
levels of 1.7-4.6 pg l"1 (Kuwabara e_t al^., 1979). Currently PCB's in Lake
Ontario exceed International Joint Commission (UC) water quality objectives
and U.S.-E.P.A. criteria (Waller and Lee, 1979).
This brief introduction illustrates our considerable-knowledge-concerning
the impact of PCB's on aquatic ec ' .••-ems. It also has revealed a distinct
)
lack of knowledge .in specific areas, to which this-report is addressed. We
know little of the impact upon a single simple food-chain, therefore we have
chosen the approach of ecosystem analysis. We also know little of the effect
of sure PCB isomers, as opposed to industrial Aroclors, on such food-chains.
More specifically we know very little concerning the impact of degradation
products of PCBIs-on the biota of the Great Lakes. The effects of metabolites
are-critical to understandl.ivj total ecosystem inpact.
Generally the role of PCB's is to inhibit ecosystem metabolism and car-
bon flow. Other natural compounds also inhibit ecosystem functions. Inhibi-
tion of grazing by zooplankton was studied in Saginaw Bay and Lake Erie. Such
inhibition in the natural environment is compared to that studied in the ~lab-
oratory, where.inhibition has-been-modeled-(McMahon and"RiglerT" 1963) and
where various biological factors resulting in inhibition of grazing have been
studied in controlled experiments (Arnold, 1971;- HcNaught et-a'-l-. ,--198.0b)-._
The natural control of algal populations will be examined by looking for
evidence of saturation feeding. In the oligotrophic waters of Southern Lake
Huron saturation feeding does not occur; that is, irv^estion increases linearly
with food availability. During the periods of high phytopiankton-growth, much
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of the biomass is harvested. The grazing pressures were especially intense on
the small nannoplankton (HcNaught et al., 1980a). If zooplankton saturation
feeding (inhibited ingestion) occurs in either Lake Erie or Saginaw -Bay-r- these
bodies..of.-water-are loosing -important -biologrcal~coirtroIs' upon algaT~blooms.
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CONCLUSIONS
Flsrt we examined the impact of PCB's on the planktonic ecosystem of
Saginaw Bay. A consideration of food chains in Lak«i Huron prompted the de-
velopment of a simple in situ assay for both~~the acute~toxicity and'bioac-
cumulation of PCB's. Two trophic levels were considered, the first the primary
producers, and the second, the primary consumers or herbivores, with the
assay utilizing all of the natural biota of ea:h trophic level. First a
14
relatively large amount of C -bicarbocate was added to the natural phyto-
plankton assemblage to measure the rate of photosynthesis. After four hours
incubation, the hot algae were fed to zooplankton, which were later assayed
14 1 •
for C activity. In a similar fashoning, JH-PCB's were simultaneously added
14
with~C to experimental phytoplankton samples. Thus the rate of-uptake and
standing-crop of PCB's could be measured; once these dbubTe-tagged" algae had
been fed to zooplankton, the uptake of PCB's and their bioaccumulation could
be estimated. But most impo -:antly, the effect of PCB's on carbon flow could
be precisely measured. Our in situ assay considers the impact of PCB's on
carbon flow through two trophic levels; the use of this technique led to eight
important conclusions:
The-parent isomer, 2, 2* PC? was more toxic to nannoplankton than net-
plankton. This is_an important conclusion, since Great Lakes food-chains are
based upon small nannoplankton algae. Secondly, based on exposure, 2, 2' PCB
metabolites were more toxic than the parent isomer. Although estimates of
metabolite abundance in the Great Lakes are not available, this finding
suggests problems similar to those encountered for other man-made organics.
The greatest reductions of primary carbon fixation by PCB's were in the
ecosystem contributions of diatoms and green algae, the most grazed-upon
conponents. Sorption or binding was a significant factor in the accumulation
of PCB's by these algae.
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Surprisingly, reductions in grazing by zooplankton were also attributed
to the presence of PCB metabolites. Again this finding points to potential
widespread environmental problems; later we will show in an ecosystem naturally
high in PCB's that little grazing occurs. The accumulation of PCB's by
zooplankton was increased by the addition of detritus. We suspect that
detritus binds PCB's and removes them from the dissolved pool; it also in-
creases their availability to the higher trophic levels.
Secondly, we examined the inhibition (stimulation) of algal photosynthesis
by low ambient concentrations of hexachlorobiphenyl and dichlorobiphenyl.
i
The former was considered because of higher toxicity and slower ~degradabil"lty,
while the latter degrades more rapidly. We asked whether ambient levels of
5 to 500 ng_l were inhibitory. Both the intermediate hydxoxylated. and
final degradation products-(furans) were used, in addition-to the parent
isomer. "The natural phytoplankton populations in'Saginaw Bay were utllTi'zed
for in situ-estimates of productivity, with appropriate controls-in—aH-ex—
perimental series.
Ambient levels of PCBrs (hexa- and dichlorobiphenyl) inhibited nanno-
plankton productivity. In the hexa- series the hydroxylated intermediates and
the dibenzofuran were more inhibitory than the-parent- isomer in-surface-
waters (seasonal range of inhibition of -2 to -93%). At depth, the parent
hexachlorobiphenyl and degradation products stimulated carbon fixation
(seasonal range or +7 to +572). This is a new and striking result! Total
average inhibition in the Saginaw Bay ecosystem is usually less than 10%, but
may average 30% during periods of high spring runoff. The lower threshold
for inhibition of photosyntheses was 5 ng 1 PCB, an order of magnitude
lower than previously reported.
In the dichlorobiphenyl series, inhibition of photosynthesis occured in
surface waters, where botn the hydroxylated intermediate and furan reduced
photosynthesis about 7% (range -6 to -22%), much less than that by the higher
A
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chloronated isomer. Again, low ambient levels of dichlorobiphenyl stimulated
carbon fixation at depth (seasonal range of +4 to +199%).
Light levels determined whether PCB's stimulated or inhibited algal
photosynthesis. At-depths-(2,5-5-m) with-2-10% of—surface light-intensity
PCB's were stinulatory. The level of. chloronation was also a factor, as
higher chloronation produced more inhibition. Thirdly, the inhibition of
f,
algal photosynthesis increased with the partition coefficients (log P) of the
isomer. In this respect, the hydroxylated intermediate degradation products
/
were much more toxic than their partition coefficients would indicate.
Thirdly, we examined the long term toxicity of PCB's to the crustacean
Diaptomus. Natural exposure levels of 100 ng ,1~ to 10 yg 1~ resulted in
significant mortality in the laboratory.—Such higher values-are not-encountered-
in Saginaw Bay.
Lastly, we considered natural zooplankton grazing as a control~upon
phytoplankton populations ~i) Saginaw Bay and Western Lake ^rie. In Saginaw
Bay, some unknown environmental factor leads to significant inhibition of
grazing. Populations of zooplankton consumed 66% less phytoplankton than
they did in the open waters of Lake Huron. Such inhibition of grazing was
not related to unusual abundances of blue-green algae. Since we have shown
in this report that PCB's inhibit grazing in field situations, chemical
inhibition is a possibility in Saginaw Bay. This is a serious environmental
consequence, with obvious implications for* reduced water quality.
la western Lake Erie, zooplankton grazing was only 37% less than levels
observed in the open waters of Lake Huron. Apparently the Lake Erie ecosystem
is in better shape than Saginaw Bay.
Ecosystem inhibition by toxic chemicals is a serious environmental problem.
Our results indicate that levels of available PCB's should be held beJow
5 ng 1 (ppt) in Great Lakes waters. Natural levels of PCB's in Saginaw
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Bzy currently reach 316 ng 1 . Since the degradation products of PCB's are
so toxic at ambient levels, we suggest strongly that the USEPA fund additioral
studies concerning these compounds.
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SECTION-3- ,:
RECOMMENDATIONS
3.1 RECOMMENDATIONS FOR WATER QUALITY CRITERIA ON PCB'S
The ^oxic Substance Control Act has banned a well known and rightfully
feared class of persistent toxic chemicals, tha polychlorinated biphenyls.-
Considerable justification has been provided (Nisbet, 1977)--for—the~estab-'
lishment of a 1 ng 1 (1 ppt) level for natural waters. We must "both agree
and work to support this criteria, as we have shown (Section 5.2) a signifi-
cant effect-on-photosynthesis upon exposure -of -phytoplankton-to—5-ng-l
However, our mosfimmedi'ate responsibility Ts to protect the food fishes from
contamination. Lake Huron, <-'ith 5-316 ng 1 in.Saginaw Bay,-produces .fishes.
occupying lower trophic leve >, as the alewife, with PCB levels of 0.1-0.6
ppin; more importantly, popular food fishes like the walleye, likely a compon-
ent of trophic level-five, are contaminated -at unacceptably high levels (0.3-
2.5 ppm), while the lake trout, the species considered by the International
Joint Commission for revitalization in the upper lakes, is a very effective
accumulator of PCB's, with levels of 0.2-1.8 ppm in Lake Superior. The
splake, a lake trout x brook trout hybrid, had PCB levels of 0.3^1.5 ppm in
Lake Huron, and the bloater, an oily species of chub, levels of "5-6/4";jpm
(Frank e_t al^., 1979) Clearly a cutoff of 25 ppt won't help, as shown by Lake
Michigan. Logically 5 ppt PCB is a better objective, but levels below 1
total PCB must be our ultimate goal.
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3.2 RECOMMENDATION FOR FUTURE RESEARCH
The ecosystem approach must be utilized to a greater extent in testing
"persistent contaminants and their degradation products. Utilizing a single
species of algae, as shown in many studies/ gives very different response to
a given exposure to PCB's than an intact phytoplankton community gives. The
ecosystem approach utilizes the built-in interactions inherent to all ecosys-
tems, whether the components tend to act synergistically or not. Moreover, in
considering the ecysystem approach to an analysis of contaminant_e£fects,_ the
investigator is forced to involve related factors. In this particular study
we discovered that PCB's stimulate carbon fixation at low light levels. We
would not have made this discovery if we had grown a typical test algae in the
presence of PCB's in a lighted growth chamber.
The U.S.-E.P.A. should provide support for studies of the degradation.
products of" PCB's. We have shovm that the intermediate hydroxylated products
are more toxic than the chlorinated dibenzofurans. Yet we have no idea of the
prevalence of such compounds in Lake Huron ,or any of the other Great Lakes.
One of sciences saving graces is the ability of individuals to predict where
problems will occur. From studies off DDT we realized that related-degrada-
tion- products behaved differently than the initial compound. Yet we have been
slow to examine the environmental hazzards of other common metabolites.
Biologists studying the Great Lakes must consider the role of detritus
in scrubbing toxic compounds from the water column, removing.them from the
pelagic food chain (and introducing them to the benthic food web). Lake
Superior, with its continued atmospheric inputs of PCB's, may ultimately be
more difficult to decontaminate because of its relatively low productivity of
algae, and thus the low levels of particulate organj.cs (detritus).
10
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The waters of Saginaw Bay, with 5 -316ppt PCB, must be considered pol-
luted. In effect, that pollution has created local investigations of which
this is a component. Our findings regarding the effects of PCB's on the food
chain in Saginaw Bay suggest that strong measures are required to limit inputs
of PCB's to the Bay and ultimately the Lake. New creative measures to hold
PCB's in river muds or to expedite their removal may be necessary.
A very basic biological problem common to all polluted ecosystems and all
organisms must be tackled. We have examined the effects of- PCB's-on a> few
components of a natural system. Yet from these short-term experiments (4 hr
or 30 days) we have no insight into the long-term adaptation of the plankton
and fishes to PCB's. Short-term studies of physiological acclimation-by
phytoplankton and zooplankton to PCB's are needed; long-term studies of genet-
ic-adaptation are vital. It is certain that the phytoplankton, still abundant
in Saginaw Bay, have adaptc^ more rapidly to PCB's than humans have!
11
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SECTION 4
EXPERIMENTAL PROCEDURES
4.1 METHODS FOR DETERMINING EFFECTS OF PCB'S ON THE SAGINAW BAY ECOSYSTEM
An abbreviated diagram of the ecosystem carbon flow experiment indicates
the findings expected from the four treatments effecting both algal photosyn-
thesis and zooplankton grazing (Table 1).
Phytoplankton methods
*The natural assemblage of phytoplankton was harvested from 2 m depth
with a pump. Polyethelene bottles of 1 1 capacity were filled with lakewater
and stored in the dark. All bottles were poured gently through 22 pm aperture
nitex to separate out the netplankton, which were then resuspended in filtered
lakewater. Controls were run upon and treatments applied to both nannoplank-
ton and netplankton, which were then incubated in situ for 4 to 5 hr. about a
time of midday.
The treatments were applied in the following fashion. An amount of a
strong surfactant, Triton X-100, was added to appropriate bottles'" for a final""
concentration of 0.01%. This concentration of Triton alone was shown not to
inhibit photosynthesis. Bottom sediments were harvested with a PONAR dredge;
fine surface sediments were resuspended, allowed to settle, and the remaining
fine sediments (200 ml) added to the phytoplankton. These treatments were
14
applied following the addition of C-bicarbonate and preceeding the additipn
of 3H-PCB's.
