Download Benthic and Pelagic Secondary Production in Lake Erie

J. Great Lakes Res. 26(1):31–54
Internat. Assoc. Great Lakes Res., 2000
Benthic and Pelagic Secondary Production in Lake Erie after the
Invasion of Dreissena spp. with Implications for Fish Production
Ora E. Johannsson1,*, Ron Dermott1, Donna M. Graham1,
Julie A. Dahl2, E. Scott Millard1, Debra D. Myles3, and Jennifer LeBlanc4
1Great
Lakes Laboratory for Fisheries and Aquatic Sciences
Canada Centre for Inland Waters
867 Lakeshore Rd.
P.O. Box 5050
Burlington, Ontario L7R 4A6
2INAC-Environment
and Conservation
P.O. 2310
Yellow Knife, Northwest Territory X1A 2R3
3Dept.
of Fisheries and Oceans
Box 1500, 4914-50th St P.O. 2310
Yellowknife, Northwest Territory X1A 2P7
44072
Cid Way
Pleasanton, California 94566
ABSTRACT. Benthic and pelagic secondary production were measured at nearshore and offshore sites
in the western, west-central, and eastern basins of Lake Erie in 1993 to determine the relative importance
of benthic and pelagic foodwebs to the fish community after dreissenid colonization. Benthic biomass
increased greatly between 1979 and 1993 because of the presence of dreissenids, and > 90% of benthic
production in 1993 came from dreissenids. Biomass of “other” benthos (excluding unionids and dreissenids) did not decline. Dreissenid production was in addition to, and not at the expense of, “other” benthic production. Zooplankton production was close to or within the 95% confidence interval of that predicted from primary production (photosynthesis) based on the relationship described by Makarewicz and
Likens (1979). Deviations from this relationship were correlated with summer zooplankton mean length,
suggesting that planktivory was an important factor in the regulation of zooplankton production in the
lake. Dreissenids therefore impact zooplankton production by reducing algal biomass and primary production particularly in unstratified regions, by decreasing rotifer abundance and hence biomass and production, and by producing veligers which contribute 10% to 25% to zooplankton production.
Potential fish biomass which could be supported by the benthic and pelagic foodwebs was estimated
from empirical equations. The benthic food chain could potentially support more fish biomass than the
pelagic food chain in all basins in 1993, even if dreissenids were excluded from the calculations.
INDEX WORDS:
Benthos, zooplankton, Dreissena, fish, production, planktivory.
INTRODUCTION
Zebra (Dreissena polymorpha) and quagga mussels (D. bugensis) are re-organizing community
structure and the flow of energy through freshwater
communities in North America (Leach 1993; Hol-
land et al. 1995; Dahl et al. 1995; Dermott and
Kerec 1997; Fahnenstiel et al. 1995a, b; Madenjian
1995; Nalepa and Fahnenstiel 1995; Graham et al.
1996). In so doing, they are changing the relative
availability of pelagic and benthic food sources for
the fish community.
Dreissenids may affect zooplankton both directly
through predation (Shevtsova et al. 1986 in
*Corresponding author. E-mail: [email protected]
31
32
Johannsson et al.
MacIsaac et al. 1995, MacIsaac et al. 1991) and indirectly through competition for food (Ten Winkel
and Davids 1982, Cotner et al. 1995, Lavrentyev et
al. 1995). Common food sources of dreissenids include rotifers, ciliates, small nauplii (also eaten by
omnivorous copepods, particularly cyclopoids),
large algae (also eaten by copepods, particularly
calanoids), and to a lesser extent, small algae and
bacteria (also eaten by cladocerans) (Ten Winkel
and Davids 1982, Sprung and Rose 1988, Cotner et
al. 1995, Lavrentyev et al. 1995, MacIsaac et al.
1995). In addition to physically consuming the
same food as zooplankton, dreissenids may also reduce primary production below the potential set by
the phosphorus concentration (Millard et al. 1999),
and in some instances, they may decrease the
pelagic phosphorus pool, at least temporarily (Mellina et al. 1995, Fahnenstiel et al. 1995b, Millard
unpubl. data). In phosphorus-limited systems, such
as Lake Erie, phosphorus levels set the level of primary production which in turn should set the maximum level of zooplankton production (Makarewicz
and Likens 1979; Lean et al. 1983; McQueen et al.
1986; Millard et al. 1996a,b).
While the impact of dreissenids on the pelagic
community is predominantly negative, their effects
on the benthic community are mixed. The benthic
community benefits from increased water clarity,
the extension of littoral habitat, and increased habitat structure in the presence of dreissenids (Dermott
et al. 1993, Griffiths 1993, Stewart and Haynes
1994, Lowe and Pillsbury 1995, Skubinna et al.
1995). However, mussels are responsible for the
decimation of unionid and larger sphaeriid clams
(Mackie 1993, Gillis and Mackie 1994, Dahl et al.
1995) and are thought to be largely responsible for
the disappearance of the benthic amphipod Diporeia in eastern Lake Erie (Dermott and Munawar
1993, Dermott and Kerec 1997).
Lake Erie is a focal point for research on dreissenids and was chosen for this study because it was
near the epicenter of the invasion, a range of
trophic and substrate conditions exist within the
lake, and most importantly, the potential impact of
dreissenids on the fishery was of economic significance. The fishery in Lake Erie is one of the more
profitable freshwater fisheries in the world (T.
Cowan, DFO, pers. comm.) with a long-term commercial catch of 11 to 20 million kg/yr in Canadian
waters (OMNR 1995) and with a valuable sports
fishery for walleye and salmon in American waters.
In the present study lower trophic level productivity in the presence of dreissenids in nearshore
and offshore environments in Lake Erie was investigated. The production and community structure of
benthos and zooplankton, and the relative importance of the benthic and pelagic food chains in supporting the fish community were examined.
METHODS AND MATERIALS
Description of Study Site
Morphometrically, Lake Erie consists of three
basins with distinct structural and trophic characteristics (Fig. 1) (Burns 1985). The western basin is
shallow (mean depth = 7.4 m; Mortimer 1987),
rarely stratifies, and is separated from the central
basin by the Lorain Ridge southeast from Point
Pelee. The offshore of the central basin is a plain 20
m to 24 m deep (mean basin depth = 18.3 m). The
basin stratifies in summer and extensive areas of
the hypolimnion on the western side of the plain go
anoxic or experience low oxygen conditions by the
end of the summer. The Pennsylvania Ridge, south
of Long Point, divides the central and eastern
basins. The deepest regions of the east basin are off
Long Point (mean basin depth = 25.0 m, maximum
depth = 64 m). Strong gradients in temperature and
productivity exist along the east-west axis of the
lake. In 1993, the mean May to October temperature of the mixed layer was 2°C to 3°C lower in the
eastern and west-central basins than in the western
basin, average total phosphorus ranged from 7
µg/L to 10 µg/L in the eastern basin to 17 µg/L in
the western basin, and chlorophyll a increased from
1.06 µg/L to 2.24 µg/L in the eastern basin to 4.50
µg/L in the western basin (Dahl et al. 1995).
Field Program
Two stations in the western basin, two in the
west-central basin, and three in the eastern basin
were sampled as part of the Lake Erie Biomonitoring Program (LEB) (Fig. 1). Sites were chosen to
include both nearshore and offshore regions, and in
the eastern basin, areas which did and did not stratify during the summer (Table 1). Sampling extended from 3 May 1993 to 25 October 1993 in the
western and west-central basins, and from 10 May
to 18 October 1993 and 10 May to 8 November
1994 in the eastern basin. All parameters were sampled every 2 weeks except benthic samples were
taken monthly from May to October 1993 and once
in May 1994 from all sites, except E1 in the eastern
basin.
Epilimnetic, metalimnetic, and hypolimnetic or
Benthic and Pelagic Production in Lake Erie: Post-Dreissena
33
FIG. 1. Morphometric map of Lake Erie indicating the sampling locations and station names.
whole-water-column zooplankton samples were
collected depending on the thermal stratification of
the water column. The water column was considered stratified when the density gradient caused by
the difference in temperature exceeded 0.08/m3/m
at a depth > 4 m (Reynolds and Wiseman 1982,
Reynolds et al. 1984). Zooplankton were collected
with a 0.5-m diameter, 110-µm mesh Wisconsin
closing net, 3-m in length, which was metered to
allow correction for filtering efficiency. The net
was raised at 0.8 to 1.0 m/s. A 2-m gap was left between samples from different strata to prevent overlap of the samples caused by movement of the boat
Two replicate samples were collected, preserved in
4% phosphate-buffered, sugared formalin, and combined before sample analysis. In 1994 total water
column samples were also collected at E2 to assess
the ability of the stratified sampling method to provide seasonally reliable biomass estimates. The seasonally-weighted (weighted for intersampling
interval) mean biomass of zooplankton in the total
water column during the stratified period was 26.9
µg/L as estimated from the stratified samples and
26.6 µg/L as estimated from the total water column
samples.