Finally 2,2' dichlorobiphenyl in 3 ml acetone was added for a final con-
12
-------
TABLE 1 . DESIGN OF EXPERIMENT TO OBSERVE EFFECTS OF PCB'S ON
' CARBON FLOW IN SAGINAW BAY ECOSYSTEM
' 1
1 •
14
Control: C
bicarbonate
Phytoplankton a) control
upon pri-
mary pro-
ductivity
(mgCm~3 hi
Control and Treatments (4)
1 :
Treatment 1:
14C 4- JH-PCB
a) inhibition
photosynthe-
sis by PCB's
Treatment 2: Treatment 4:
14C +• H-PCB Treatment 3: *4c +
+ surfactant •*• detritus -PCB metabolites
a) reduction a)
in inhibi-
tion of
photosynthe-
sis
reduction a)
in inhibi-
tion of
photosynthe-
sis by PCB's
inhibition
of photo-
synthesis
by metabo-
lites
b) accumulation b) reduction b) particulate b) accumulation
rcn'o by phy- in PCB compotitibn of motnho-
toplanktori binding for PCB's lites by
phytoplank-
ton
^ooplankton
a) control
upon zoo-
plankton
ingestion
a)
inhibition
ingestion L ,'
PCB's
reduced in- a) reduced or
gestion increased
PCB's in PCB's in
food food
b) accumulation b)
PCB's by zoo-
plankton
reduced ac- b)
cumulation
PCB's via
food
reduced or
increased
accumulation
of PCB's via
foods
a) inhibition
of ingestion
by metabo-
lites
b) accumulation
of metabo-
lites by
zooplankton
-------
centratioii of- 100 ng I"1 or 25 pg 1 . The PCB's were added following the
addition of either the surfactant or the detritus. The 2,2' PCB was tritiatfid
by New England Nuclear and had a specific activity of 2.0rcCi/mg. This pro-
vides appropriate counts from an aliquot of 100 ml of 100,000 to 400,000 dpm.
Following incubation for 4-5 hr, the samples were brought to the surface.
Two subsamples of 100 ml each were filtered through glass iiber filters (GC),
which were then ground in scintillation cocktail. The filter/cocfctail solu--
tion was placed in a scintillation vial for counting in the laboratory.
In the laboratory the Beckman 200 scintillation counter was calibrated
for best results in this double tag experiment. The efficiency or the counter
was compared to the external standard ratio (ESR) measured with each counted
sample-. An appropriate 4fc" order polynomial was fitted, using a stepwise re-
gression analysis. In data reduction, corrected C counts were calculated
by selecting efficiencies indicated by appropriate ESR values.
Phytoplankton productivity was determined as outlined by Wetzel (1969).
Zooplankton methods
The natural assemblage of zooplantkon was collected with a 64 pm aperture
net, vital to the inclusion of small herbivores like nauplii. These zooplank-
ton were acclimated to ambient food concentrations for 2 hr. Then they were
placed into the hotf phytoplankton (with some phytoplankton foods treated by
the 4 applications outlined). The zooplankton were allowed to feed for 15
min, following which they were- filtered onto 2 coarse Whatman paper, narco-
tized with CO -water, and killed with hot water.
In the laboratory, 50 animals of each species were hand-picked and
placed in scintillation vials. Usually four replicates of each common spe-
cies were picked. The zooplankton were digested in Protosol at 53°C and
-------
counted in the Beckman counter. Efficiencies for C counting were determined
as outlined above. Filtering rates were calculated according to the methods
of Rigler (1971).
Preparation of metabolites
The 3H-2,2' dichlorobiphenyl was activated to the metabolite (likely a
mixture of hydroxylated products and chlorinated dibenzofurans) by the use of
the nixed microsomal function oxydose (MMFO) system of the rat liver (Shimada,
1976). We thank Jay Fisher and Ruth Anderson for preparation of these metabo-
Iftes.
4.2 METHODS FOR DETERMINING EFFECTS OF PCB'S UPON CARBON FIXATION
Exposure levels of PCB's were matched to ambient levels in Saginaw Bay
in an attempt to determine thresholds for inhibition of photosynthesis. Two
isomers, dichlorobiphenyl and hexachlorobiphenyl w^.re used, along with their
probable degradation prod'C' -J.
»
Isomers and degradation products
The -simulated hexachlorobit>henyl series tested in 1978 was obtained from
the RFR Corp. and consisted of 2,2',4,4*,5,5' hexachlorobiphenyl (RFR No.
RFC 047), 2',3',3t,3,3'-pentachloro-2-biphenol (RPM-25), and octachlorodihen-
zofuran (RPE-19). The simulated dichlorobiphenyl series tested in~1979 con-
sisted of 2,2' dichlorobiphenyl (RPC-009), 4,4* dichloro-3,3' biphenydiol
(RPM-14) and 2,8-dichlorobenzofuran (RPE-18).
Phytoplankton methods
Phytoplankton were collected at depths of 0.5, 2,5 and 5.0 meters by
pump. The nannoplankton (< 22 Un diameter) were spearated from the netplank-
ton (> 22 ynr.), which were resuspended in filtered lake water. Controls con-
sisted of either sized plankton innoculated with 50 uci C-bicarbonate and
15
-------
incubated at the three depths of collection (total of 6 bottles). Experimen-
tal incubations of both nanno- and netplankton were treated with 5, 100 and
500 ng 1 of the parent isomer, and 100 ng 1 of the hydroxylated metabolite
-and the fur an. The PCB-'s-were dissolved in 1 ml-of-acetone-and-frozen-prior
to use. Thus 10 experimental incubations were made at each depth, for a total
of 30 bottles.
Phytoplankton controls and treatments were incubated for 4 hr in situ.
After that time the bottles were brought to the surface. Two ICO ml subsara-
ples were taken from each of 36 bottles and filtered through a glass fiber
(GC) filter, which was then ground in scintillation cocktail. The-ground fil-
ter was diluted with cocktail to a constant volume 'in a scintillation vial and
returned-to the laboratory for counting. All work with PCB's was-conducted
by investigators wearing face~masks—(respirometers)~.~~J —
Calculations of phytoplankton productivity were made using standard pro-
cedures (Wetzel, 19S9) following scintillation counting in the laboratory.
All counts were corrected for counting efficiency.
Light measurements
Measurements of light intensity at depth were made with a Montodoro
(LMT-8A) light meter. Readings were expressed a-s-~a percentage of sun's inten-
sity in late June (at maximum azimuth). This gave us a measure ct relative
intensity over a growing season, as compared to the commonly employed % sur-
face intensity.
4.3 METHODS FOR DETHRMINING EFFECTS OF CHROMIC EXPOSURE TO PCB'S
Experimental procedures
Zooplankton from Lake Hurcn via the Detroit River were collected in a net
of 64 pm aperture and brought into the laboratory. Ten zooplankton of the
16
-------
genus Diaptomus were handpicked and placed into glass tissue culture bottles
containing filtered river water. These culture bottles were then corked and
attached to silicon tubing from a manostatic pump. The puaip drew water from
-four stock bottles containing three concentrations of dichlorobiphenyl (100-
ng 1 , 1 lag I"1, and 10 Ug 1~ ), and the control water. Five culture flasks
containing 10 zooplankcon each served as controls. Each of three-concentra-
tions of PCB's were pumped through 5 additional flasks, to make a total of 2O
flasks containing 200 animals per experiment. The rate of pumping of PCB's
could be varied from 0-9 ml hr"1; we selected 1 ml hr"1.
Twice each day the 20 culture flasks were examined with a hand lens to
determine the number of animals alive (swimming) and' those values recorded in
tabular form, as summarized in the results.
Problems with procedure
The obvious lack of effect of 2,2'—dichlorobiphenyl on the_survivorship
df~Di'aptomus prompted a c:' t£ul analysis of" the concentrations of dichlorobi-
*
-phenyl reaching the culture flasks-.
In the experiment of 12 March 1979, the stock bottles were teflon and
silicon tubing was used to carry water to the culture flasks. The concentra-
tion of PCB in the more dilute stock bottle was expected to be 3.43 pg 1~ ;
-it-was~ never observed-above detectable limits. - The—concentration- of-PCB-in-
the more concentrated bottle was expected to be 200 pg I"*; it varied between
0 and 27 yg 1~ . Obvious problems existed in maintaining desired concentra-
tions of PCB.
Therefore in planning the experiment of 24 March 1980, we used glass
stock bottles and tubing, with the employment of silicon tubing only within
the pump itself. Over a period of days 0 to 7, the PCB concentration in the
17
-------
bottle expected to be 3.8 yg 1 varied from 3.0 to 0.3, with a regularly de-
creasing concentration. The concentration in the 20 yg 1~ stock bottle
varied from a high of 7.4 yg 1-1 on day 1 to a low of 1.7 yg 1 on day 7.
-Because of severe problems-regarding-the-concentrations of-PCB'-s—to-
which organisms were subjected, we .will-limit-the presentation and discussion-
of these data.
**
4.4 METHODS FOR ASSESSING ZOOPIANKTON GRAZING
For total grazing a modification-was-used,of-the original-methods^-of
' 14
Nauwerck, who determined grazing using tagged ( C) phytoplankton. The radio-
activity of zooplankton was measured, after a brief feeding period (15 min),
too short for the production of radioactive faeces at low food levels. Before
being given radioactive food, the animals were acclimated for l.-'hr~in~non—-
radioactive cells of the same natural assemblage tagged with Na CO . -Approx-
imately 2000 animals were acclimated in 600 ml of natural algae in lakewater...
After 1 hr, 400 ml of tagged food was added. The animals were then allowed
to feed on the hot mixture for 15-30 min. They were relaxed with CO- water,
killed with boiling water, and preserved. Each experiment was run in quadru-
plicate. In the laboratory animals were picked, using a 1 mm. diameter metal
loop, carefully avoiding the_ removal.. o£-large-filamentous algae— Approxi-
mately 50 animals were placed in a scintillation vial and digested with
Protosol (New England tiaclear); after 24 hr at 60°C, the vials were filled
with 10 ml of cocktail. All samples were placed in the dark for 24 hr to
eliminate chemoluminescence, and then counted in a Beckman Model 133 liquid
scintillation counter. Typically zooplankton samples were counted with an
efficiency of 95%, as contrasted to phytoplankton foods counted at 65% effi-
ciency.
18
-------
For selective grazing, techniques similar to the above were employed,
except that food resources were size-fractionated. The natural assemblage of
phytoplankton was passed through a fine net (22 Vim), leaving the nannoplank-
ton (< 22 Urn) in the lakewater and removing the netplankton (> 22 um), which
14
was-resuspended in-filtered (0/45 Urn) lakewater. Tagged ( C) nannoplankton,
following a 4 hr in situ incubation, were mixeu with cold netplankton to re-
constitute the natural assemblage. In- a similar manner, tagged netplankton
were mixed with cold nannoplankton just before feeding. The natural assem-
blage of herbivores, already acclimated to their food assemblage, was reac-
climated for 1 hr in water-cooled shipboard tanks. Animals accliminated in
400 ml lakewater were fed 600 ml hot food. After feeding-for 12-15 min the
animals were killed and preserved.
Assimilation was calculated"by feeding animals for 2 hr, as above, and
then removing them and placing them in cold food for 4 hr, during-which time
any hot food would be elian'-.Ated from the gut. Assimilated food, was measured
as above, using liquid scin'^.llation techniques. Percentage-assrmriation
(Sorokin, 1968) was calcualted from the ratio mgC assimilated hr :mgC in-
gested hr" .
19
-------
4.5 LOCATION OF EXPERIMENTS
Saginaw Bay, Lake Huron
—The-effect-of-algal—productivity on zooplankton grazing was examined on
Saginaw Bay during 1976, while the effects of PCB's on food chain dynamics
were studied from 1977 through 1979. In 1976 all feeding experiments were
conducted in Segment III at Station 56, west of Fish Point (Figure 1). In
1977 the effects of PCB's on phytoplankton photosynthesis and zooplankton-
ingestion were measured at the same station. During 1978 and~~1979~the effects
of low (ambient) concentrations of PCB's were .usually studied-at Station 56,
but in both years strong September storms forced skipper Ed McHugh-ind crew
to-seek the-shelter— of- the leeward shore-at Station 2, southeast of~~Nayanquing
Point. Station-56—was~originally selecteir"because it was characterized by
-the highest algal productivity in the_Bay_.
Western Lake Erie
The effect of algal productivity on zooplankton grazing was likewise
examined in Lake Erie. The Ohio State University motor vessel Hydra, under
the leadership of Denny NayIon was anchored for all studies at Station 59,
just 2 miles SW of West Sister Island. In times of high westerly winds, the
vessel was moved to Station 59 North in the leeward of West Sister Island.
2C
-------
IO
LAKE HDEOM
• $ AGIN AW BAY
Figure 1. Location of studies op Saginaw Bay, Lake Huron.
-------
N>
\
DETROIT
RIVER
CANADA
HURON RIVER
WEST
SISTER, 59 N
V
BASS
ISLAND
KELLEY'S
ISLAND
LAKEEHIE.
Figure 2. Location of studies on Western Lake Erie,
-------
5,1 EFFECTS OF PCB'S UPOM CARBON TLOW I» THE SAGINAW BAY ECOSYSTEM
Purpose
The upper, food producing levels of aquatic ecosystems in the Great
Lakes are based upon planktonic food chains. The basic processes of primary
productivity by phy top lank ton and grazing by zooplankton may be impared by
toxic substances. We proposed to examine the important fluxes and standing
crops of the Huron ecosystem. A controlled experiment, utilizing tagged
PCB's in various treatments, was designed to meet our six basic purposes in-
cluding:
1. to measure the effects of PCB's on carbon fixation by phy top lank ton,
2. to measure the effects of PCB's on the grazing rates of zooplankton;
in addition, to examine the resultant accumulation of PCB's in zoo-
plankton,
_3._ .to .estimate, the relative role of adsorption (binding) in the concen-
tration of PCB's ' i upper t*ophic levels,
4. to estimate the role of detritus in concentration PCB's in the
food chain,
5. to measure the inhibition of the above fluxes of carbon (to algae
and zooplankton by PCB metabolites,
6. to examine the seasonal effects of PCB's on the algae (selective
inhibition of major groups of algae).