To sample rotifers, integrated, whole-water samples were collected over the same depth ranges as
the zooplankton net hauls using a Shurflo diaphragm pump. Ten liters of this water was passed
through a 20-µm sieve and preserved with 4% phosphate-buffered, sugared formalin. In 1994, a 20 L
sample was taken from the epilimnion where ro-
tifers were most abundant, otherwise 50 L were filtered. The rotifers were anaesthetized for 2 minutes
in soda water before being preserved.
Five replicate petit-Ponar samples (0.0232 m 2
each) were taken every month for benthos. Each
sample was sieved through a 0.25-mm screen and
preserved in 10% neutral formalin.
Additional information on the other parameters
measured and results of the Lake Erie Biomonitoring Program are given in Dahl et al. (1995) and
Graham et al. (1996).
Sample Analysis
A minimum of 400 individual zooplankton were
enumerated and measured using a stratified, random, counting procedure (Cooley et al. 1986) ensuring that at least 100 individuals of each major
group were included. If animal density was low,
20% of the sample was counted. De Milo (1993)
found that the genus Bosmina in the Great Lakes
consists of two new species (B. liederi and B. freyi)
and not B. longirostris. The two species are difficult
to separate; consequently, Bosmina were identified
only to genus. Lengths of cladocerans were measured from the top of the helmet to the base of the
tail spine, copepods from the anterior end of the
cephalothorax to the end of the caudal rami, and
veligers across the widest section of the shell. Body
mass was estimated from length-weight regressions
from the literature: the equations for the dominant
groups were verified with field data (Appendix 1a).
9.6
Fine
silt
Station Depth (m)
Substrate Type
Fine
silt
10.4
none
W3
1993
May 6–
Oct. 27
Coarse
sand
16.3
Jul. 15–
Aug. 17
WC1
1993
May 7–
Oct. 26
Temperature of
SWM*
18.9
19.6
16.7
Mixed Depth
Max.
25.5
24.6
23.3
(oC)
Min
10.5
10.1
6.6
*SWM is the seasonally weighted mean over the period sampled.
none
Period of Stratification
Sampling Date Range
W1
1993
May 7–
Oct. 26
16.9
23.5
6.8
Fine
silt
21.6
Jun. 30–
Sept. 17
WC2
1993
May 7–
Oct. 26
17.5
23.7
10.6
Fine
sand
5.9
none
E1
1993
May 14–
Oct. 20
16.6
22.5
8.0
5.9
none
E1
1994
May 10–
Oct. 18
16.8
23.1
7.0
Fine
silt
9.2
none
E3
1993
May 12–
Oct. 20
Station and water quality parameters for the LEB sites sampled in 1993 and 1994.
Parameter/Station
TABLE 1.
16.4
22.1
5.2
9.2
none
E3
1994
May 10–
Oct. 18
17.0
23.3
4.3
Fine
silt
38.0
Jun. 24–
Sept. 24
E2
1993
May 14–
Oct. 5
16.2
23.0
2.9
38.0
Jun. 16–
Oct. 18
E2
1994
May 10–
Oct. 18
34
Johannsson et al.
Benthic and Pelagic Production in Lake Erie: Post-Dreissena
A minimum of 400 rotifers were enumerated in a
Sedgewick-Rafter chamber. Body mass was estimated according to the formulae of Ruttner-Kolisko
(in Bottrel et al. 1976). Polyarthra biomass was estimated from a simplified formula, however, the literature equation was not applicable for Lake Erie
rotifers. A common equation was developed for P.
remata, P. vulgaris, and P. major: v = 0.158a3 (95%
confidence interval: 0.153 to 0.163) where v = volume in µ3 (or wet body mass in µg × 10–6 assuming
a density of one) and a = longest dimension in microns. The equation for P. dolichoptera was v =
0.205a3 (95% confidence interval: 0.195 to 0.215).
Three or four of the preserved benthic samples
were analyzed from each station on each sample
date, while the remaining samples were archived.
All organisms retained on a 580-µm screen (#30
mesh) were enumerated. The finer material retained
on a 250-µm screen was subsampled by volume,
and a minimum of 1/4 of this material was sorted
under a microscope at a magnification of 20X. The
counts were converted to number per sample. Invertebrates were identified and their blotted wet
weights were measured. The organisms in each taxonomic group were placed into distilled water for
exactly 60 s before weighing to ensure wet weights
were consistent. Common taxa were identified to
genus or species where possible, but only to family
level for the Nematoda, Oligochaeta, Ostracoda,
and Harpacticoida. The Chironomus species, Procladius species, Gammarus fasciatus, and the zebra
(Dreissena polymorpha) and quagga (D. bugensis)
mussels were divided into size classes and enumerated. Average density and wet biomass (g/m2) of
each taxon were calculated per m2 for each station.
Wet weight of the mollusks was converted to shell
free wet weight using calculated ratios of soft tissue
to total wet weight: D. polymorpha 0.56, D. bugensis 0.58, Sphaeriidae 0.3.
Production Calculations
All zooplankton production was calculated on a
dry-weight basis unless otherwise indicated. All
benthic production was calculated on a shell-free,
wet-weight basis. All comparisons between the production of the benthos and plankton were done on a
wet-weight basis assuming zooplankton dry body
mass was 10% of wet weight. This is consistent
with the associated literature. Sufficient error is associated with the numerous steps in production
(sampling, enumeration, length-weight regressions,
Production/Biomass approximations), that small
35
differences in production should not be considered
significant.
Zooplankton
Seasonal (1 May to 31 October) zooplankton production was calculated for the total water column at
each station. Production estimates calculated using
the egg-ratio method are based on changes in abundance and egg ratios between dates and on mean
temperature. Production estimates calculated from
P/B ratios depend on seasonally-weighted mean
body size, seasonally-weighted mean population
biomass, and median temperature. Therefore, production was calculated for each species within individual thermal layers over the temporal duration of
that layer. For example, in 1993 production in the
metalimnion of station E2 was calculated for the
stratified period: 18 June to 29 September. In the
offshore of the eastern basin, the data from the preand post-stratified periods were combined with the
hypolimnetic data from the stratified period to create a single continuous season because water temperatures were similar (> 4 and < 10°C) and warm
water species were not abundant until after stratification. Similarly, in the west-central basin, the preand post-stratified data were combined with the
epilimnetic data because the systems became unstratified while temperatures were still high (17 and
23°C). For each station, the species productions for
each thermal layer were summed to generate seasonal water column production.
The egg-ratio method of Paloheimo (1974), as
described in Cooley et al. (1986), was used to calculate production of cladocerans, cyclopoids, and
calanoids if the seasonally-weighted, mean biomass
of the species was > 50 mg/m 2 /season and the
species carried its eggs. Development coefficients
are listed in Appendix 1b. When these conditions
were not met, production was estimated using P/B
relationships. P/B estimates for non-predatory
cladocerans were taken from Stockwell and Johannsson (1997): when temperature was > 10°C,
P/B = 0.162/d and when it was < 10°C, P/B =
0.042/d. For the larger, predatory cladocerans,
Bythotrephes cederströemi and Leptodora kindtii,
the size-dependent equations of Stockwell and Johannsson (1997) were used to estimate daily P/B:
mean seasonal temperature > 10°C
log (daily P/B) = –0.23 * log (dry wt (µg)) –0.73
(1)
36
Johannsson et al.
mean seasonal temperature < 10°C
log (daily P/B) = –0.26 * log (dry wt(µg)) –1.36
(2)
The P/B estimates for cyclopoid, calanoid and rotifer production were taken from the seasonal daily
P/B equations of Shuter and Ing (1997):
log(median daily P/B) = A + 0.04336 *
(median temperature (°C))
(3)
where A = –1.844 (cyclopoids)
= –2.294 (calanoids)
= –1.631 (rotifers)
Comparisons between production estimates using
the P/B equations of Stockwell and Johannsson
(1997) and Shuter and Ing (1997) and egg-ratio production estimates from a long-term monitoring site
in Lake Ontario (Johannsson, unpubl. data), indicated that the equations of Stockwell and Johannsson (1997) came closer to predicting egg-ratio
estimates of seasonal zooplankton production for
cladocerans while the seasonal daily P/B equations
of Shuter and Ing (1997) were better for cyclopoid
species. No calanoid species were present in Lake
Ontario in sufficient biomass to calculate production using the egg-ratio method, therefore comparisons were not possible for this group.