Detailed Results of Field Experiments
Experiment of 23 May 1977—
Phytoplankton productivity was markedly reduced by PCB's. Phytoplankton
populations were dominated by diatoms (94% biovolume). The important genera
were Asterionella formosa, Cyclotella, Diatoma, Melosira islandica, Stephano-
23
-------
discus binderanus, and Tabellaria fenestrata. The non-diatoms were rare, and
consisted of Cryptomonas orata and Dinobryon divergans (2.8% biovolume) and
bluegreens (2.1%) (pers. comm., E. Stoenner).
In this initial experiment, phytoplankton populations received a treat-
ment of 100 ng 1 , 2,2'dichlorobiphenyl. The- rate of carbon fixation by the
nannoplankton (< 22 pm diameter) was reduced from 3.72 mgCm hr to-1.78, a
reduction of 52%. With the addition of a surfactant (0.01% Triton), carbon
fixation-was reduced to 2.48 mgCm hr , a reduction of only 33%. Thus
bnding of PCB's was an important mechanism in the inhibition of nannoplankton
photosynthesis. At the same time the netplankton productivity was not-ef-
fected (Table 2).
Grazing by zooplankton was not reduced significantly by the- addition-of
100 ng 1 dichlorobiphenyl (Table 3). Copepod nauplii and copepodites, as
~weH-as-adult- Chydorus sphaericus, failed-to exhibit significant reductions-
in filtering rates in the presence of PCB's. This conclusion applies to both
nannoplankton and netplankton foods.
However, the addition of organic detritus caused the same animals to
filter more rapidly. Thus detritus was likely a preferred food; it also
carries adsorbed PCB and should significantly increase the intake of PCB's by
these animals (Table 4 ).
Experiment of 9 July 1977—
The treatment levels with PCB's and metabolites were increased to 25 Jjg
1 to follow the effects on the zooplankton more closely. In addition, the
PCB's were tritiated, utilizing the double tag (C and H ) technique for
the first time in this study.
Phytoplankton populations were comprised'of greens (44.3% biovolume).
24
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TABLE 2 . EFFECT ON PHYTOSYNTHETIC RATES (mgCra hr ) OF NATURAL NANNOPHYTO-
PLANKTON (< 22 U) AND NETPHYTOPLANKTON (> 22 p) POPULATIONS OF ADDITON OF 100
ng 1~L 2-2' DICHLOROBIPHENYL. MAY 28, 1977 AT STATION S56,
SAGINAW BAY, LAKE HURON ;
Population Size Class -
Treatment Nannoplankton Netplankton Total
Control 3.72 +_ .09 1.76 £ .14 5.48
100 ng 1-1 2-2' PCB 1.78 +_ .12 1.86 + .16 3.64
100 ng 1-1 2-21 PCB 2.48 ± .06 1.38 + .05 3.86
+ 0.01% Triton
25
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TABLE 3 . FILTRATION RATES (ml an'1 hr"1) OF DOMINANT SPECIES OP ZOOPLANKTON FED
NATURAL POPULATIONS OF PHYTOPLANKTON GROW IN 100 ng 1~1 DICHLOROBIPHENYL, 28-29
MAY 1977 :
; : 1 • - -
Species or Life Stage
Copepods
Copepod nauplii
Cyclopoid copepodites
Cyclops bicuspidatus(A)
Filtering
Nannoplankton (<22y)
with 100 ppt
Control PCB
0.00210
0.002i0.001
i !
0.00610.001
0.004±0.002 0.
0.00410.001 0.
0.
Rates Upon
Netplankton (>22u)
with 100
ng I"1
Control PCB
OOStO.OOl 0.004±0
007±0.001 0.004±0.
003±0.001
with 100
ng 1-1
PCB+
detritus
0.024
001 0.027
Cladocerans
Chydorus sphaericus
0.00440.001 0.00510.001 0.00810.002 0.00510-001 0.025
-------
bluegreens (33.0%), flagellates (6%), and diatoms (16%).
Carbon fixation by the phytoplankton was reduced 68% with the addition
of 25 Ug !"*• dichlorobiphenyl. The fixation by nannoplankton was reduced 53%,
whereas the netplankton was reduced 74.6% (Table 4).
When the surfactant was added, the fixation by nannoplankton was reduced
only 36.1% by PCB's, as opposed to 53% without, a significant alleviation of
both binding and inhibition, Inhibition of nannoplankton algae by PCB's may
thus be related to surface binding. However, the net algae behaved different-
ly. Fixation of carbon was reduced 74.6% without the surfactant, and 68% with
the addition. It appeared that binding was not so important a factor in con-
centrating PCB's in the case of net algae, many of which were bluegreens"
(Table 4 ).
PCB metabolites had a very inhibitory effect on carbon fixation. Separ-
ate tests were not performed on the different size classes of algae. How-
ever, total carbon fixatio" vas reduced from 5-54 mgCm ht~ "to 0:7, a re-
duction (inhibition) of 87. T (Table 4). Obviously-metabolites-of—PGB'-s-are-
more toxic than the parent isozner.
Accumulation rates by algae of dichlorcbiphenyl wera also estimated,
using the H tag. The nannoplankton accumulated 0.013% hr of their dry
weight in PCB's, whereas the-netplankton accumulated 0.079% -hr . -The-sur-
factant did not reduce accumulation rates (Table 5 ). We thus see that while
nannoplankton, the base of the food chain, accumulate less the impact on
carbon fixation is very great. Indeed the nannoplankton are very sensitive
to PCB's.
The effect of PCB's on the filtering rate of zooplankton of 9^ July was
not significant. The zooplankton filtered just as much algae in the presence
27
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TABLE 4. EFFECT ON PHOTOSYNTHETIC RATES (mgCm~3 hr"1) OF NATURAL
.NANNOPLANKTQN (<-22-ym) AND.NETPLANKTON (> 22 Um) OF 25 Ug l"1 2-2'
DICHLOROBIPHENYL. JULY 9, 1977 AT STATION S56, SAGINAH BAY, LAKE HURON
Treatment
Control
25 ppb 2-2' PCS
25 ppb 2-2' PCB
+0.01% Triton
25 ppb 2-2' PCB
metabolites
Population Size Class
Nannoplankton Netplankton Total
1.63 +_ .10 3.91 + .19 5.54
.77 + .05 .99 + .08 1.76
1.34 +_ .07 1.30 i .05 2.64
0.7
TABLE 5 . AMOUNT (% DRY WT HR"1 x 10 ) OF 2-2' PCB (25 yg l" )
ACCUMULATED BY ALGAE DURING 4 HR INCUBATION. JULY 9, 1977
SAGI'NAW BAY, LAKE HURON
- •
Treatment
25 ppb 2-2' PCB
25 ppb 2-2' FCB
Algae
Nannoplankton
1.31
1.61
Size Class
Netplankton
7.92
8.74
Total
-2.52-
2.91
+ 0.01% Triton
28
-------
of PCB's as they did in natural waters (Table 4 ). "However, this dues not
mean that PCB's do not effect the zooplankton, as we will discuss later.
Experiment of 28 July 1977 —
Phytoplankton populations were dominants in Saginaw Bay in late July by
green algae (73.5% biovol'une) including Oocystis and Cosmarium; bluegreens
(14.0%) including Chroococcus; flagellates (8.9%), mainly Dinobryon; and
diatoms (3.6%), including Asterionella, Surinella and Cyclotella (Stoermer,
pers. ccmm.).
;
The total carbon fixation rate on 28 July was 10.16 mgCmhr . -Di-
chlorobiphenyl (25 \ig 1 ) reduced the carbon fixation to 3.12, an inhibition
of 69%. The nannoplankton photosynthesis, being more sensitive to PCB's, was
reduced 77% and the netplankton 64% (Table 6 ) .
Adsorption of PCB's was again important. Treatment with PCB's and the
surfactant reduced carbon fixation to 5.42, only 42%, as opposed -to the-69%
reduction without
PCB metabolites reduced carbon fixation from 10.16 mgCm""* hr to 1.63,
a significant inhibition of 84% (Table 6 ) .
The accumulation of PCB's by the phytoplankton again told an important
story. rCB metabolites- accumulated more rapidly than the parent dichlorobi-
phenyl; the rate ~of~metabo lite accumulation— (.-093 — d-.w— hr — )— was— 4.-3-tisjes-
-1
faster than the rate of accumulation of the parent isomer (0.22 hr ). This
high-rate- of accumulation of metabolites by algae (Table 7 ) may be directly
related to the high level of inhibition of carbon fixation by metabolites.
The parent 2,2' PCB isomer had little effect upon zooplankton -filtering
rates. In contrast the metabolites (25 yg 1~ ) inhibited feeding by 43%.
Species affected by the parent isomer included only Daphnia retrocurva and
29
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TABLE 6. EFFECT ON PHOTOSYNTHETIC RATES (mgCm~ hr"1) OF NATURAL
pANNOPLANKTON (< 22 ym) AND NETPLANKTON (> 22 Vm) OF 25 Ug I"1 2-21
PICHLOROBIPHENYL. JULY 28, 1977, SAGINAH BAY :-
Population Size Class
Treatment Nannoplankton Netplankton Total
Control 3.65^.62 6.51^.89 10.16
25 ppb 2-21 PCB 0.81 £ .23 2.31 +,.26 3.12
25 ppb 2-21 PCB 2.36 +_ .31 3.06 £ .22 5.42
+ 0.01% Triton
25 ppb 2-2' PCB . 1.63 +_ .20
metabolites
TABLE 7. AMOUNT (% DRY WT HR"1 x 10~2) OF 2-2' PCB (25 ug- l"1)
ACCUMULAT'gD BY ALGAE DURING 4 HR INCUBATION. JULY 9, 1977, SAGINAW-BAY
Treatment
25 ppb 2-2' PCB
25 ppb~ 2-2' PCB
Algae
Nannoplankton
1.4
3.68
Size Class
Netplanktcn
4.92
6.96
Total
2.15
4.62
+ 0.01% Triton
25 ppb 2-2' PCB 9.34
metabolites
30
-------
Cyclops vernalis (Table 8). Species whose filtering rates were inhibited an.
average of 47% by the metabolites of dichlorobiphenyl included Chydorus
sphaericus, Daphnia retrocurva, Eubosmina coragoni and copepod nauplii, the
most important grazers in this ecosystem (Table 8 ).
Accumulation rates of 2,2' PCB and two mixed metabolites by zooplanktcn
were rapid. Five of seven species or stages feeding upon nannoplankton had
rater- of accumulation of 0.002 to 0.006% d.w. per 15 min. exposure (Table.9 ).
The highest rate of accumulation was by nauplii, the most active feeders in
Lake Huron (McNaught et al., 1980). Two species of Cyclops, and-Chydorus~and"
Daphnia also had high rates of accumulation when feeding on nannoplankton.
When detritus was added to nannoplankton incubated in PCB's and then fed
to zcoplankton, the rates of accumulation of PCB's increased in five of seven
cases (Table 9 ). It would appear that many zooplankton which graze on algae
-feed- simultaneously-upon detritus. In productive environments detritus is
abundant, adsorbs PCB's, a^^ thus selves to increase the PCB intake of
herbivorous organisms.
Ecosystem Impact of PCB Acute Toxicity
Experiment of 28 July 1977—
The experimental addition of 25 pg 1 2,2' PCB to the Saginaw^ Bay-eco-
-system-had-iaportant short-term consequences—(Figure—3~)~—In—this~diagranr
the flow of carbon is diagrammed with arrows and boxes and summarized on the
right side, while the effect of PCB's upon carbon flow is._suramarized_on_the
left. -
Fluxes of carbon into tha phytoplankton (controls) were reduced by 2,2'
PCB (-69%) , alleviated by surfactants, and inhibited more severely hy metabo-
lites (-84%). Bioaccumalation of H -PCB by the phytoplankton was significant
31
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TABLK 8. COMPARISON OF FILTERING RATES FOR ZOOPIANKTON FEEDING-ON-
PULATIONS GROWN AS CONTROLS, IN 25 ]ig i"1 DIC
AND IN 25 Ug I"1 METABOLITES, JULY 28, 1977
NANNOPLANKTON POPULATIONS GROWN AS CONTROLS, IN 25 ]ig i"1 DICHLOPOBIPHENYL,
Species
Chydorus sphaericus
Daphnia - retrocurva
Eubosmina coregoni
Nauplii
Cyclops vernalis
Tropocyclops prasinus
Diaptomus spp.
Filtering Rates (ml an hr
'' Control Dichlorobiphenyl
.064
.138
.071
.106
.126
.061
.087
+.031 .041 £ .017
+ .046 .254 i .008
+ .032 .038 i .034
i .009 .099
£ .063 .272 +_ .039
+_ .031 —
+ .051
~r)
Metabolites
.028
.127
.026
.049
32
-------
TABLE 9. AMOUNT OF 2-2' PCB (25 pg 1 ) ACCUMULATED (yg/g) IN 15 MIN. FEEDING
ON NANNOPLANKTON (<22ym) AND NETPLANKTON ( >22ym) WITH REGARD TO TREATMENT, JULY
28, 1977. '
Species or Stage
Chydorus sphaericus
Cyclops vernalis
Daphnia retrocurva
Eubosmina coregoni .
Nauplii
Cyclops bicuspidatus
Diaptomu-i spp. (A)
PCB
20.7
33.6
22.9
8.9
60.3
14.6
7.5
NannoplarJcton
PCB+Triton . ••
49.2
34.1
27.5
43.0
84.9
19.4
16.7
plus
K:fl+Betritus
TJbl
55.9
24.9
15.2
144-1
34. ll
" i "
28.6
PCB
95.9
18.0
13.5
~
10.7
10.9
.29.7
Netplankton
PCB+Triton
68.1
51.8
32.2
12.6
53.4 '
26.9
26.0
plus
PCB+Detritus
1.6
'13.4
i
11.0
7.0
86.8
0.2
1.7
Mean
24.1
39.3
53.9
29.8
38.7
17.4
-------
UXE HURON
23 JULY 1977
PCB BlOArrilMllI ATION
CARBON FLUXES
fCD ACCUMULATION BY JOpPLANKTOM
BlOACCUHULATION NOT REDUCED
SURFACTANT
BlOACCUHULATION INCREASED
DETRITUS (•*• 2.2 X)
PCB ACCUMULATION BY ALCAf
I
BIOACOmULATIOK IS0.1ER (1 x)
I . >
BIOACCUMUUTION MET. (+ 4.3 X)
SORPTION • 33Z BlOACCUHULATION
ZOOPLANKTON
f.
EbYIQPUNKTON
73. 51, GREENS
(pocysTis.
fjP$MAR|UM)
GRAZING FLUX
2 S?PB PCB ± OX
2 5PPB METABOLITES - 43X
PHODUCT1VIT|| FLUX .•
25 PPB PCB • -69X
25 PPB PCB t SURFAC-
TANT • -46X
25
PCB METABOLITES
B-SORPT10N
METABOLITES
I •»
Figure 3. Ecosystem impact of experimental addition of
25 yg'l-1 dichlorobiphenyl, including inhibition of
carbon flow (right column) and accumulation of PCB
with trophic levels (left column).
-------
with the relative bioaccumulation noted (IX). The bioaccumulation of PCB
metabolites exceeded that of the parent isomer by a factor of 4.3 X.
Zooplankton grazed upon these experimental phytoplankton populations, in
this instance composed of the green algae Oocystis and Cosmarium. The grazing
rate of the zooplankton ( controls ) was not reduced by 2b yg 1 , 2,2' PCB.
This was not a fortunate circumstance as it might seem, since they therefore
ingested PCB rich algae and then bioaccumulated PCB. However, the PCB metab-
olites were apparently acutely toxic to zooplankton, inhibiting ingestion of
i
' phytopiankton by-43%. The ultimate bioaccumulation of 2,2' PCB--by the..zoo-
plankton was not significantly affected by reducing adsorption of PCB's on
algae. Bioaccumulation of 2,2' PCB by zooplankton was increased when datri-
tus was added to tae nannoplankton foods (Figure 3).
Relative Toxicity of 2,2' PCB and Metabolites to Phytopiankton
The relative toxicity of 2,2* FCB and its metabolites to phytopiankton
must be determined relativ co the drse received, and not simply the environ-
i
mental exposure. Th exposure was determined from the amount of H -PCB added
to the phytopiankton cultures. The dose was calculated from H uptake, and
the relative acute toxicity of 2,2" PCB from phytopiankton carbon fixation
relative to the photosynthesis in the control cultures.
The-effect of 25 \iq 1~ of the~parent_2,2-1_PCB_upon nanno- and netplank-
ton, as well as the effect of the metabolites on the total phytopiankton as-
semblage is summarized for the cruises of 9 July and 28 July 1977 (Table 10).
The inhibitory effect of the PCB on photosynthesis (% dec) divided by the
dose (PCB accumulation in 4 hr) gives an estimate of relative toxicity.
Based on dose, the parent isomer of 2,2' PCB is more toxic to the nannoplank-
ton (40.5, 55.0) than the netplankton (9.3, 13.1) by a factor fo 4.3 X. The
35
-------
TABLE 1O. RELATIVE LEVELS OF TOXICITY OP PARENT PCB ISOMER (2-2*) AND PCS
METABOLITES TO SMALL AND LARGE ALGAE
% Decrease in Relative
Size PCB Photosynthesis PCB Accumulation Toxicity
Phytcplankton Product Rate (%d.vr./4hrs) (%dec/%d.w. )
nanno
nanno
net (>
net (>
total
{< 22 jJin) Parent Isomer 53 1.31 x 10
(< 22 Um) Parent Isomer 77 1.40
22 um) Parent Isomer 74 7.92
22 }im) Parent Isomer 64 4.90
(all sizes) Metabolites 84 9.30
40.5
55.0
9.3
1-3.1
9.0
TABLE! 1 . MECHANISM OF PHOTOSYNTHETIC AFFECT. SORPTION OF PCB'S ON CELL
WALL INVOLVED IF SURFACTANT INCREASES PHOTOSWTHESIS ABOVE
LEVEL OF TREATMENT (PCB)
Size Phytoplankton
nanno (< 22 pm)
nanno (< 22 pm)
net (> 22 ym)
net (> 22 yjm)
Increase in Photosynthesis
PCB S Surfactant
36%
42%
8%
0%
Forms
small diatoms
small diatoms
large bluegreens
large bluegreens
36
-------
metabolites are less toxic than the parent isomer per unit dose, but in field
experiments more metabolites are accumulated, accounting for greater de-
creases in photosynthesis at constant levels of exposure. It is expected
that the metabolites bind nore actively than the parent isomer.
Mechanisms of Algal Inhibition
Field studies suggest that phytoplankton taxa adsorb PCB's to different
degrees. If we select field data illustrating inhibition of carbon fixation,
wherein the phytoplankton in a given size group (nanno- or netplankton) are
of chiefly one order, we gain insight into one possible mechanism.
Data from two months are presented (Table 11). The nannoplankton
were predominantly small diatoms and greens, whereas the netplankton
were composed of greens.
The experiment is interpreted as follows-. In all cases the addition of
dichlorobiphenyl (25 \iq 1 ) inhibited photosynthesis. In parallel experi-
mental series, the additic- jf a surfactant with the PCB either acrain in-
»
creased photosynthesis, or affected the PCB treatment very little. -Where
diatoms and greens were involved, the addition of a surfactant with the PCB
led to an alleviation of inhibition. Thus we interpret these results to
mean that binding to cell walls/membranes was reduced. Where bluegreens. were_
involved, the addition of a surfactant with,the-P.CB-di d not-increase-photo-
synthesis. Bluegreens are surrounding with a hydrophilic sheath which may
interfere with binding PCB's. Thus bluegreens may not initially-suffer from
PCB's to the degree which diatoms and greens do. Bluegreens and other
sheathed forns may have a selective advantage in environments polluted with
PCB's.
37
-------
Summary of Effects of PCS's on Carbon Flow
1. The parent isozner, 2,2' PCB was more toxic (inhibitory to carbon fixation)
to nannoplankton than netplankton.
2. On the basis of exposure, PCB metabolites were more toxic than the parent
2,2' PCB.
3. The greatest reductions by PCB's were in photosynthetic rates of diatoms
and green algae.
4. Sorption or binding was a significant factor in the accumulation of PCB's
by phytoplanktoa .(excluding-bluegreens).
5. Zobplankton feeding rates were not affected by 2,2' PCB.
6. Zooplankton feeding rates were reduced by 2,2 PCB metabolites.
7. The accumulation of PCB's in zooplankton was increased through the addi-
tion of detritus.
8. In an evolutionary sense, PCB's may increase the fitness of bluegreens-at
the expense of diatoms.
38
-------
5.2 INHIBITION OF NATURAL PHYTOPLANKTON PHOTOSYNTHESIS AT ENVIRONMENTAL CON-
CONCENTRATIONS CF PCB'S AND METABOLITES
Purpose
PCB's are present in the waters of Saginaw Bay (Station 56), xake Huron,
at concentrations of 5-316 ng 1 (Table 12). We originally proposed to exam-
ine the inhibitory effects of PCB's and' their degradation products upon algal
photosynthesis. In the process of this investigation, as clearly shown in
the results which follow, we made the important discovery that PCB's also
stimulate carbon fixation by phytoplankton. These two specific implications
are examined for natural mixed populations of nannoplankton (> 22 jam diameter)
and netplankton (> 22 yin diameter).
Description of Phytoplankton Populations
During the summer of 1978 diatoms constituted 1.4 to 43.8%--of the nanno-
planktic biovolume in Saginaw .Bay (Table 13).. Melosira was far the dominant
genus. In contrast, non-di • corns made u? 56.2 to 98.6% of the nannoplankton.
i
*
The small non-diatoms were c..iefly Anabaena and Scenedesmus-spp. -(Table-"!3)'.
Thus the nannoplankton was comprised of diatoms, greens and bluegreens, with
a cryptomonad present during May.
The netplanktic biomass in Ssginaw Day during 1978 was also dominanted
by-diatoms and greens. Bluegreens were-relatively unimportant. Diatoms-con-
stituted 23.4 to 98.7% of the biomass of large cells. Stephanodiscus niagarae
was overwhelmingly dominant in terms of total biomass. Tabellaria, Asterio-
nella, and Fragillaria wera of lesser importance. Large non-diatoms present
were Pediastrum and Staurastrom (Table 14).
During 1979 very similar populations cf phytoplankton served as -test
organisms for assessing the impact of PCB's. The nannoplankton were again
comprised of diatoms (0.2 to 21.6%) and non-diatoms (78.4 to 99.8%). Melo-
39
-------
TABLE 12- TOTAL PCB CONCENTRATION (ng l"1) IN SPECIFIED PORTIONS OF
SAGiraW BAY, 1977*
Date
19 April
10 May
24 May
28 June
19 July
2 Aug.
12 Sept.
26 Sept,
31 Oct.
Cruise
1
2
3
4
5
6
7
8
9
Mean Segment 3
22
7
21
295**
32
33
9-
6
9
Mean Station 56
-
7
24
316**
5
39
9
7
5
•Courtesy W. Richardson, Large Lakes Lab. U.S.-E.P.A., Grosse lie, MI.
**High winds resuspended sediments.
-------
TABLE 11 COMPOSITION OF NANNOPLANKTON (< 22 Um DIAMETER) DURING 1978
Date
Depth
Relative Biomass, % and
Carbon Content (mgCm"-')
Diatoms
6 May
10 June
9 July
13 Aug.
8 Sept.
0.5
2.5
5.0
0.5
2.5
5.0
0.5
2.5
5.0
0.5
2,5
5.0
0.5
2.5
5.0
43
22
42
1
6
.8(85.1)
.5(73.8)
.4(62.2).
.4(11.3)
.4(21.4)
10.3(23.2)
14
6
2
11
5
11
2
9
12
.6(42.5)
.2(24.1)
.2(15.9)
.2(25.2)
.6(13.0)
.6(39.3)
.6(29.1)
.5(90.3)
.5(130.1)
Non-diatoms
56.
77.
57.
98.
93.
89.
85.
93.
97.
88.
94.
P3.
n.*
90.
87.
2(109.
5(253.
4)
8)
6(84.5)-
6(797.
6(312.
7(201.
4(249.
8(362.
8(721.
8(199.
4(219.
4(298.
4(1105
5(855.
5(910.
7)
8)
9)
2)
8)
4)
7)
4)
9)
.5)
3)
8)
-Relative Biomass (%-)•
of Dominants
Diatoms
Steph.b.
Melosira
Melosira
Melosira
Cyclo.c.
Melosira
Melosira
. n •
if
Melosira
-tt-
n
Melosira
if
»
(14
b.
.3)
(10.5),
,b..(14.4)/
g-
(4.
.*•
9*
II
-n-
g-
it
(i
g.
ii
•tt-
(1.0)
3)
(10.4)
(7.5)
(3.6)
(2.9)
(10.3)
(5.4)
(8.9)
(2.2)
(7.1)
(7.3)
Non-diatoms
Anabaena(23.9)
Cryptomonas (57
Scenedesmas.( 26
Sc9nedesmus(16
Scenedesmus (42
Anabaena(41.0)
Anabaena(9.2)
Anabaena (72, 6)
.5)
.3)
.9)
.5)
-
Scenedesmus-(23-fl)'-
Anabaena(71.4)-
-"• (55.8)
(15.8)
Anabaena(27.2)
(49.1)
(33.8)
.
-------
TABLE 14. COMPOSITION OF NETPLAUKTON (> 22 \m DIAMETER) DURING 1978
Date
Relative Biomass, % and
Carbon Content (mgCm )
Relative Biomass {%)
of Dominants
Diatoms
Non-diatoms
Diatoms
Non-diatoms
6 May
10 June
9 July
13 Aug.
8 Sept.
0.
2.
5.
0.
2.
5.
0.
2.
5.
0.
2.
5.
0.
2.
5.
5
5
0
5
5
0
5
5
0
5
5
0
5
5
0
85.
96.
98.
62.
54.
39.
35.
47.
23.
53.
41.
58.
64.
41.
57.
8(104
8(218
7(217
0(181
.8)
.2)
.9)
.5)
2(156.4)
6(125
1(129
6(195
4(172
6(78.
4(66.
8(74.
2(265
5(213
9(255
.9)
• 4)
.8)
.9)
3)
4)
9)
.0)
.7)
.5)
14.
3.
1.
38.
45.
60.
64.
52.
76.
46.
42.
41.
35.
58.
42.
2(17.
4)
2(7.1)
3(2.9)
0(111
8(132
4(192
9(239
4(215
5(565
4(67.
4(93.
2(52.
8(147
5(301
1(185
.3)
.4)
.4)
.7)
.6)
.7)
9)
8)
4)
.7)
.3)
.4)
Tabellaria f.(25.0) Pediastrum(9.7)
Steph. n.(23.4) " (3.2)
" (20.1)
Steph. n.(30.4)
Aster.(10.3)
Fragill.(12.3)
Steph. n.(32.7)
" (41.1)
* " (12.2)
Steph. n.(36.6)
" " (26.3)
" (41.6)
Steph. n.(32.1)
11 (34.9)
11 (32.7)
Pediastrum(25.1)
S tauras trum ("• 5.7)
(50.2)
Staurastrum(42.2)
(41.3)
(26.9)
Staurastrum.( 27.0)
(35.2)
(22.2)
Pediastrum(17.7)
Staurastrum(16.5)
" (26.9)
42
-------
sira and CycloteTla were the dominant genera of small diatoms, with the lat-
ter more abundant than during 1978 (Table 15), The small non-diatoms
represented by Scenedesmus, which was dominant on all dates and all depths.