Dreissenid veligers grow from approximately 60
to 250 µm in length, or from 0.033 to 1.711 µg dry
weight over a 44 to 70 day period (Leach 1993,
Doka 1994), which equates to a daily P/B of 0.160
to 0.101/d. A daily P/B of 0.1/d was used to be conservative and to allow for slower growth during the
colder portions of the season. This rate was applied
to veligers in the epilimnion. A rate of 0.04/d was
applied when the median temperatures was
< 10°C.
The daily P/B of a species in a specific thermal
layer was multiplied by the seasonally-weighted
mean biomass of that species and by the length of
the season of that thermal layer in days in order to
calculate seasonal production. Egg-ratio and P/B
estimates of production for individual species were
compared, where possible, in order to test the validity of using the above P/B values to calculate the
production of the less abundant species. Where the
average egg-ratio estimates were more than 25%
different from the P/B estimates, the P/B estimates
of all similar species were adjusted by the average
percent difference.
Benthos
Annual production of the common benthic
species: Dreissena spp., Chironomus spp., Procladius spp., and Gammarus fasciatus was calculated
using the size-frequency method of Krueger and
Martin (1980). These calculations used monthly
mean densities in four size classes, average wet
weight (shell-free) per individual in each size class,
and the geometric weight between neighboring size
classes j and j+1. A cohort generation time of 1
year was used at all sites except E2. Data at E2 suggested that in deep water, growth of D. bugensis
was half that at the other stations, so a generation
time of 2 years was used at E2. Where numbers of
the common species were insufficient to calculate
size frequencies, and for all other benthic taxa, production was calculated from the mean annual wet
biomass and published values for the turnover (P/B)
ratios for each taxon (Appendix 2).
RESULTS
Dreissena spp. represented between 90% and
99% of the benthic biomass at all stations except
WC2 in the west-central basin, where the biomass
was dominated by Chironomus spp. (Table 2). As a
result, the biomass and production of the benthic
fauna in Lake Erie were dominated by Dreissena
spp., which contributed over 90% of the benthic
production at 5 of the 6 stations (Table 3). Dreissenid veliger production was not as significant in
the pelagic system as adult dreissenid production
was in the benthic system. In most instances, it was
responsible for 10% to 25% of pelagic production.
No clear spatial pattern was evident except for the
low production at WC2 (Table 4).
Zooplankton
Spatial gradients of zooplankton production
within the lake were dissimilar among the three
subgroups of zooplankton: macrozooplankton, rotifers, and veligers (Table 4). Macrozooplankton
production was higher in the west and west-central
basins than in the eastern basin. Rotifer production
was greatest in the west-central basin and offshore
of the eastern basin, and least in the nearshore of
the eastern basin. Veliger production was lowest in
the nearshore of the eastern basin and in the offshore of the west-central basin. Production may
best be understood if examined on a basin basis.
In the eastern basin, total water column, May to
October zooplankton production (TZP) was much
Benthic and Pelagic Production in Lake Erie: Post-Dreissena
37
TABLE 2. Annual benthic biomass at selected Lake Erie stations, 1993. Biomass is wet, shell-free weight
(g/m2). Averages were calculated from 7 sampling dates, with the exception of Station W3 (n = 5) and E2
(n = 6).
W1
Species
Biomass
Nematoda
0.064
Platyhelminthes/
Nemertea
0.001
Oligochaeta
4.002
Hirudinae
0.094
Amphipoda
0.050
Isopoda
0.000
Ostracoda
0.286
Harpacticoida
0.222
Ephemeroptera
0.009
Trichoptera
0.031
Chironomidae
1.630
Gastropoda
0.014
Sphaeriidae
0.188
Dreissena
polymorpha
64.800
Dreissena
bugensis
0.000
W3
S.E.
Biomass
WC1
S.E.
Biomass
WC2
S.E
Biomass
E2
E3
S.E.
Biomass
S.E.
Biomass
S.E.
0.030
0.081
0.018
0.022
0.010
0.129
0.028
0.155
0.020
0.171
0.030
0.001
0.989
0.033
0.025
0.000
0.046
0.031
0.006
0.031
0.781
0.009
0.046
0.187
4.068
0.752
0.925
0.000
0.076
0.109
0.001
0.038
0.299
0.655
0.148
0.104
0.831
0.153
0.585
0.000
0.018
0.019
0.001
0.021
0.081
0.273
0.057
0.050
1.649
0.010
0.112
0.066
0.105
0.005
0.000
0.000
1.445
0.291
0.008
0.031
0.426
0.007
0.106
0.059
0.053
0.002
0.000
0.000
0.827
0.125
0.005
0.075
6.647
0.022
0.002
0.000
0.129
0.070
0.000
0.000
12.311
0.000
1.206
0.055
1.185
0.022
0.002
0.000
0.022
0.013
0.000
0.000
1.583
0.000
0.127
0.074
12.593
0.004
0.000
0.000
0.143
0.021
0.000
0.000
0.114
0.001
0.091
0.029
1.555
0.004
0.000
0.000
0.021
0.006
0.000
0.000
0.054
0.000
0.048
0.392
3.906
0.090
3.573
0.030
0.055
0.177
0.001
1.669
2.653
1.623
0.039
0.072
0.440
0.064
0.926
0.030
0.016
0.047
0.001
0.553
0.479
0.139
0.011
64.416 624.100 249.577 347.633 161.073
0.263
0.218
0.552
0.366 115.382
52.370
0.001 416.490 171.374
5.147
3.875
264.005
81.157 246.287
63.893
0.000
0.001
Total Dreissena
% Quagga
64.800
0.0
65.599 624.101 254.033 764.120 244.812
—
0.0
—
54.5
—
5.410
95.1
3.995
—
264.557
99.8
79.321 361.669 111.460
—
68.1
—
Total Benthos
% Dreissena
71.393
90.8
66.669 631.440 250.533 767.884 247.250
8.2
98.8
6.9
99.5
9.4
26.002
20.8
5.630
5.9
277.753
95.2
83.414 376.050 113.823
0.9
96.2
1.6
lower in the nearshore (stations E1, E3) than in the
offshore (E2) (Table 4). Offshore epilimnetic production during the stratified period exceeded
nearshore production for the season. Macrozooplankton production in the nearshore ranged from
0.72 g dry wt/m 2 to 1.72 g dry wt/m2. In order of
decreasing contribution, the majority (> 85%) of
this production came from Epischura lacustris,
Leptodiaptomus minutus, Skistodiaptomus oregonensis, Tropocyclops extensus, and Bosmina spp., in
1993, and from E. lacustris, Diacyclops thomasi, S.
oregonensis, Daphnia retrocurva, Bosmina spp. and
L. minutus in 1994. Offshore TZP was 20.03 g dry
wt/m2 in 1993 and 10.75 g dry wt/m2 in 1994. Over
85% of macrozooplankton production came from E.
lacustris, Bosmina spp., T. extensus, D. thomasi,
Mesocyclops edax, S. oregonensis, Eurytemora affinis, and Bythotrephes cederstroemi in 1993, and
from D. thomasi, D. retrocurva, Bosmina spp., E.
lacustris, Leptodiaptomus ashlandi, and B. cederstroemi in 1994. Total zooplankton production in
1993 was elevated compared with that in 1994 pre-
dominantly because of the high level of veliger production, 9.80 g dry wt/m2 compared with 1.69 g dry
wt/m2. The high densities of veligers in the metaand hypolimnion and the large size of these individuals compared with those in the epilimnion suggests that the pediveliger stage may have postponed
settlement (Peterson 1984, Boudreau et al. 1993,
Sprung 1993). Veligers in the hypo- and metalimnion were 64 µm and 27 µm longer, respectively,
than veligers in the epilimnion in 1993, while the
length difference was much less in 1994 - 9 µm. In
normal circumstances when the pediveligers settle
out more rapidly, their production would be associated with the benthic food chain. If the relative production of veligers in the three thermal layers were
similar in 1993 and 1994, then total veliger production at E2 would drop from 9.80 g dry wt/m 2 to
2.48 g dry/m2 in 1993 and TZP would drop to 12.98
g dry wt/m2. Rotifer production contributed a significant proportion to total zooplankton production
in the eastern basin and tended to be higher in 1994
than in 1993 except in the meta- and hypolimnion
38
Johannsson et al.
TABLE 3. Annual benthic production estimates for different taxonomic groups at the sampled Lake Erie
stations, 1993. Production is given in wet, shell-free weight (g/m2/yr).