Thus-diatoms-and-greens -were-important, -as-during—19-78,—but -bluegreens-were-
less abundant than in 1978 (possibly due to phosphate diversion).
The netplanktic biovolume i.i 1978 was again represented by diatoms (0-
66.0%) and nin-diatoms (34.0-100%). The large diatoms were again dominated
by Stephanodiscus; again Fragillaria and Asterionella were secondary. As in
I
1978, the lar^- non-diatons were Pediastrum and Staurastrcim,- both-green-algae-(TabLe-16).
We emphasize that the dichlorobiphenyl and hexachlorobiphenyl series were
tested during 1978 and 1979 against very similar phytoplankton populations.
Inhibition and Stimulation of Phytoplankton Photosynthesis "by-Hexachlorobi-
phenyl and its Degradation Products
Hexachlorobiphenyl was-.selected as an example of a highly chlorinated
isomer. As such, it was expected to be relatively toxic, since toxicity -is
thought to increase with chV-rination. It was also suspected, of being rela-
tively refractive; slow degradation would suggest its degradation products
would be difficult to find in the water, although they may occur in the livers
of fishes with HFO enzymes. Lastly, penta- and hexachlorobiphenyls and their
furans have been found in humans, specifically in the livers of Yusho pa-
tients, where 2, 3, 4, 7, 8 pentachlorodibenzofuran was observed (Rappe et
al., 1979). Since hexachlorinated isomers are likely relatively refractiver
we also decided to test a possible intermediate hydroxylated product, penta-
chlorobiphcnylol, as well as a furan, octachlorodibenzofuran. These consti-
tuted our best approximately to a degradation series (Figure 4B). The highly,
chlorinated furan was selected because hexachlorodibenzofuran was unavailable.
-------
TABLE 15. COftPOSITION OP >tANNOPLANKTON (< 22 ym DIAMETER) DURING 1979
Relative Biomass, % and
Date Depth Carbon Content (mgCm~^)
Relative Biomass (%)
of Dominants
7 June
14 July
16 Aug.
0.5
2.5
5.0
0.5
2.5
5.0
18 Sept. 0.5
2.5
5.0
Diatoms
2.1(10.2)
3.7(12.3)
4.2(14.8)
Non-diatoms
97.9(472.0)
96.3(318.7)
95.8(328.1)
Diatoms
Non-diatoms
Cyclotella c.(0.4) Scenedesmus(25.3)
" (1.7) " (51.7)
" (2.1) " (43.8)
0.5 0.2(1.2) 99.8(553.4) Synedra n.(0.0) Scenedesmus(24.5)
2.5 21.6(140.2) 78.4(507.6) Cyclotella c.(1.0) " (22.6)
5.0 3.3(25.9) 96.7(726.3) " " (5.4) M (15.6)
1.9(29.8)
3.6(58.4)
2.4(24.5)
98.1(1533.8)
96.4(1577.2)
97.6(978.1)
Cyclotella c.(0.8)
Melosira(2.2)
Cyclotella(0.9)
5.7(120.6) 94.3(2000.9) Melosira(5. 2)
6.5(132.6) 93.5(1912.8) ." (5.6)
9.1(139.9) 90.1(1398.1) " (5.1)
Scenedesmus(16.8)
(14.6)
(51.7)
Scenedesmus(15.3)
(11.5)
(11.4)
44
-------
TABLE16. COMPOSITION OF NETPLANKTON (> 22 pm DIAMETER) DURING 1979
Date
7 June.
14 July
16 Aug.
18 Sept. 0.5
2.5
5.0
Relative Biomass, % and
Carbon Content
Diatoms
Non-diatoms
0.5
2.5
5.0
0.5
2.5
5.0
0.5
2.5
5.0
15.1(22.3)
35.4(37.7)
22.3(72.9)
0.0(0)
2.2(8.4)
3.6(5.2)
4.1(16.2)
15.7(45.1)
11.2(74.7)
84.9(125.9)
64.6(68.9)
77.7(254.4)
100.0(267.2)
97.8(373.1)
96.4(140.2)
95.9(375.2)
84.3(241.5)
88.8(589.7)
66.0(137.7) 34.0(71.0)
57.5(260.6) 42.5(192.9)
56.5(233.4) 43.4(176.7)
Relative Biomass (%)
of Dominants
Diatoms
Non-diatoms
Stephanodiscus(5.2) staurastrum(57.4)
(27.3) " (39.9)
" (S.,7) Pediastrum(29.8)
•»
- Staurastrum(69.4)
Rhizoselenia(0.7) " (19.4)
Pragillaria c.(7.2) Pediastrum(46.1)
Asterionella(2.3) Pediastrum(46.2)
" (7.0) Staurastzum(39.6)
Stephanodiscus(6.3) Pediastrvan(29.1)
(42.2) " (27.8)
" (34.8) Staurastrum(18J7)
(41.8) " (24.4)
45
-------
2-2' dichlorobiphenyl
ci 4-4' dichloro-3,3' biphenyldicl
2,8-dichlorodibenzoferur
a Z.Z'.M'.S.S1- hexacblorobipheny I
a ZlsKS.S1 pentachloro-2-biphenylol
a octachlorodibenzofuran
Figure 4A. Simulated route of transfer of dichlorobiphenyl
to dichlorodibenzofuran (di- series).
Figure 4B. Simulated route of transfer of hexachlorobiphenyl
to its furan (hexa- series).
46
-------
Detailed Monthly Results—
The mean monthly inhibition (stimulation by 100 ng I"1 PCB) of carbon
fixation by nannoplankton and netplankton, relative to the controls, is shown
-iiv-Table.17. Eirst we will discuss the results from surface samples from two
months. Then we will summarize effects of PCB's with depth. The objective
of examining results of surface incubation and resulting carbon fixation was
to note the effect of increasing exposure to PCB's. Examining results with
depth enabled us to observe the effect of light intensity on inhibition/stimu-
*
lation df photosynthesis in the presence of PCB's.
The results of the experiment of 10 June 1978 represent an example where
phytoplankton photosynthesis was relatively equivalent at the three depths
(Table17).; also, there was no evidence of increased surface inhibition due to
the effect of increased exposure-to-PCB-Ls-4Eigure_5__)-. Nannoplankton^Jo) were
inhibited by 5 ng 1 to the same extent as by 500 nc 1 . The-hydroxylated..
PCB (OH-PCB) and the furan (CDBF-PCB; caused slightly more inhibition. Net-
plankton (•) likewise were not effected much by an increase in exposure from
5 ng 1 to 500 ng 1 . The OH-PCB was slightly more inhibitory and the
CDBF-PCB slightly less inhibitory, as compared to the parent isomer (Figure
5). We suspect that this example was representative of inhibition in a well
nixed water column; the wind velocity at noon was 12-24 mph~from the'SW."
Returning to Table , we see that the nanr.oplankton population was inhibited
at 5 m. The particular phytoplankton asemblage involved was--dominated (bio-
volume) by a small diatom, Melosira (17.6%) and a large green, Pediastrum
(41%).
The experiment of 9 July 1978 portrays strong surface inhibition with
increasing exposure to hexachloro ((5-500 ng _1 ); as _illustrated in Figure 6 .
47
-------
TABLE 17. RELATIVE EFFECTS OF 100 ng 1~L HEXACHLOROBIPHENYL SERIES UPON
NANNOPLANlCrON AND NETPLANKTON PHOTOSYNTHESIS (% INHIBITION/STIMULATION)
Date and Depth
Nannoplankton
Treatment
6
May 1978
0.5 m
2.5 m
5.0 m
Parent
Isomer
-37.7
-31.9
+5.3
OH-PCB
-31.9
+13.2
-5.4
CDBF
*
-21.5
0
-8.9
Netp lank ton
Treatment
Parent
Isomer
-42.8
-18.4
+56.9
OH-PCB
-21.4
-10.7
+46.6
CDBF
-22.1
+5.3
+18.1
10 June 1978
9
1-3
8
0.5
2.5
5.0
July 1978
0.5
2.5
5.0
-August -197 8-
0.5
-2,5
5.0
September 1978
0.5
2.5
5.0
-22.3
-
-17.4
-46.6
-25.3
••156.0
+1.9
+12.0
+4.6
+4/F
+3.9
-44.1
-37.4
-
-23.8
-74.1
-49.4
+162.0
-16.0
-10.7
-9.2
-7.0
+3.9
-27.0
-31.3
-
-38.3
-
+0..3
+106.0
+12.7
-3.6
+53.1
+1.0
+18.1
-22.3
-22.0
-8.1
-5.6
-5-. 8
-13.4
+34^9
-18.3
-4.3
+7.O
-18.1
+25.3
+9.6
-25.7
+8.5
+46.3
-93.6
-2.1
- +30.2
-10.0
-1970-
-4.9
-20.7
+25.6
-10.0
-17.. 6
-7.0
+48.1
--
-8.0
+53.3
-41.1
-107 6 -
-7.8
-22.7
+7.0
-11.4
48
-------
500
glOO
a.
o»
ut
X
UJ
10
iPCBIjomar
OH-PC8 OH-PC8 I fCDBF-PCB
9
ftJ
COSF-PCB-*
I
I
I
I
I
20 40 60 80 100
Relative productivity (%control)
Figure 5. Relative nannoplankton (o) and netplankton (o)
productivity on 10 June 1978 at 0.5 m depth upou
exposure to 5, 100 and 500 ng I"1 hexachlorobiphenyl
and 100 ng I"1 pentachlorobiphenylol (OH-PCB)
and octachlorodibenzofuran (CDBF).
-------
500
^.100
CD
o»
3
tn
a
X
UJ
10
iPCBIsomer
_c
OH-PCB fOH-PCB
V0
I
I
I
I
I
20 40 60 80 100
Relative productivity (%control)
nH,' *el*tive nannoplankton (o) and netplatikton (o)
productivity on 9 July 1978 when exposed to hexa-
series at 0.5 m depth.
50
-------
Relative productivity dropped with increased exposure for both nannoplankton
(o) and netplankton (•). The nannoplankton was dominated by Scenedesmus
(21.7%), where as the netplankton biomass was chiefly Stephanodiscus niagarae
(32.7%). The-CDBF-PCE-was-less or about- equally- inhibitive to photosynthesis
as the parent isomer. The hydroxylated product was extremely inhibitive; the:
nannoplankton were inhibited 74.1% (or productivity was 25.9% of control).
Whereas the large diatom Stephanodiscus and the rest of the netplankton was
inhibited 93.6%. Again the diatoms are often inhibited the most. Again we
suspected previous that this example was representative of inhibition during
a calm speel of weather; the wind velocity during the experiment-varied from
calm to 7 mph from the SW.
Estimate of Seasonal-Inhibition of Nannoplankton"by Hexachlorobiphenyl in
Saginaw Bay—
Total-PCB concentrations in Saginaw Bay vary between 5 and 316 ng 1 .
It is very difficult to estimate how much is soluble or "available" PCB; how-
ever, Eisenreic'i (1980) has emonstrated for L. Superior that more-is soluble
than particulate. At Station 56 we measured nannoplankton productivity
(mgCm~ iir~ ) for the water column (Figure 7). From experimentally measured
inhibition due to PCB's at concentrations of 5, 100 and 500 ng 1~ , we-should.
be able to make interpolative estimates for inhibition-over—the—r.atural-range-
of 5-316 ng I"1. Clearly such inhibition is usually beloe 10%; however, fol-
lowing storms which resuspend the PCB rich sediments, waterborne PCB's may_
reach 316 ng 1 and inhibit productivity more than 30% (Figure 7). Thus .
significant PCB effects upon algae may be linked to turbulence.
Estimates of Threshold Effects from Low Concentrations of PCB's—
Intensive studies utilizing exposure of natural populations of nanno-
planktor, and netplankton to 5 ng 1~^ hexachlorobiphenyl enable us to examine
51
-------
N>
o
! <3
i
roductivity
fo
o.
"o
8
i.l
c
?i
- 300
7
1
-^200
o>
c
CD
01
_o
<
^
/
//
— Jf
/I 1
1 J
/A-'^^
MAY 1978 |
f\
1 \ ^ SAGINAW BAY
1 \ !\ Sfa56
' -;\\^
/l- \\ ^"""^
/ \ \ ' •<
\\
> o »
N»
NVx^" —A
JUNE 1 JULY I AUG 1 SEPT
T
30 i
20 1
*•
]>
«»
u
TJ
10 I
D
E
I . t - .,
Figure 7. Estimated reiatiye inhibition of productivity
(o) relative to actual productivity (o) and
PCB levels (ng I'1).
-------
thresholds for inhibition. On three occasions (6 May, 10 June and 9 July)
(Table 18 , nannoplanktic populations algal dominated by Melosira and Scenedes-
-mas, showed inhibitions greater than 20%. Thus we feel we have established a
new lower threshold for the effects of PCB's on carbon fixation of 5 ng 1
(utilizing a 4 hr incubation),
Dark uptake of carbon is stimulated by PCB's. Now we can suggest a
threshold for dark stimulation of 5 ng 1 . On four of five occasions popu-
lations dominated by Scenedesmus, Scenedesnus, Anabaena and flnabaena were
*
stimulated 21 to 80% with the addition of 5 ng 1 hexachlorobiphenyl.
These threshold levels of 5 ng 1~ are in order of magnitude lower than
previously reported. Harding (1975), Powers et al. (1977), Biggs ejt al.
(1978), and Harding and Phillips (1978) all .found thresholds of 3D. _ug I"1 -for
suppression of photosynthesis. Moore and Harriss (197 ) found a threshold
of 7 yg 1 for inhibition by 2,4'dichlorobiphenyl.
Inhibition and Stimulation of Phytopj.ankton Photosynthesis—by-Diciilorobiphenyl
and its Degradation Productr . _ .'•'-.-
Dichlorobiphenyl was selected as an example of a relatively unchlorinated
isomer. It was expected to be relatively less toxic than hexachlorobiphenyl
and more rapidly degraded. Degradation models have suggested formation of
the hydroxylated intermediate in lakes within 2 years (Bunce et al_., 1978) .
It hs not been found in humans to the degree that the penta- and hexachloro-
biphenyls have.
Detailed Monthly Result—
Dichlorobiphenyl was not particularly inhibitory to the phytoplankton on
16 August 1979. In surface waters the narnoplankton (o) and netplankton (o)
showed little response to increased exposure. The nannoplankton inhibited
were 12.7% at 5 ng 1~ and stimulated 4.4% at 500 ng l-i. The nannoplankton,
53
-------
TABLE 18. THRESHOLD EFFECTS OF 5-ng 1 HEXAGHLORQBIPHENYI. SERIES-UPON-
NANNOPLANKTCN AND NETPLANKTON PHOTOSYNTHESIS (% INHIBITION/STIMULATION
Date and Depth
6 Kay 1978
' 0.5
2.5
5.0
10 June 1978
0.5
2.5
5.0
9 July 1978
0.5
2.5
5.0-
13 August JL978
0.5
2.5
. 5.0
8 Sept. 1978
0.5
2.5
5.0
Nannoplankton
Treatment = Parent Isomer -
-20.7
+28.3
-1-6.5
-22.3
-
-8.5
-20.1
-5.7
-H05.0
-2.0
+10.4
-10.9
-13.5
+18.7
-33.5
Netplankton
Treatment = Parent Isomer
-
-12.3-
+68.1
-8.7
-6.3
+80.2
-1.4
'-11.7-
—+21. 7
-17.-4
-14.7
+29.7
-3.3
H-7. 3
-11. 0_
-------
500
I
en
UJ
10
OH-PGE 1 OH-PG8
OED •
COBF-PCBlCDeF-PCB
0 20 40 60 80 100
Relative productivity ( % Control)
Figure 8. Relative nannoplankton (o) and netplankton (o)
productivity at 0.5 m depth on 16 August 1979 whei
. . exposed-to dichlorobipheriyl series.
55
-------
0
NETPLANKTON (1978)
ICOngl"1 hexachlorobiphefnyl
+10
lOOngf1 pentachlorobphenylo!
lOOngl"1 octachlorobibenzofuran
MAY
JUNE
JULY
AUG SEPT
56
-------
dominated by Cyclotella, were inhibited y the CDFB (16.2%) and only slightly
less by the hydroxylated product (7.0%). The netplankton (»} , dominated by
Scenedesmus, likewise showed lictle inhibition ac any exposure (Figure 8).
The furan inhibited photosynthesis 7.4%. Generally we may conclude that
2,2' PCB had little effect on carbon fixation at or above ambient concentra-
tions (39 ng 1 ). .
Seasonal Summary - 2,2' PCB Series—
The effects of 2,2' PCB's on the ahytoplankton are. basically. to., inhibit-
photosynthesis at the satface and stimulate carbon uptake at depth. The
I
nannoplankton were inhibited at all depths by the parent isomer during June
1979 (Figure 8 ). By August, photosynthesis was stimulated at all depths,
with carbon uptake at 5 m about two times the control. Tlamember that phyto-
plankton-populations-were-dominated in the spring by the sirall green algae,
Scenedesmus, which carried into August. The hydroxylated product also inhi-
bited photosynthesis durin, the spri,»g, whereas the CDBF was inhibitory to
nannoplankton at 5 m in spring and fall and stimulatory at depth in July and
August.
From Table 19 we have calculated that the mean stimulation to nannoplank-
ton photosynthesis-of dichlorobiphenyl -dOO-ng-l"1)—ov'er_ the_column_was 31.1%,
while that of the hydroxylated product was 10.0%, while inhibition due to the
CDBF was 1.7%. Thus the effects of dark stimulation of carbon uptake by
nannoplankton resulted in a net column stimulation for the parent isomer and
the hydroxylated product. Only the' furan was slightly inhibitory.
The netplankton, chiefly Sterhanodiscus and Staurastruri, were likewise.-
frequently inhibited in surface light by 100 ng 1 of the three PCE com-
pounds. Of the surface samples, 11 of 12 showed inhibition (Table 19). How-
57
-------
NANNOPLANKTON (1979)
100 ng I"1 dichlorobiphenyl
(A
OJ
8-5
JUNE
*4
+52
+82
+57
+199
i-l
lOOngl"1 dichlorobiphenyldiol
JULY
-2
+58
.-72-
-8
dichlorodibenzofuran
AUG f SEPT |
Figure 10. Inhibition (hatched) and stimulation of
nannoplankton carbon fixation by di- series
(100 ng 1-1) during 1979.
58
-------
TABLE 19. RELATIVE EFFECTS OF 100 ng l"1 DICHLOROBIPHENYL UPON NANNOPLANKTON
AND NETPLANKTON PHOTOSYNTHESIS (% INHIBITION/STIMULATION.),
Date and Depth
7 June 1979
0,5 m
2.5 m
5.0 m
14 July 1979
0.5
2.5
5.0
16 Aug. 1979
0,5
2,5
5.0
Sept. 1979
0,5
2.5
5.0
Narnoplankton
Treatment
Parent
Isoaer OH-PCB CDBF
Netplankton
Treatment
-6.15
-15.64
-7.56
-13.31
+20.32
+6.73
-5.7
- +4.7
+52.7
+81.5
+5T.3
+199.2
-0.95 +9.58
-27.27 -22.25
+4.84 -22.57
-22.04 -61.5
+11.82 +26.78
-1.90 +2.08
-16.2
—+47 r2~
-1.7 +11.8
+58.4 +61.2
+71.7 -13.9
-8.3 -43.3
Parent
Isomer
OH-PCB CDBF
-9.11 -18.13 -19.30
-12.53 . -16.40 +1.7
+6.23-' -28.36- - +3.11
-1.92 -21.04 +91Z5-
-1,79 -5.98 +1.7
+65.3 +22^81 +11.08
-T,20 -15.87.4
+5.4T +15.0 +27.9
-15.6 +11.5 +0.3
-78.8 -50.8 -48.7
-2,5 +28.4 +104.9
+54,7 +64.9 +110.2
59
-------
ever, the mean_stimulation of netplankton in the water column was 0.1% for
the parent isotner, an inhibition of 1.1% for the hydroxylated product, and
stimulation of 16.1% for the CDBF. Again the effect of dark stimulation by
PCB of carbon uptake was apparent. These striking results stress'the impor-
tance of working at typical ambient levels of PCB's for Saginaw Bay (Table 19).
Thus PCB's must be considered as both stimulatory and inhibitory to al-
gal photosynthesis. Those factors effecting dark stimulation and light inhi-
bition must be clearly understood.
Factors Interacting to Reduce Carbon Fixation
/
Relative Chlorination of PCB's Versus Light Intensity—
The literature suggests that toxicity of PCB's increases with chlorina-
tion. In turn, the light intensity at the- surface in Saginaw Bay is often
100 X that at 5 m depth-. We see that the three iiomers of the hexa- series
inhibited both netplankton and nannoplankton in surface waters (Figure 9).
In contrast only two isomers, the present 2,2' and the hydroxylated product,
inhibited the netplankton; In contrast',—the~nannop lank ton were -stimulated—by-
all three isomers of the 2,2' series (Fig. 10) over the entire water colume the 2,2'
series was predominantly stimulatory to carbon fixation, while the hexa-
series was inhibitory (Figure 11), illustrating the effects of chlarination '
Threshold for Dark Stimulation of Carbon Fixation in Presence PCB—
Since absence of light is such an important factor in understanding the
effects of PCB's upon photosynthesis, and since individual species act dif-
ferently, we have plotted the inhibition/stimulation of hexachlorobiphenyl
and its hydroxylated product against light intensity. For both compounds,
stimulation of carbon fixation in populations dominated by the diatom Helo-
sira occurs between 2 and 10% of maximum daily light intensity (Figure 12) •
Such intensities are found at depths" of 2.5-5 m during the sunmertime in
60
-------
8
B
£
•40
-30
-20
-10
0
+10
« -10
o>
sr
o
o
-HO
1+20
QJ
+30
Number'Chlorine Atoms
Figure 11. Stimulation/inhibition of carbon fixation by PCB's
and metabolites relative to degree of chlorination.
61
-------
O.I
I 10
% Maximum intensity
100
Figure 12. Stimulation/inhibition of carbon fixation by 100 ng
1 i hexachlorobipnenyl (o) and its hydroxylated product (o)
relative to light intensity.
62
-------
Saginaw Bay. On the other hand, inhibition of carbon fixation above 15% oc-
curs above 15% of maximum light available to the organisms.
Partition Coefficients and Inhibition—
The lipid-water partition coefficients (log P) for the di- and hexa-
series of isomers should predict their effect upon photosynthesis. However,
partition coefficients for PCB's are hard to obtain from the literature.
Veith (1979) found coefficients ranging from 6 to 7. Pavlou and Dexter (1979)
measured the water-lipid coefficient for zooplankton for hexachlorobiphenyl
(Table 20). Leo £t al^. (1971)_ provided .a model^for-^the detennination-of-the
effects of hydroxyls and furan groups on partition coefficient:*. We have
calculated partition coefficients for each of the six compounds (Table 20 ).
Generally chemicals with ? log P of 4 and greater cannot be treasured with
precision (Verth, 1979).
The partition coefficients of the parent isomers (di- and hexa-) and-
CDBF overlap; these isorner. '.re generally less inhibitory than tneir corres-
ponding h,'droxylated product^. For the parent isomers inhibition of carbon
fixation (acute toxicity) increased with log P. The same was true for the
CDBF; the octa-DBF had a larger log V and was more inhibitory.
The hydroxylated products were characterized by low estimated -log P
values (Table ), but within the OH effects toxicii:y_increased-as-log-P.
Note that the toxicity of the hydroxylated products to netplankton (o) and
nannoplankton (o) were the highest of the three products for any value of
log P (Figure 13).
63
-------
TABLE 20. PARTITION COEFFICIENTS FOR DI- AND HEXACHLOROBIPHENYL ISOMERS AND THEIR
SUSPECTED DEGRADATION PRODUCTS, DOTH MEASURED AND CALCULATED
Isomer and Degradation
Partition
Coefficient
(P),
lipid-water
Correction for
hydroxyl and
furan groups
log P
Dichlorobiphenyl Series
2,2' dichlorobiphenyl
4,4' dichloro- 3,3' biphenyldiol
2,8 dichlorodibenzofuran
Hexachloroblphenyl Series
2, 2', 4, 4', 5, 5' hexachlorobiphenyl
2', 3', 4', 5, 5' pentachloro -2 biphenyl
octachlorodibenaofuran
0.4 x 104
-2(1. 1^)**
-.98**
2.41 x 106*
ol -1.16**
-.98**
3. CO
1.28
2.62
6.38
5,22
5.40
* from Pavlov and Dexter, 1980.
•
** from Leo, Hanch and Elkins, 1971.
-------
Figure 13. Stimulation/inhibition of carbon fixation by di-
and hexachlorobiphenyi and tnetabolites relative to
their lipid-water partition coefficients.
-------
5.3 CHRONIC EFFECTS OF DICHLOROBIPHENYL UPON THE SURVIVAL OF THE CRUSTACEAN
DIAPTOMUS
Purpose
The chronic effects of dichlorobiphenyl were examined by exposing the
zooplankter Diaptomus to three concentrations of PCB's, with control organ-
isms held in lake water. The presence of food was also regulated.
Results «•
Results of May 1978: Effects of PCB concentration upon survival of Diaptomus.
The experimental apparatus, including flasks with animals, pumps and
PCB s£ock solutions were placed in a constant temperature room at 11.1'C.
The Diaptomus all died after 14 days (Table 21). The animals in flasks
receiving 100 ng 1 showed reduced movement, and often it was difficult to
-tell whether they were living, even under a dissecting microscope^ If neces^-
sary, they were touched with a probe to elicit movement. Similar observations
'have been made on zooplankton subjected to thermal shock. This demonstration
of induced torpor shows -the locomotory-effects of minimal, environmentally"
realistic concentrations of PCB upon Diaptomus^
Concentrations ranging froa 100 ng 1 to 10 yg 1~ cannot be shown to
have major effects upon Diaptonus, certainly not proportionally to exposure
(Table ). The-number~of aniraals- rurviving~in 100 mj 1 PCB~after 14~cays
(8.2 +_ 1.3) and in 1 jag 1~ PCB (6.8 +_ 2.0) was not significantly less than
that surviving in the control (6.8 ^ 1.3). However, significantly fewer ani-
mals (2.4 +^ 1.8) survived in 10 lag 1 PCB. Thus the effect of concentration
was only observed at s relatively high level of exposure (10 pg 1~ ) net
found in the natural environments of Lake Huron, and not even in the rela-
tively contaminated waters of Saginaw Bay.
fifi
-------
TABLE 21. NUMBER OF SURVIVING, STARVED DIAPTOMUS IN FLASKS EXPOSED TO THREE
-CONCENTRATIONS (100 ng I"1, 1-yg-l"1, 10-yg 1~-L)-OF 2.2' DICHLORO8IFHENYL,
BEGINNING MAY 18, 1978
Day
0
1
4
5
6
7
8
12
13
14
Control
10.0
9.2 + .83
8.6 + .56
8.3 + .18
7.8 -I- .63
7.6 + .54
7.4 + .54
5.2 + 1.7
7.0 + 0
6.8 + 1.3
100 r.g I"1
10.0
10. C
9.6 + 1.5
9.0 + 1.1
9.2 + 1.2
8.4 + 2.0
8.4 + 2.0
8.6 + 1.2
8.0 + 1.4
8.2 + 1.3
1 VJg I'1
10.0
9.0 + 1.4
8.8 + 1.0
8.8 + 1.1 i
8.2 + 1.2
8.6 4- 1.3
6.3-+ 1.9
7.6 + 2.5
6.8 + 2.0
10 ug I"1
10., 0
9.0 +1.4
6.1 + 1.6
5.1 + 1.9
5.6 i 2.2
5.8 + 1.9
2^6 -+- 1.2
2-8 + 1.3
2.4 - i.8
67
-------
Results of 12 March 1973: Effects of PCB concentration upon survival.