Species
Nematoda
Platyhelminthes/Nemertea
Oligochaeta
Hirudinae
Amphipoda
Isopoda
Ostracoda
Harpacticoida
Ephemeroptera
Trichoptera
Chironomidae
Gastropoda
Sphaeriidae
Dreissena polymorpha
Dreissena bugensis
Total Dreissena
Total Production
% Dreissena
W1
0.91
0.01
18.70
0.32
0.10
0.00
1.16
1.12
0.02
0.16
7.07
0.02
0.51
448.50
0.00
448.50
478.60
93.71
W3
1.14
1.34
18.99
2.25
4.87
0.00
0.31
0.55
0.00
0.19
1.11
1.18
0.32
3,010.67
0.01
3,010.68
3,042.93
98.98
of the offshore station. Inshore, rotifers contributed
30% (1993) and 40% to 60% (1994) toward TZP.
Offshore, the contribution was approximately 35%
in both years; however, rotifer production was more
important in the epilimnion in 1994 (52%) than in
1993 (36%).
In the west-central basin, total water column production was greater at the nearshore station (WC1)
than in the offshore (WC2): 18.71 g dry wt/m2 as
compared with 13.92 g dry wt/m2 (Table 4). This
difference was mainly because of higher levels of
production of Bosmina spp. and veligers in the
nearshore. Bosmina spp. production was 6.08 g dry
wt/m2 at WC1 and 2.35 g dry wt/m2 at WC2, while
veliger production was 4.13 g dry wt/m2 at WC1
and 0.24 g dry wt/m2 at WC2. Together Bosmina
spp., B. cederstroemi, D. thomasi, M. edax, L. minutus, Eubosmina spp., and calanoid and cyclopoid
copepodids contributed > 85% of macrozooplankton production at WC1, and Bosmina spp., D.
thomasi, B. cederstroemi, M. edax, Leptodiaptomus
sicilis, E. lacustris, Leptodiaptomus siciloides, T.
extensus, D. retrocurva, and Eubosmina spp. contributed > 85% at WC2. Rotifers contributed 23%
toward TZP at WC1, and 46% at WC2. The majority of rotifer production occurred in the epilimnion
where they were the principal grazers at WC2 contributing 66% of TZP.
WC1
0.32
0.30
7.93
0.03
0.18
0.21
0.47
0.03
0.00
0.00
7.44
0.48
0.02
746.64
1,161.54
1,908.18
1,925.59
99.10
WC2
1.86
0.61
32.66
0.07
0.01
0.00
0.54
0.37
0.00
0.00
24.58
0.00
3.04
1.33
32.74
34.07
97.81
34.83
E2
2.19
0.40
53.81
0.01
0.00
0.00
0.64
0.11
0.00
0.00
0.39
0.00
0.18
1.79
532.55
534.34
592.07
90.25
E3
2.42
2.60
15.61
0.25
20.46
0.10
0.27
0.89
0.00
8.42
17.34
5.25
0.07
492.35
2,484.85
2,977.20
3,050.88
97.58
Total zooplankton production at the two sites in
the western basin were markedly different. At the
northern nearshore site (W1), TZP was 12.09 g dry
wt/m2, while in the center of the basin at site W3 it
was 23.77 g dry wt/m2 (Table 4). The difference
was principally a consequence of the much greater
productivity of Daphnia retrocurva in the offshore:
15.42 g dry wt/m 2 as compared with 2.40 g dry
wt/m2. Daphnia were 12% more abundant and 13%
longer at W3 than W1 in 1993. This translated into
a 66% increase in biomass and 543% increase in
production. The marked increase in production was
a result of an exponential increase in the number of
eggs per female with increasing body size. At W3,
Daphnia alone contributed 88% of macrozooplankton production. At W1, D. retrocurva, E. affinis,
Bosmina spp., Diaphanosoma spp., D. thomasi, and
E. lacustris together contributed just > 85% to total
macrozooplankton production. Veliger production
was similar at the two stations, approximately 2.50
g dry wt/m2. Rotifer production was slightly higher
at W3 ( 3.73 g dry wt/m2) than at W1 (2.22 g dry
wt/m2). At both sites, rotifers contributed approximately 17% toward TZP.
The empirical relationship between primary production (PP), measured as photosynthesis, and zooplankton production, developed by Makarewicz and
Likens (1979), can be used to evaluate whether ob-
Benthic and Pelagic Production in Lake Erie: Post-Dreissena
39
TABLE 4. Seasonal zooplankton production at the LEB sites by thermal layer (non-bolded numbers)
and for the whole water column (bolded numbers).
Species/Stations
Cladocerans
Bosmina spp.
Eubosmina spp.
Daphnia retrocurva
D. galeata mendotae
D. longiremis
Daphnia spp.
Ceriodaphnia spp.
Holopedium gibberum
Diaphanosoma sp.
Bythotrephes
Leptodora kindtii
Total Cladocerans
W1-t
0.95
0.05
2.40
0.00
0.15
0.00
0.00
0.00
0.71
0.00
0.03
4.31
Zooplankton Production (g/m2/May-Oct. season)
W3-t
WC1-te WC1-m
WC1-h
0.13
3.22
1.52
1.34
0.29
0.31
0.03
0.01
15.42
0.02
0.00
0.00
0.00
0.00
0.00
0.00
0.19
0.02
0.02
0.01
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.10
0.01
0.06
0.03
0.00
0.10
0.52
0.01
0.32
0.00
0.02
0.00
16.45
3.69
2.17
1.41
WC1-t
6.08
0.36
0.02
0.00
0.05
0.00
0.00
0.00
0.10
0.62
0.02
7.26
Cyclopoids
Diacyclops thomasi
Tropocyclops extensus
Mesocyclops edax
Cyclops vernalis
Cyclopoid copepodids
Cyclopoid nauplii
Total Cyclopoids
0.32
0.01
0.11
0.05
0.09
0.04
0.62
0.51
0.00
0.06
0.01
0.05
0.01
0.65
0.08
0.18
0.21
0.02
0.12
0.02
0.63
0.16
0.02
0.11
0.02
0.10
0.02
0.41
0.35
0.00
0.09
0.05
0.06
0.00
0.56
0.59
0.20
0.41
0.10
0.28
0.04
1.61
Calanoids
Leptodiaptomus minutus
L. ashlandi
Skistodiaptomus oregonensis
L. sicilis
L. siciloides
Limnocalanus macrurus
Eurytemora affiinis
Senecella calanoides
Epischura lacustris
Epischura copepodids
Calanoid copepodids
Calanoid nauplii
Total Calanoids
Total Macrozooplankton
0.04
0.17
0.00
0.10
0.02
0.03
1.84
0.04
0.10
0.12
0.04
0.02
2.51
7.44
0.03
0.05
0.01
0.03
0.00
0.06
0.04
0.00
0.04
0.00
0.12
0.02
0.40
17.50
0.02
0.01
0.02
0.01
0.01
0.00
0.04
0.00
0.10
0.02
0.10
0.01
0.35
4.66
0.13
0.05
0.06
0.01
0.01
0.00
0.08
0.00
0.04
0.02
0.05
0.01
0.46
3.04
0.23
0.06
0.03
0.05
0.02
0.00
0.02
0.00
0.02
0.00
0.12
0.00
0.56
2.53
0.38
0.13
0.11
0.07
0.05
0.00
0.13
0.00
0.16
0.04
0.28
0.02
1.36
10.23
Dreissenids
Veliger
2.43
2.55
2.58
1.46
0.09
4.13
3.90
11.14
0.38
4.87
0.08
2.70
4.35
18.71
Rotifers
Rotifers
2.22
3.73
Total Production
12.09
23.77
t = total water column, e = epilimnion, m = metalimnion, h = hypolimnion
(Continued next page)
served zooplankton production achieved potential
levels set by PP in Lake Erie (Fig. 2). Zooplankton
production in Makarewicz and Likens’ tabulation
included both rotifers, collected with at least a
45-µm mesh net, and crustacean zooplankton. A
similar comparison in the present study would include rotifers, veligers, and macrozooplankton
(TZP). Their PP included all sources of PP including benthic and macrophyte. Only pelagic algal production was measured in the present study which
may underestimate PP at the shallower stations (E1,
E3, W1, and W3). Seasonal TZP was predicted for
each station from seasonal PP estimated during the
present study (Millard et al. 1999). Observed TZP
40
TABLE 4.
Johannsson et al.
(Continued).
Species/Stations
Cladocerans
Bosmina spp.
Eubosmina spp.
Daphnia retrocurva
D. galeata mendotae
D. longiremis
Daphnia spp.