The initial experiment examining the effects of exposure level upon the
survival of Diapto:nus was repeated with similar results to the previous ex-
-1 -1
periment (Tabla 22). Animals exposed to 3.43 vg 1 PCB and 20 yg 1 PCB-
survived longer than animals grown in lake water (controls). At 21 days sur-
vival was Significantly longer in 3.43 and 20 pg 1 PCB than in lakewater
alone. Clearly we were unable to demonstrate long-term chronic mortality of
Diaptcmus through exposure in flow-through chambers to ambient levels of PCB's
characteristic or exceeding those of the Great Lakes.
Results of 10 April 1979: Effects on survival of PCB's combined with food.
One hypothesis suggested that equilibrium partitioning of PCB's at low
concentrations might not result in zooplankton mortality. However, if nanno-
-plankton foods ClOOO^celis^.l" Chlamydomonas) were added to the ttock bottles
previous to the addition of dichlorobiphenyl, we might expect to involve
another step in the physical-biological concentration of PCB's, leading to
greater bioconcentration higher in the food chain, and a significant mortal-
ity of'a herbivore like Diaptomus.
The addition uf food to adsor, • PCB's did not increase the mortality of
Diaptomus at high PC3 concentrations. The numbers of Diaptomus liv±ng~ after-
30 days at 3.43 ^g 1 and 20 ug 1~ ", as well as in the controls-(Table-23),
were not significantly different. Clearly food was not the critical inter-
acting-factor which we- sought. The addition of smalJ Chlamydomonas-did-not—
significantly increase the mortality of Diaptomus in experimental treatments
involving tea's. In fact, a larger but insigu/icant number of animals-sur-
vived in the presence of dichlorobiphenyl.
-------
TABLE 22- NUMBER OF SURVIVING, STARVED DIAPTOMUS (MALES) IN FLASKS EXPOSED
TO CONCENTRATIONS OF 3.43 Ug I"1 AND 20 ug I"1) OF 2,2' DICHLOROBIPHENYL,..-
BEGINNING 12 MARCH, 1979
Day
0
1
2
3
4
7
8
9
10
11
14
15
16
17
18
21
Control
10
9.8
9.8
9.6
9.2
8.8
8.0
7.6
7.2
6.0
4.4
-4.0
3.4
3.0
3.0
2.4
3.43 vg I"1
10
9.8
9.8
9.5
9.5
8.5
8.5
8,0
8.0
7.5 -
7.0
-6.5-
5.8
5,3
5.0
4.3
20 yg I'1
10
9.2
9.0
8.8
8.6
8.0
7.8
7.6
7.2
6.4
6.4
6.4
6.4
6.0
6.0
5^.2
69
-------
CONCENTRATIONS (3.43 yg I"1 and 2O yg I"1) OF 2,2' DICHLOROBIPHENYL,
'SEGINNING-IO APRIL, 1979. ANIMALS- FED -1000 CELLS I"1 CHLAMYDOMONAS -
Day
0
1
2
3
6
7
8
9
10
13
14
15
16
* «7
LI
20
21
22
23
24-
27
23
29
30
Control
10.0
9.8 + .44
9.6 + .54
9.6 + .54
9.4 + .89
9.0 + .70
9.0 + .70
9.0 + .70
8.8 + 1.0
8.6 + .89
8.6 + .89
8.2 + L.3
7.7 +_ 1.0
7 A J_ 1 1
.4 T 1.1
7.2 + 1.0
7.0 +1.0
7.0 + 1.0
6.8 + 1.3
6.4 +1.8
6.0 + 1.4
5.7 + 1.2
5.2 + 1.3
5.2 + 1.3
3.43 yg I"1
9.0
7.2 + 4.2
8.6 + 2.0
8.4 + 2.5
8.0 + 2.3
8.0 + 2.3
7.8 + 2.2
7.8 + 2.2
7.6 + 2.2
7.2 + 1.9
7.2 + 1.9
7.0 + 1.8
«.8 +; 1.6
6s- . ' i r*
.&-•+ 1.5'
6.6 + 1.5
6.6 + 1.5
6.6 + 1.5
6.6 + 1.5
6.2 + 1.2
5.8 + 1.3
5.8 + 1.3
5.5 +_ 1.1
.5.3 + 0.9
20 yg I"1
10.6
10.4 + 1.5
10.2 + 1.6
9.8 + 1.3
9.2 + 1.9
8.8 + 2.3
8.8 + 2.3
8.8 + 2.3
8.8 +2.3
8.6 + 2.0
8.2 + 2.2
a. 2 + 2.2
8.0 +_ 2.3
O f\ 1 ** t
O.O -r~£..3
7.8 +" 2.0
7.8 + 2.0
7.2 + 2.5
7.2 + 2.5
6.6 + 2.1
5.7 + 1.9
5.7 + 1.9
5.7 + 1.9
5.7 + 1.9
70
-------
Results of 24 March 1980: Effects of flow in interpreting PCB induced mor-
tality.
Container modifications were designed (see Methods, 4.3) to keep larger
amounts of PCB in solution. In addition, the extremely low flow of 1 ml hr
was eliminated as a variable which might effect the planktonic Diaptomus.
Survival at 3.43 \ig 1 and 20 yg 1~ dichlorobiphenyl exceed that in
the control (Table 24). When static tests were run in zero flow, survivor-
ship at 20 yg l"1 PCB also exceeded that in the control (0 yg l"1 PCB with
flow or water replacement every 70 hr). Very little difference existed be-
tween the experimental (PCB treatment) and control data (Figure 14).
We must conclude that Diaptomus (males) donot show obvious mortality—
when grown in low concentrations (34-20 yg 1~ ) of dichlorobiphenyl under
continuous flow. Static test (no flow) results indicate either that flow
tends to increase mortality or that static conditions result in less-PCB in
solution, probably the latter. Clearly a lack of evidence does not implicate
2,2'PCB with chronic effects of zooplankton. Likely-the zooplankton-are-more-
important, on an ecosystea basis, in the bioconcentration of PCB'i, increasing
the body burden In the important food fishes of Lake Huron, thcja they are as
direct recipients of PCB induced maladys.
71
-------
TABLE 24 . NUMBER OF SURVIVING, STAR\
TO CONCENTRATIONS (3.43 Vg I"1 AND
BEGINNING 2*
Day
0
1
2
3
4
7
8
9
10
11
14
Control
10.2
10.0
9.8
9.5
8.6
8.4
7.8
7.6
7.2
6.6
0.0
3.43 U
-------
,Q
10
19
o p
8 8
•.£ 7
OJ
J 6
o
*5
I 4
O ?
2 ^
S i
O)
2 0
IV-
I I I I
\ *X 3.4ng/l 2.2' PCB
\
XA 20ng/l 2.2' PCB(dlred)
20ng/l 2.2' PCB (flow)
l.l I I ' I ' *g Control
i^ — CM
in ID f«-
Date (1980)
-------
5.4 INHIBITION OP GRAZING AS AN ALGAL CONTROL
Purpose
Grazing controls the productivity of nannoplankton in oligotrophic Lake
Huron (McNaught et al., 1980). The eutrophic waters of Lake Huron are char-
acterized-by-phytoplankton assemblages -dominated-by-green-and-bluegrpftn al -
gae, with the diatoms of importance during the.spring. This characteristic
applies to Saginaw Bay (Stoermer, unpub. data), as well as the Western Basin
of Lake Erie (Munawar and Munawar, 1976). We thus proposed to study grazing
in these eutrophic waters, first to see if it was inhibited, and secondly, to
see what might be responsible for inhibition if it occurred.
Concepts of Zooplankton Ingestion
Curvilinear functions have been used to.describe the relationship be-
tween ingestion-rate of planktonic herbivores-and their algal-foods—Typi-
cally ingestion increases linearity or curvilinearity until a critical food
concentration_has been reached (Rigler, 1961). This food concentration
value, v;hich describes the onset of saturation feeding, has been of particu-
lar interest. Call the food concentration at saturation, it varies with en-
vironment; in freshwater it has been characterized at about 10 cells ml
(McMahon and Rigler, 1963), but may occur as low as 4 x 10 cells ml in
the sea (Frost, 1975).
Typically in open water environments of Lake Huron, feeding does not
saturate, and ingestion increases linearily with food concentration (McNaught
et al., 1980). Thus it was of interest to see if zooplankton ingestion sat-
urated in Saginaw Bay.
Zooplankton Uptake Curves (Ingestion vs. Concentration) for Saginaw Bay
Zooplankton ingestion was determined for the eleven species and life
-------
stages of zooplankton which dominante in Saginaw Bay (Table 25). Diaptomus
(adults) and Eurytemora (adults) ingested large amounts of nannoplankton on
occasion, but these organisms are not abundant. The high ingestion rates for
copepod nauplii, Cyclops vernalis, and Daphnia retrocurva are significant,
since these organisms are often dominant. These ingestion rates have then
been compared to estimates of nannoplankton biomass made from phytoplankton
collections on Saginaw Bay (Stoermer, pers. conun.), These biomass estimates
are listed in Table 26.
Four species or forms of zooplankton "which .were important-in terms of
biomass; or less abundant but present over much of the summer, were selected
for comparison with their feeding behavior in the open lake (Figures ISA- D).
Copepod nauplii (A) and the cladocerans Eubosmina coregoni (O) and Chydorus
sphaerlcrus (O) were common in the Bay; "Piaptomus adults (A) were less common,
but-important as progenitors of the most vital grazers, the nauplii.
These four grazers all showed intense inhibition of feeding in Saginaw
Bay. That is, their uptake curves are characterized by saturation at low
food concentrations; in effect these animals were consuming very little nan-
noplankton, as compared to their feeding behavior in the open lake. When the
uptake curves were drawn at an expanded scale, it was observed that satura-
tion occurred about 175 mgCm .for alLfour-.species.
When compared~to ingestion-concentration curves for these organisms in
the open lake (solid lines, Figure 15 A-D), we find in the cases of Piapterous,
Eubosnina, and Chydorus that their uptake"curves lie along the baseline for
ingestion of nannoplankton. The curve for nauplii shows an increase to 175
zngCm , but is only visible because of the expanded scale of that graph.
Zooplankton ingestion is severely inhibited in Saginaw Bay. How can one mea-
75
-------
TABLE 2S. INGESTION RATE (mgC ind"1 d"1 X 10"6j FOR MAJOR SPECIES WITH
REGARD TO NANNOPLANKTON RESOURCE.CONCENTRATION. SAGINAW BAY, 1976
't-r>
"
Ingestion Rate
Nannoplankton Diaptomus Diaptomus Cyclops
Date mgCm (A) (C) , vernalis Mesocylops Eurytemora Nauplii
2 July 76 72.0
11 July 76 85.0
9 Oct. 76 177.0
4 June 76 250.7
3 Sept. 76 1032.
55.3 41.5 12.1
32.6 12.2 28.6 36.? 44.9 28.6
866. 169.9 203.9 140.1 437.5 212.4
162.4 108.3 210.6
123.8 74.3 123.8 277.2 148.6
Bpsmina Eubosmina Chydorus Daphnia
lohgirostris coregoni Ceriodaphnia sphaericus retrocurva
2 July 75 72.0
11 July 76 85.0 :
9 Oct. 76 177.0 12
1 ! '
I
69.1 --- 43.2
!2.4 26.5 44.9 18.4 36.7
!3.2 101.9 152io 144.4 106.2
4 June 76 250.7 48.1 78.2 ' — - 258.7
1
3 Sept. 76 1032.
,i
49.5 123.8 74.3
• •• 1 . ' '
-------
TABLE 26 . COMPARISON FOOD RESOURCES IN SAGINAW BAY AND OPEN WATERS OF LAKE HURON
Characteristic Date
%BG (vol) 4 June
11 July
3 Sept.
9 Oct.
3
Volume BG (U )
4 June
11 July
3 Sept.
9 Oct.
Phytoplankton Productivity
(mgCm"3 hr'1)
4 June
11 July
3 Sept.
9 Oct.
Size 6 Species Phytoplankton
4 June
11 July
3 Sept.
9 Oct.
1 . .1 i ' ' '
Saginaw Bay
0.3
13.9
34.3
31.6
11156
48549
58752
1488
7.9
53.2
159.9
20,4
Fragilaria cr. (LG)
ChroococCus (SM)
Anacystis (SM)
Anacystis (SM) ; Cyclo-
i • tella(SM)
• • . . ' I '
Open Lake
0.3
8.0
67.3
21.1
'f
42
5059
58752
12477
0.7
10.0
19.1
0.5
Fragilaria cr. (LG)
Fragilaria cr. (LG)
Chroococcus (SM) ; Cycio-
tella c. (SM)
Anacystis (SM) ; Cyclo-
! tella c. (SM) i
'1
BG » bluegreens, LG - large, SM => small
-------
x,_^Dp,_pu!o6uj).