Ceriodaphnia spp.
Holopedium gibberum
Diaphanosoma sp.
Bythotrephes
Leptodora kindtii
Total Cladocerans
Zooplankton Production (g/m2/May-Oct. season)
WC2-te
WC2-m
WC2-h
WC2-t
1.18
0.10
1.07
2.35
0.22
0.01
0.01
0.24
0.12
0.02
0.11
0.25
0.00
0.00
0.00
0.00
0.00
0.02
0.18
0.20
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.02
0.00
0.02
0.00
0.00
0.02
0.82
0.01
0.02
0.00
0.03
1.88
0.63
1.38
3.90
Cyclopoids
Diacyclops thomasi
Tropocyclops extensus
Mesocyclops edax
Cyclops vernalis
Cyclopoid copepodids
Cyclopoid nauplii
Total Cyclopoids
0.13
0.25
0.17
0.01
0.03
0.01
0.61
0.09
0.01
0.11
0.01
0.04
0.02
0.26
0.68
0.00
0.29
0.01
0.02
0.01
1.00
0.90
0.26
0.56
0.02
0.09
0.04
1.87
Calanoids
Leptodiaptomus minutus
L. ashlandi
Skistodiaptomus oregonensis
L. sicilis
L. siciloides
Limnocalanus macrurus
Eurytemora affinis
Senecella calanoides
Epischura lacustris
Epischura copepodids
Calanoid copepodids
Calanoid nauplii
Total Calanoids
Total Macrozooplankton
0.02
0.01
0.00
0.09
0.00
0.00
0.02
0.00
0.06
0.03
0.02
0.01
0.28
2.76
0.03
0.03
0.07
0.09
0.01
0.00
0.01
0.00
0.25
0.02
0.03
0.02
0.55
1.45
0.03
0.06
0.06
0.20
0.32
0.00
0.00
0.00
0.03
0.00
0.01
0.00
0.70
3.09
0.08
0.09
0.15
0.38
0.33
0.00
0.03
0.00
0.34
0.05
0.05
0.03
1.53
7.30
Dreissenids
Veliger
0.16
0.06
0.02
0.24
0.35
1.85
0.35
3.45
6.38
13.92
Rotifers
Rotifers
5.69
Total Production
8.62
t = total water column, e = epilimnion, m = metalimnion, h= hypolimnion
(Continued next page)
from the LEB sites all fell within or close to the
95% confidence interval surrounding the relationship developed by Makarewicz and Likens (Fig. 2).
Zooplankton mean length (ZML) was calculated
for the summer season, 27 June to 30 September in
the eastern and west-central basins, and 15 May to
30 September in the western basin, as an index of
planktivory. Shorter ZMLs are thought to be associated with more intense planktivory (Brooks and
Dodson 1965, Lynch 1979, Mills et al. 1987). Mills
et al. (1987) suggested that a ZML of 0.8 mm, as
determined with a 153-µm mesh net, was characteristic of a well balanced fish community. Zooplankton mean lengths were converted to 153-µm
Benthic and Pelagic Production in Lake Erie: Post-Dreissena
TABLE 4.
41
(Continued).
Species/Stations
Cladocerans
Bosmina spp.
Eubosmina spp.
Daphnia retrocurva
D. galeata mendotae
D. longiremis
Daphnia spp.
Ceriodaphnia spp.
Holopedium gibberum
Diaphanosoma sp.
Bythotrephes
Leptodora kindtii
Total Cladocerans
Zooplankton Production (g/m2/May-Oct. season)
E1-t93
E3-t93
E2-e93
E2-m93 E2-th93
0.08
0.15
0.33
0.10
0.56
0.00
0.00
0.00
0.00
0.00
0.01
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.01
0.00
0.00
0.00
0.00
0.00
0.10
0.05
0.01
0.01
0.01
0.10
0.03
0.00
0.12
0.22
0.54
0.20
0.57
E2-t93
0.99
0.01
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.16
0.00
1.18
Cyclopoids
Diacyclops thomasi
Tropocyclops extensus
Mesocyclops edax
Cyclops vernalis
Cyclopoid copepodids
Cyclopoid nauplii
Total Cyclopoids
0.01
0.07
0.00
0.00
0.01
0.00
0.09
0.04
0.18
0.05
0.00
0.00
0.00
0.28
0.02
0.70
0.02
0.00
0.01
0.00
0.74
0.09
0.01
0.11
0.00
0.01
0.00
0.21
0.37
0.08
0.14
0.01
0.01
0.00
0.60
0.47
0.78
0.26
0.01
0.02
0.00
1.55
Calanoids
Leptodiaptomus minutus
L. ashlandi
Skistodiaptomus oregonensis
L. sicilis
L. siciloides
Limnocalanus macrurus
Eurytemora affinis
Senecella calanoides
Epischura lacustris
Epischura copepodids
Calanoid copepodids
Calanoid nauplii
Total Calanoids
Total Macrozooplankton
0.41
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.10
0.11
0.01
0.00
0.64
0.86
0.54
0.00
0.19
0.02
0.00
0.00
0.02
0.00
0.30
0.06
0.07
0.02
1.23
1.72
0.35
0.05
0.00
0.01
0.03
0.00
0.01
0.00
0.19
0.11
0.02
0.02
0.79
2.06
0.20
0.04
0.12
0.01
0.00
0.00
0.07
0.00
1.05
0.00
0.03
0.00
1.52
1.93
0.08
0.06
0.09
0.02
0.01
0.00
0.09
0.00
0.06
0.00
0.00
0.00
0.41
1.58
0.63
0.15
0.21
0.04
0.04
0.00
0.16
0.00
1.30
0.11
0.06
0.03
2.72
5.45
2.20
4.26
3.35
9.80
2.38
6.64
1.99
8.18
4.16
0.68
5.60
2.31
5.05
20.30
13.98
Dreissenids
Veliger
0.48
1.00
modified as per 1994(see text)
Rotifers
Rotifers
0.53
1.29
Total Production
1.86
4.01
Total Production (modified veligers)
t = total water column, e = epilimnion, m = metalimnion, h = hypolimnion
(Continued next page)
equivalent ZMLs and ranged from 0.49 mm at WC2
to 0.67 mm at W3 (Table 5). The lack of larger
species of Daphnia, normally D. galeata mendotae
in the Great Lakes, was also indicative of intense
fish predation (Wells 1970, Johannsson et al. 1991).
In 1993, D. g. mendotae was observed briefly at
only one site (E1). In 1994, D. g. mendotae was
again observed briefly at E1 and was less abundant
than D. retrocurva at E2.
Regression analysis indicated that the percent deviation of observed TZP from predicted TZP [(predicted TZP—observed TZP)/predictedTZP*100]
was negatively related to summer ZML (p < 0.001,
r 2 = 0.88), as were the percent deviations of the
42
TABLE 4.
Johannsson et al.
(Continued).
Species/Stations
Cladocerans
Bosmina spp.
Eubosmina spp.
Daphnia retrocurva
D. galeata mendotae
D. longiremis
Daphnia spp.
Ceriodaphnia spp.
Holopedium gibberum
Diaphanosoma sp.
Bythotrephes
Leptodora kindtii
Total Cladocerans
Zooplankton Production (g/m2/May-Oct. season)
E1-t94
E3-t94
E2-e94
E2-m94 E2-th94
0.04
0.05
0.53
0.14
0.07
0.00
0.00
0.01
0.00
0.00
0.02
0.08
0.08
0.52
0.43
0.00
0.00
0.02
0.02
0.01
0.00
0.00
0.01
0.01
0.01
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.01
0.02
0.08
0.02
0.01
0.02
0.01
0.02
0.00
0.00
0.10
0.17
0.74
0.71
0.53
E2-t94
0.74
0.02
1.03
0.05
0.03
0.00
0.00
0.00
0.00
0.10
0.00
1.96
Cyclopoids
Diacyclops thomasi
Tropocyclops extensus
Mesocyclops edax
Cyclops vernalis
Cyclopoid copepodids
Cyclopoid nauplii
Total Cyclopoids
0.24
0.00
0.00
0.00
0.01
0.00
0.26
0.33
0.01
0.01
0.00
0.02
0.00
0.37
0.16
0.02
0.02
0.00
0.04
0.01
0.25
1.44
0.00
0.05
0.00
0.02
0.00
1.51
0.28
0.00
0.02
0.00
0.01
0.00
0.32
1.88
0.03
0.08
0.00
0.07
0.01
2.08
Calanoids
Leptodiaptomus minutus
L. ashlandi
Skistodiaptomus oregonensis
L. sicilis
L. siciloides
Limnocalanus macrurus
Eurytemora affinis
Senecella calanoides
Epischura lacustris
Epischura copepodids
Calanoid copepodids
Calanoid nauplii
Total Calanoids
Total Macrozooplankton
0.04
0.00
0.09
0.00
0.00
0.00
0.01
0.00
0.07
0.02
0.10
0.03
0.36
0.72
0.06
0.01
0.04
0.01
0.00
0.00
0.00
0.00
0.14
0.06
0.06
0.04
0.42
0.96
0.12
0.06
0.05
0.02
0.00
0.01
0.01
0.00
0.25
0.11
0.05
0.02
0.70
1.69
0.16
0.08
0.03
0.02
0.00
0.00
0.00
0.00
0.23
0.01
0.02
0.00
0.55
2.77
0.01
0.01
0.01
0.01
0.00
0.00
0.00
0.00
0.03
0.00
0.01
0.00
0.09
0.93
0.29
0.15
0.08
0.05
0.00
0.01
0.01
0.00
0.51
0.12
0.07
0.02
1.33
5.37
Dreissenids
Veliger
0.44
0.37
1.47
0.15
0.06
1.70
3.34
6.51
0.27
3.20
0.08
1.07
3.69
10.75
Rotifers
Rotifers
0.79
2.18
Total Production
1.95
3.51
T = total water column, e = epilimnion, m = metalimnion, h = hypolimnion
macrozooplankton + veliger production (p = 0.001,
r2 = 0.85), and macrozooplankton alone (p = 0.003,
r2 = 0.78): one outlier (WC1) was removed from
these analyses (Fig. 3). The relationships were still
significant if WC1 were included but the explained
variances were lower (r2 = 0.45, 0.43, and 0.47 respectively). The slopes of the three relationships
were not significantly different (ANCOVA p =
0.33): the adjusted means were significantly differ-
ent from one another (p < 0.001). Neither variation
in dreissenid seasonally-weighted mean biomasses
in 1993 nor dreissenid clearance rates in May of
1993 and 1994 could explain the percent deviation
in observed versus predicted zooplankton production. The estimated clearance rates were taken from
Table 17 of Graham et al. (1996).
Thus zooplankton production in Lake Erie appears to be controlled by a combination of the level
Benthic and Pelagic Production in Lake Erie: Post-Dreissena
FIG. 2. Relationship between seasonal zooplankton production (TZP) and primary production (PP): the predictive relationship and 95%
confidence intervals are presented for the equation developed by Makarewicz and Likens (1979)
where log(TZP mg C/m2) = 3.032 + 0.0063 (PP g
C/m2), and (●) data from Lake Erie in 1993 and
1994. Carbon data were converted to dry weight
assuming a 50% C composition. *Data for E2
1993 where the veliger production was modified
(see text for explanation).
of PP during the growing season (May to October)
and the intensity of predation. These factors could
be expressed jointly in multiple regression relationships where zooplankton production is expressed in
g dry wt/m2/season, ZML is in mm, and PP is in g
C/m2/season: MP = macrozooplankton production,
and MVP = macrozooplankton + veliger production:
TZP = –36.5 + 62.7 * ZML + 0.111 * PP
F = 51.1, p < 0.001, n = 8, adjusted R2 = 0.94
(4)
MVP = –34.0 + 57.7 * ZML + 0.083 * PP
F = 16.4, p = 0.006, n = 8, adjusted R2 = 0.82
(5)
MP = –28.1 + 46.2 * ZML + 0.076 * PP
F = 11.8, p = 0.013, n = 8, adjusted R2 = 0.76
(6)
The statistical procedure identified WC1 as an
outlier and it was removed from these relationships.
Tolerance levels were greater than 0.95 indicating
no correlation among the independent variables.
Log transforming the zooplankton production esti-
43
FIG. 3. Percent deviation of the Lake Erie total
zooplankton production estimates from the
Makarewicz and Liken (1979) relationship (see
Fig. 2) with respect to the summer zooplankton
mean length. See text for definition of summer
period. Open symbols are station WC1.
TABLE 5. Whole-water column, summer zooplankton mean length (ZML) as determined by a
153-um net. The 1993 data were taken from Figure 4 of Johannsson et al. (1999). The 1994 and
E1 1993 data were converted from 64-µm to 153µm equivalent data using the equation of
Johannsson et al. (1999): ZML153 = 0.042 + 1.330
ZML64 . The season was determined by temperature. June 27 to Sept. 30 in the eastern and westcentral basins, May 15 to Sept. 30 in the western
basin.
Station/Year
E1
E3
E2
WC1
WC2
W1
W3
Mean Body Length (mm)
1993
1994
0.56
0.54
0.54
0.52
0.64
0.61
0.52
0.49
0.53
0.67
mates did not improve the relationships. The
veliger distribution and size structure at E2 in1993
were unusual; therefore, the adjusted values described above were used for all the percent deviation and regression analyses.
Benthos
Benthic production was higher at the nearshore
stations of the central and eastern basins than at the
44
Johannsson et al.
offshore stations (Table 3). The eastern and western
basins had similar ranges of benthic production.
The zebra mussel, D. polymorpha, contributed most
of the production in the western basin, D. bugensis
contributed the majority of the benthic production
at the other stations. The calculated P/B ratios of D.
polymorpha averaged 4.4 (SE = 0.7) while those for
D. bugensis averaged 5.3 (SE = 1.8), and were
greatest at the nearshore stations, and lowest at the
deep offshore station of the eastern basin (P/B =
2.0).
After the mussels, oligochaetes contributed the
most to benthic production in the lake. Annual production by the oligochaetes ranged between 8 and
54 g/m2/y (Table 3), with their greatest production
at the two offshore hypolimnetic stations, WC2 and
E2. Chironomids, mostly Chironomus thummi, were
important contributors to the benthic production at
the inshore stations and less important offshore in
the eastern basin, but total chironomid production
was greatest in the offshore of the west-central
basin.
Benthic production was much lower (97.8
g/m2/y) at the offshore west-central station (WC2)
than at the other stations, due to the low density of
Dreissena at that station. The benthic community at
this station was comprised of oligochaete worms,
chironomids, Pisidium, and a few Sphaerium clams,
typical of the hypolimnetic benthic community of
Lake Erie prior to the arrival of Dreissena (Dermott
1994). The low proportion of Dreissena and relatively high biomass of Sphaeriidae (1.2 g/m2, wet
shell-free) and Chironomidae at station WC2 probably reflects the low mid-summer oxygen conditions
in the hypolimnion of the central basin. The
oligochaetes, Chironomus spp., and several of the
Pisidium species are adapted to survive in water
that experiences short periods of low oxygen
(Jonasson 1972). At this station, calculated production by the Tubificidae was 32.6 g/m2/y, size-frequency production by the Chironomus semireductus
group was 17.1 g/m2/y (P/B = 1.7) and that by C.
thummi group was 7.2 g/m2/y (P/B = 2.9). Together,
production by the Chironomidae represented 25%
of the total benthic production at this hypolimnetic
station.
Amphipods were only common at the nearshore
stations. No specimens of the deep-water amphipod
Diporeia hoyi were found in any of the samples collected for this study. Gammarus fasciatus was present at all the nearshore stations, its biomass ranged
from 0.05 g/m2 in the west basin to was 0.11 g/m2
at WC1 in the central basin. The biomass (3.6 g/m2)
and production (20.5 g/m2/y) of this species were
greatest at the nearshore station E3 in the eastern
basin, where a large population of Gammarus was
associated with the Dreissena colonies (Table 2).
However, the high production of amphipods at E3
represented only 0.7% of the total annual production at E3 because of the high biomass of Dreissena
spp. at that station. Gammarus also contributed a
minor amount to the production at the nearshore,
west-central basin station. The calculated P/B ratios
of Gammarus averaged 3.9 (SE = 0.9) in Lake Erie,
ranging between 1.1 and 5.7. Sphaeriidae clams
contributed little to the benthic production of Lake
Erie, except at station WC2. Although numerous,
the small Nematoda contributed a minor share of
the production in the eastern basin (2.2 to 2.4
g/m2/y). The contributions of the other members of
the benthic community were generally less than 1
g/m2/y.
Both abundance and biomass of the benthic fauna
were dominated by the vast number of settled
Dreissena spp. (Dahl et al. 1995). In 1993, the
quagga mussel (D. bugensis) was not present in the
western basin but represented 95% to 99% of the
mussels present at the two stations > 20 m, WC2
and E2. During 1993, D. bugensis became increasingly more common in the central and eastern
basins. Dreissena bugensis was able to colonize
WC2 during the summer of 1993 when the hypolimnion of the central basin did not go anoxic
(M. Charlton, pers. com.). Biomass of D. bugensis
at station WC2 increased steadily from 0.05 g/m2/
(wet shell-free) in May, 1993 to 28.12 g/m2 in May
1994, as the settled mussels grew over the year.