Figure 15. A-D. Ingestion-concentration curves for Eubosmina
(o), Chydorus (o), Diaptomus adults (A) and r.auplii (A) in
'Saginaw Bay (dashed line), as compared to the same
ingestion rates as identical concentrations in the
open waters of Lake Huron (solid line).
78
-------
sure inhibition, and what are the causes?
Modelling inhibition of Inaestion
Inhibition of ingestion was estimated using a double Monod model sug-
gested by O. DiToro of Manhattan College (pers. comm.). Ingestion (I) is
described in terms of the half-saturation constant (Km) for ingestion and the
food concentration (Co) at the onset of ingestion. Inhibition (Ih) is de-
scribed in terms of the food concentrations at the onset of inhibition (C. )
and the half-saturation constant (KnOi as diagrammed in Figure 16, such
that:
z = Jc . Ih(C-Ch)
Km +• C Kinn (C-Oh)
Ingestion o£ Observed Inhibition in Saginaw Bay
Algal-Foods—
The phytoplankton-of~Saginaw~Bay are similar in relative composition to
those of the open lake (Table_26) • The waters of-.the_B.iy-are-dominated-by
diatoms (D) during the spring. These give way to greens during_the summer-
time, although during late summer the greens occur in almost equal biomass as
the bluegreens (about 30% by volume), as shown in Figure 17. Thus relative
composition is not the only key to our story.
Our overwhelming feature separating the waters of the Bay from those of
the open lake is the large biomass of bluegreens. For example, during-June
they are 265 times more abundant than in the open lake. Zooplankton in Lake
Huron prefer not to ingest sheathed algae (McNaught et^ al., 1980). This
great abundance of bluegreens and greens in Saginaw Bay is reflected in the
rates of productivity found there as opposed to the open Lake (Table 26).
Levels of Relative Inhibition of Ingestion—
The herbivorous crustaceans of Saginaw Bay are inhibited from ingesting
79
-------
00
o
O)
0
01
a>
KC) =
Kmh(C-Ch)
t
!h
Food concentration (C)
Figure 16, Model for inhibition of ingestion (I);
' symbols in text.
-------
May Juno OHLY | Aug Sept Oct
Figure 17. Relative composition (by volume) of
phytoplankton community of Saginaw Uay,
lincluding diatoms (D), green (G) and
blue-fereen (BG) algae.
-------
TABLE 27 . ESTIMATES OF RELATIVE IfJHIBITION (I ) OF INGESTION BY
CRUSTACEANS IN SAGINAW BAY DURING 1976
JL
Date Species Ih/I lake (%)
4 June Diaptomus (A) • , 88.1
Eubosmina coregoui 96.4
11 July Eubosmina coregoni }• 20.6
Chydorus sphaericus 9776
3 Sept. Diaptomus (A) 99.6
Eubosmina coregoni 99r4^
Chydorus sphaericus 99.5
9 Oct. Chydorus sphaericus 93.2
82
-------
00
10
20 .
% Blue-green algae
40
Figure 18. Percentage inhibition by Eubosmina (o)f Chydorus
(o), and Diaptomus (&') as a function of the percentage
composition of blue-green algae in Saginaw Bay.
-------
food at levels cf 2C.6 to 99.6% compared to the organisms of the open- lake
(Tablo 27). The mean inhibition of ingestion in Saginaw Bay ia 86.8%, that
is, these crustacenas of only consuming 13.2% of the amount expected, based
i -3
on linear uptake to food concentrations of 100 mgCm . This is a striking
finding. - Biological control—of- nuisance-blooms-of algae-is-unlikely-if-only
13% of the optimal grazing activity is possible.
Interpretation of this almost total inhibition of grazing is difficult.
The obvious comparison to be made, according to the grazing literature, would
be between inhibition and the percentage composition of bluegreen algae
(Figure 18). Surprisingly, there is little relationship, chiefly because in-
hibition was only observed at levels below 88% once. Diaptomus-and- Chydorus
were inhibited more than 88% at all levels of bluegreen composition, while
E'ibosmir.a-was inhibitei only 20.6%-at an intermediate bluegreen-relative bio-
mas?.. We must conclude tht grazing is severely~limrted~±n~SagiiTaw-Bay—by
factors other than bluegreen abundance. The high levels of other natural and
man-made compounds in the water must be investigated.
Zooplankton Uptake Curves for Lake Erie
Algal Foods—
Levels of algal carbon for Western Lake Erie were calculated from the
data presented by Munawar and Munawar (1976); Nannoplankton populations are
dominated in April by diatoms (79%), in May by cryptomonads (18%), in early
July by diatoms (23%) and cryptomonads (22%), in late July by Ceratium (20.5%)
and Pediastrum (19.5%), and in September by diatoms (33%) and b? /egreen algae
(20%).
Levels of Relative Inhibition of Ingestion—
The herbivorous crustaceiins of Western Lake Erie are not inhibited from
84
-------
feeding, based on comparison with the liu.?ar ke curves for the _zooplank-
ton of Lake Huron, Their ingestion rates vary from 63-4 x 10 mgC ind
day" for Chydovus at intermediate nannoplankton ca bon (800 mgCm ) to
3010 for Daphnia galeata at a higher food level (1350) Table 28. The
graphs comparing the various uptake-concentration relationships for Lake
Erie are clear evidence that these herbivores equal and even outperform
their counterparts in the open waters of Lake Huron.
t
Eubosmina (Figure 19A) exhibited equivalent or higher inyestion rates
than, the same species in Lake Huron; even though Lake Erie is rich in nanno-
plankton, with almost twice the biomass as the open waters of Lake Huron,
i -3
the rates above food concentrations of 1400 mgCm are only slightly below
the projected curve for Lake Huron. The same is true for Chydorus (Fioure
19B). Ingestion rates at 1424 and 1^85 mgCm"3 as nannoplankton lie only
slightly below the-projected curve for Lake Huron. Since the nannoplankton
biomass does not reach 1800 mgCm in mesotrophic Lake Huron, we cannot
realistically calculate inhibition levels for Lake Erie. If we were to esti-
mate a level of inhibition for Chydorus in Lake Erie relative to the open
waters of Lake Huron, we would find that Chydorus was only inhibited abcut
37%, nothing approaching the levels observed for the same species in S£*ginaw
Bay.
Similar conclusions are evident for Diapton-js (adults) and nauplii. The
nauplii are the Tiost important nannoplankton grazers in the Great Lakes. Yet
in Western Lake Erie their ingestion rates exceed the levels found in the
open waters of Lake Huron. We must, conclude that they control nannoplankton
growth rather effectively in Lake Erie. The same was true for Diaptom^s.
Ingestion levels at- a food concentration of 1000 mgCm &_e about the same
85
-------
TABLE 28 . INGESTION RATE (mgC ind~
PLANKTON RESOURCES LAKE ERIE
d X 10 FOR TAJOR SPECIES WITH-REGARD TO NANNO-
, STATION , 1977 (A ° ADULT , C = COPEPODITE) I
'
Nannoplankton Diaptomus Dia^tomus Ingestion Ratr
Date mgCm (A) (C) Cyclops vern. Eurytemora Nauplius
00
6-
1
19 April 1977 800 52.0 54.7 230.4
23 May 1977 f424 411.8 - 150.3
7 July 1977 1000 348.0 - 144.0
26 July 1977 1350 1263.6 680.4 216.0
i
15 Sept. 1977 1785 428.4 244.0 327.0
1
.
I
73.9
539.9 ?5.7
31.0
178.0
110.6
•( Cyclops
Daphnia Bosmina Eubosmina Cyclopoid Daphnia bicuspida-
galeata (A) longirostris coregoni i cops. Chydprus retrocurva tus (A)
19 April 1977
2,3 Hay 1977
7 July 1977
26 July 1977
15 Sept. 1977
i
960.0
r
2472.
3010.
I
i
• ' -
210.2 .?2Q.4
264.0 61.0
745.0
178.5
25.9
28.5
44.0
388.8
216.3
i
63.4
261.4
636, C
-
278.4
.
710.9
1888.0
1927.8
47J.O
334.0
1
193.0
300.0
1
.
-------
10
8
2?
I
o
Q
(9OI
uoijsa6u|
CD
O
(90i
uous36u|
Figure 19. A-D. Ingast ion-concentration curves lor auposmina.
(o), Chydorus (o), Diaptomus adults (A) and nauplii (A) in
Western Lake Erie (dashed line) compared to the same
ingcstion rates at identical concentrations in
the open waters of Lake Huron (solid line).
87
-------
as those measured in take Huron. If a calculation of inhibition were made
it would be positive (stimulation).
These findings concerning bioregulation of phytoplankton growth in Lake
Erie are both unexpected and stimulating. Why has the Lake Erie ecosystem
responded in this fashion? Why is grazing phytoplankton effective- in Lake
Erie and not in Saginaw Bay?
Comparative Assimilation Rates on Total Phytoolankton
The growth of any zooplankton population is equivalent to its assimila-
ti^n of food, and not siaiply to the food ingested. In the^ open waters of
Lake Huron food is scarce. The zoopJankton grazed over 100% of nanroplankton
productivity from May through August. Of the scarce nannoplankton ingested,
the major ixerbivores assimilated 93.2% (McNaught et aJU, 1980). However,
both Saginaw Bay and Western Lake Erie appear to be food rich environments,
~where herbivores could" Feed rapidly but tolerate a relatively low efficiency.
In one case, Sagiriaw Bay, populations of zooplankton did not ingest much,
and their assimilation rates may help interpret what was happening.
Assimilation rates are difficult to measure_in-the--field. -We-followed-
classical techniques (Sorokin, 1968) of determining ingestion using a short
feeding period (15 min). Then we feed a duplicate batch for a long period,
following which the zooplankters guts were cleared of tagged food for 4 hr.
Relative assimilation can be defined as:
% assimilation = ingestion rate determined with defication possible
short-terra ingestion rato
Lake Erie zooplankters ingested large amounts of food from an environ-
ment productive of diatoms and cryptomonads, with some greens and bluegreer.s.
- • • * "
Their intake could have been predicted by extending the linear uptake-concen-
-------
tration curve determined for the zooplankton of the open waters of Lake
Huron. However, from this large food suppjy they assimilated only 8.4Z
of the food ingested (Table 29). Assimilation was highest (21.3%) during
lake May when small cryptomonads are typically abundant.
Saginaw-Bay-crustaceans-live-in-an— eutrophic—environment"with a
smaller algal standing crop than Western Lake Erie (Table 26>. While
their intake of nannoplankton was inhibited 872 below that in the open
lake, their assimilation values were higher, with a mean of 14.5% and
a high of 45.7% for June (Table 30). In June the phytoplankton of_the
Bay was dominated by diatoms. We cannot determine-if--thls-higher—level
of food-assimilation helps defray the costs of low ingestion. Certainly
it is part of the answer to balancing the equation for consumption.
Alternate.foods-as- detritus probably account—for-^the-rema-inder of—the
answer to-this-st-imulating-questionr -
89
-------
TABLE 29. ASSIMILATION EFFICIENCY (%) ON TOTAL PHYTOPLANKTON
FOR LAKE ERTE ZOOPLANKTON COMMUNITY DURING 1277
Species
Cladocera
Oaphnia galeata
Daphnia retrocurva
Chydorus sphaericus ;
Bosmina longirostris
Eubosmina coregoni
Leptodora kii.dtii
Copepoda
Nauplii
Calanoid copepodites
Edaptomus (A)
I'imnocalanus macrurus (A)
I'.pischura lacustris
Eurytemora affinis
Cyclopotd copepodites
Cyclops bicuspidatus
Cyclops vernalis
Mesocyclops ed<»jc
19 April
16.7
-
-
-
-
—
0
25.0
4.8
3.5
--
^
0
0
0
0
23 May 7 June
1.2
64.0 0.6
11.1 0
8.3
2.7 5.4
2.1
0 0
-
' -
-
-
27.5
57.1 0
6.8 1.5
14.3 2.4
-
26 July
9.^
3.8
—
t
' 2.8
6.7
3.3
6.8
5.2
-
5,8
34.6
0
-
4-.0
—
15 Sept.
-
14.7
O
-
10.6
0
0
16,2
12.5
-
-
"•
0
-
0-
—
Monthly Mean 5.6 21.3 1.6 7.S 6.0
Grand Mean =8.4
90
-------
TABLE 30 . ASSIMILATION EFFICIENCY »%) ON T>TAL PHYTOPLANKTON
•• FOR SAGINAW BAY ZOOPLANKTON COMMUNITY DURING 1976
-Species 5 June- -11 July 29 July 4-Sept.— IQ-Qct.
Cladocera
Daphnia retrocurva 60.0 6.8 5.8 0 14.9
Chydorus sphaericus 65.0 9.6 0 0 ' -
Eubosmina coregoni 38.8 13.0 0 0 0
Bosttiina longirostris 33.3 9.7 - - 0
Alona spp.
Copepoda
Nauplii 0 0 ' 0 0 0
Calanoid copepodites - - - 0
Eurytemora affinis 100.0 12.8 14.4 17_8 6a.O
Di?ptomus (A) 30.0 16.6 3.6. 0
Cyclopoid cope odites 30.3 - - 0
Cyclops bicuspidatus 62.5 - - - -
Cyclops vernalis "3777" 870~ 4.10
Mesocylops edax - - - 0 1.8
Tropocylops prasinus - 0 0 0 5.0
Monthly Mean . 45.7 8.7 3.5 1.6 12.8
Grand Mean = 14.5
91
-------
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