Only one cohort existed at this site, individuals
grew from an average of 0.0002 g/ind on 20 May
1993 to 0.2917 g/ind (wet shell-free) by 20 May
1994.
DISCUSSION
Benthic filtering bivalves, such as Dreissena, can
sequester much of the pelagic primary production
(Officer et al. 1982, Stanczykowska and
Lewandowski 1993), thereby altering the balance
between pelagic and benthic foodwebs. The biomass and production of the benthic and pelagic fish
communities will shift to reflect these changes. Impacts of dreissenids were observed on both the
pelagic and benthic foodwebs in Lake Erie. The resultant impact on potential fish biomass and production is discussed in the concluding section.
Conditions that favor bivalve dominance include
Benthic and Pelagic Production in Lake Erie: Post-Dreissena
a high proportion of suitable substrate, lack of stratification of the overlying water, and good water
flow. Within Lake Erie, these areas can be found
year round along the north and south shores of the
eastern basin and among the rocky islands of the
western basin. In the offshore of the central and
eastern basins conditions are favorable during
isothermal periods. Areas less favorable for dreissenids include those regions which stratify in the
summer separating the mussels from the productive
surface layers, and the western portion of the central basin which has periodic hypolimnetic anoxia
or low oxygen levels in the late summer (Bertram
1993, Charlton et al. 1993). Thus the impacts of
dreissenids would be expected to vary both spatially and temporally within the lake.
Zooplankton Production
No estimates of zooplankton production were
made in Lake Erie immediately prior to the invasion of dreissenids. Therefore their impact can not
be assessed directly. The energy pathways leading
to zooplankton production consists of several links
which could be altered by dreissenids. They could
decrease the levels of chlorophyll a and photosynthesis (Leach 1993; Fahnenstiel et al. 1995a, b;
Millard et al. 1999), alter the level of detrital material and bacteria in the water column, consume small
zooplankton (Shevtsova et al. 1986 in MacIsaac et
al. 1995, MacIsaac et al. 1991), and compete with
zooplankton for the available primary production.
Chlorophyll a concentrations are below those
predicted from total phosphorus concentrations and
Daphnia composition in the nearshore of the eastern basin (Graham et al. 1996). Millard et al.
(1999) also documented a decrease in seasonal primary production in this region compared with that
predicted from total phosphorus. The declines in
chlorophyll a, and consequently primary production, were attributed to dreissenids. Zooplankton
production is partially dependent on the level of
primary production (Makarewicz and Likens 1979,
present study). Therefore, to the extent that
dreissenids have depressed primary production,
they have also depressed potential zooplankton
production.
The second link between observed primary production and total zooplankton production was not
affected by the presence of adult dreissenids; however, 88% of the variability in the LEB TZP estimates from the Makarewicz and Likens relationship
could be accounted for by zooplankton mean length
45
(ZML). Planktivory may play a strong role in regulating zooplankton production in Lake Erie as TZP
was reduced by an average of 36% (range 15% to
50%, n = 5) at sites with ZMLs of 0.49 to 0.56, excluding WC1. This modification of bottom-up control of zooplankton production by top-down
influences agrees with the top-down bottom-up theory of trophic regulation (McQueen et al. 1986,
1989).
An impact of direct competition for algal food resources could not be demonstrated, although zooplankton and dreissenids must both be consuming
the phytoplankton produced in the unstratified regions throughout the season. This competition is reduced as zooplankton feed throughout the water
column, while dreissenids feed predominantly from
the bottom waters (Fréchette et al. 1989, MacIsaac
et al. 1999). Dreissenid impact on chlorophyll a
and competition with zooplankton increases as the
water column shortens and as the level of turbulence increases.
Total zooplankton production now consists of
veliger larvae as well as the traditional crustacean
and rotifer species. Veligers can frequently contribute 10% to 25% to total zooplankton production.
If veligers were excluded from the calculation of
TZP, TZP would fall below the 95% confidence interval for the Makarewicz and Likens relationship
at stations E1, E3, and W1. Veligers may be replacing some of the traditional zooplankton production.
If the potential capacity for zooplankton production is set from the bottom up and modified by
planktivory, then the potential production can be estimated knowing the relationship between total
phosphorus and PP (Millard et al. 1999) and the relationship between PP, ZML, and TZP developed
above (equation 4). The Lake Erie data set is restricted in the size range of zooplankton communities encountered. A ZML of 0.67 mm (observed at
W3) was assumed as the optimum size, instead of
the 0.8 mm suggested by Mills et al. (1987) in
order to stay within the bounds of the regression
equations. Comparing observed TZP with potential
predicted TZP suggested that TZP was particularly
depressed in the nearshore of the eastern basin
(Table 6). TZP at sites E1 and E3 was 9% to 23% of
capacity. The middle of the western basin (W3) and
the nearshore of the west-central basin (WC1) were
operating at 85% of capacity, and the remaining
sites at 45% to 65% of capacity.
The decline in observed TZP can be divided
roughly into that attributable to predation and that
to decreased PP, keeping in mind that there is error
46
Johannsson et al.
TABLE 6. Calculation of potential productive capacity of zooplankton at the LEB sites assuming a summer zooplankton mean length of 0.67 mm. Primary production (PP (gC/m2/season)) was predicted from
May to October seasonally-weighted mean total phosphorus (TP (ug/L)) using the equation of Millard et
al. (1999) (PP = 390.5TP/(18.45+TP)). Potential total zooplankton production (Pot-TZP (g dwt./m2/season)) was estimated from equation (4). Similarly, Pot-TZP* was estimated using the observed ZMLs.
Observed production is expressed as a percentage of potential production.
Pot-TZP*
ZML = Observed
TP
PP
Pot-TZP
(ZML = 0.67)
TZP
Observed
Percent
Obs/Pot
7.8
8.5
6.6
10.8
12.8
17.5
19.1
116
123
103
144
160
190
199
18.83
19.62
17.37
21.95
23.70
27.05
27.99
1.86
12.98
4.01
18.71
13.91
12.09
23.77
10
66
23
85
59
45
85
11.66
17.66
8.90
12.18
11.98
17.93
27.99
16
73
45
154
116
67
85
1994
E1*
10.1
E2
8.1
E3*
8.5
* summer ZML ≤ 0.56
138
119
123
21.28
19.17
19.62
1.95
10.71
3.51
9
56
18
12.82
15.26
9.85
15
70
36
Station/Year
1993
E1*
E2
E3*
WC1*
WC2*
W1*
W3
associated with the predictive regression relationships, particularly the latter which is based on a
limited number of points. The difference between
the potential TZP calculated at optimal ZML and
that calculated at observed ZMLs is a measure of
the impact of planktivory. The difference between
the potential TZP calculated at observed ZMLs and
the observed TLP is a measure of changes in PP.
The depression in zooplankton production in the
nearshore region of the eastern basin was principally because of the impact of dreissenid filtering
on chlorophyll a levels and consequently PP (Millard et al. 1999, Table 6). After removing the effect
of changes in PP, TZP was depressed by 40% to
50% at sites with ZMLs < 0.56. A similar analysis
could be done using macrozooplankton + veliger
production or macrozooplankton production using
equations (5) and (6). The slopes of equations (4),
(5) and (6) were not significantly different, thus the
results of such an analysis would be similar.
Benthic Production
Western Basin
Production was almost exclusively dominated by
Dreissena which accounted for over 95% of the annual production and wet shell-free biomass in the
basin during 1993. Lack of benthic production esti-
Percent
Obs/Pot*
mates for Lake Erie prior to the colonization of the
lake by Dreissena prevent direct comparison of
production. Thus benthic biomass was used as a
surrogate for production, to compare pre- and postmussel periods. Annual wet benthic biomass in the
western basin averaged 351.4 g/m2 (shell-free) during 1993. Average biomass in the western basin
during autumn 1979 (without Unionidae), 9 years
prior to the invasion by the zebra mussels, was 6.7
(S.E. 1.47; N = 52) g/m 2 (Dermott 1994). This
value was comparable to the benthic biomass (7.0
g/m2, excluding the mussels) in the west basin during 1993, after the invasion of Lake Erie by D.
polymorpha. This similarity suggests that the huge
biomass in the mussel populations was not at the
expense of the biomass of the remaining benthic
community.
In the nearshore areas of Lake Erie, the populations of Gammarus fasciatus increased in association with the newly established mussel colonies.
The mussel colonies provide interstitial spaces and
a probable increased food supply in the form of
pseudofaeces (Dermott et al. 1993, Stewart and
Haynes 1994). Biomass of Gammarus in the western basin increased from an average of 0.002 (S.E.
0.0008 g/m2) at 52 sites sampled during 1979 (Dermott 1994) to 0.487 g/m2 (wet weight) at the two
stations sampled during 1993.
Benthic and Pelagic Production in Lake Erie: Post-Dreissena
West-Central Basin
Dreissena have altered production of the benthic
community more at the shallower station (WC1)
where they accounted for > 99% of the total production, than at the deeper station (WC2) where
they accounted for only 27% of production. This is
consistent with the low mussel density at the deeper
station. The average wet benthic biomass in the
central basin during 1979 was 10.6 (S.E. 1.43; N =
69) g/m2 (Dermott 1994), compared with 12.2 g/m2
(without Dreissena) in 1993. Again, this indicates
that there has been little change in biomass of endemic benthic fauna, but Dreissena have increased
the benthic biomass of the central basin sites to
396 g/m2 (shell-free).
Eastern Basin
In 1993, total abundance of the benthic fauna was
greatest in the eastern basin, because of the very
high density of recently settled quagga mussels (D.
bugensis) of < 1 mm length (Dahl et al. 1995). As
in the western basin, benthic production and biomass were dominated by Dreissena and the huge
amount of biomass in the mussel population was in
addition to the pre-mussel biomass of the benthic
community. In 1979, average wet biomass in the
eastern basin was 7.6 (S.E. 1.03; N = 38) g/m 2,
compared to 13.8 g/m 2 (without Dreissena) in
1993. The total benthic biomass including Dreissena in 1993 was 326.9 g/m2. Thus, energy transferred to the mussels was presumably removed
from the pelagic foodweb or derived from more efficient use of organic material which was settling to
the bottom. Although the biomass of the benthic
community had not declined, community composition in the eastern basin had been altered. Historically, the burrowing amphipod, Diporeia, was
common in the profundal zone (> 30 m) in the eastern basin, contributing up to 20% of the biomass
(Barton 1988, Flint and Merckel 1978, Dermott
1994). The wet biomass of this species averaged
over all the eastern basin during 1979 was 1.7 (S.E.
0.5; n = 38) g/m2. No specimens of Diporeia were
collected in this study at the deep 38 m station (E2)
between May 1993 and May 1994. Populations of
this amphipod have disappeared, possibly because
of competition for settling algae, in particular the
large diatoms with the large populations of quagga
mussels (D. bugensis) now present in Lake Erie at
depths beyond 30 m (Dermott and Munawar 1993,
Dermott and Kerec 1997). In all the other Great
Lakes, Diporeia accounts for the majority of the
47
benthic production, and is a key component of the
foodweb (Hurley 1986, McDonald et al. 1990).
The energy to support the high biomass and production of Dreissena in Lake Erie appears not to be
at the expense of the benthic community, except for
the physical competition with the native Unionidae
and Sphaeriidae clams (Ricciardi et al. 1996).
Rather the energy is being diverted from the microbial or pelagic foodwebs. It might be expected that
the uncoupling of the benthic-pelagic link to fish
production through the deep-water amphipod Diporeia in the hypolimnion of the eastern basin may
be causing a reduction in condition and commercial
catch of pelagic rainbow smelt (Osmerus mordax,
Witzel et al. 1994). However, the increase in deepwater Dreissena may favor benthic feeding fish
species such as whitefish (Coregonus clupeaformis), a native coregonid, and freshwater
drum (Aplodinotus grunniens) (French and Bur
1993).
Comparison of Benthic and Pelagic Production
Does the dominance of pelagic production over
non-dreissenid benthic production in 1993 (Table 7)
mean that fish production in Lake Erie was more
dependent on the pelagic foodweb? That will depend on the relative mean size of the plankton and
benthos and on the amount of dreissenid production
which went into higher trophic levels. Borgmann
(1982) argued that an ecosystem has a characteristic
efficiency of biomass or energy transfer from
smaller to larger organisms (particle-size efficiency
hypothesis), and that the amount of biomass or energy passed to predators by prey depends on the relative size of the predator and its prey. In this way, a
fish would obtain more energy from a larger organism, like an amphipod, than from a smaller organism, like a cladoceran. Thus, pelagic and benthic
biomass are not equivalent in supporting fish production. Boudreau and Dickie (1992) developed an
empirical relationship relating the biomass (expressed as kcal/m 2 ) and mean mass (again expressed in kcal) of organisms in an ecosystem from
plankton to fish using mean mass and total biomass
of phytoplankton, zooplankton + benthos, and fish.
log (Biomass) =
a – 0.05 * log (Mean Individual Mass)
(7)
If the biomass and mean individual mass of one
group of organisms are known, then the intercept
“a” can be calculated for that system and the bio-
48
Johannsson et al.
TABLE 7.
Comparison of benthic and pelagic production at the LEB sites in Lake Erie: 1993.
Dreissenids
96.7
75.2
79.7
Percent Contribution
Other Benthos
2.4
8.2
8.7
Zooplanktona
0.8
16.6
11.6
92.3
19.7
0.8
36.9
6.9
43.5
West
W1
557
W3
3,252
a Zooplankton includes macrozooplankton and veligers.
bE2 with adjusted veliger production (see text).
77.7
92.8
5.2
1.0
17.1
6.2
mass of a different group of organisms of a known
mean mass calculated. The intercept “a” was determined for each site for 1993 from the observed zooplankton plus benthic data, and then for the
zooplankton and benthos separately. These intercepts were inserted into the equation to determined
the capacity of zooplankton and benthos both separately and together to support a fish community
with a mean individual mass of 460 g wet wt (600
kcal). Fish biomass was converted to an estimate of
annual production using the following equation
from Boudreau and Dickie (1989):
fish. The estimates of fish production derived from
these equations are considered potential production
because they were estimated from relationships developed from traditional ecosystems: the Lake Erie
ecosystem has been disturbed recently by the invasion of dreissenids and Bythotrephes and by other
exotics such as smelt and alewife during this century, and may not be functioning efficiently.
Potential fish production (PFP) was determined
from the combined benthos + zooplankton biomass
and mean mass estimates. Boundreau and Dickie
(1989) noted that the contribution of the benthic
and zooplankton components varied between
ecosystems. The PFP derived from the benthic and
pelagic food chains were used separately to suggest
their potential relative importance in supporting
fish production in Lake Erie. The sum of these separate estimates was 13.5% (± 6.6% S.D.) greater
than the estimate derived from benthos + zooplankton. It was found that the benthic food chain should
support 75% to 95% of the PFP in Lake Erie in all
the regions studied except in the nearshore of the
west-central basin where the contributions from the
two food chains were essentially equal (Table 8).
Thus the lake, as represented by the sites studied,
was dominated by the benthic foodweb irrespective
of any consumption of dreissenids by higher trophic
levels.
Basin
East
Station
E3
E2
E2-altb
Total Production
(g wet wt/m2)
3,119
710
670
West-Central
WC1
WC2
2,068
173
log (Production) = 0.08 –0.32 * log
(Mean Individual Mass) + 1.01 * log (Biomass) (8)
where the units are the same as above.
The chosen mean mass of the fish (460 g wet wt)
will not influence the relative contribution from
pelagic and benthic sources.
The equations of Boudreau and Dickie (1989,
1992) were developed for normally functioning
ecosystems and will overestimate the potential of a
disturbed portion of the foodweb to support fish
production. Therefore, dreissenids were excluded
from the benthic estimates as it was likely that they
were at least a partial energy sink. Rotifers and
meiofauna were not included in these calculations.
Veligers are closer to the size of small copepods
and cladocerans, and therefore were included. Dry
weight and wet weight were converted to kcal using
the following equalities (McLaren et al. (1989) and
Banse and Mosher (1980) in Boudreau and Dickie
(1992)): 1 g dry wt = 6 kcal and 1 g wet weight = 1
kcal for invertebrates and 1 g wet wt = 1.3 kcal for
ACKNOWLEDGMENTS
Without the support and help of a number of people this project would never have been accomplished. We thank John Cooley and Vic Cairns for
initiating the DFO study in Lake Erie in response to
Benthic and Pelagic Production in Lake Erie: Post-Dreissena
49
TABLE 8. Potential fish production (PFP g wet wt/m2/y) in Lake Erie derived from benthic + zooplankton biomass and mean mass assuming a normally functioning ecosystem and a mean fish biomass of 460
g wet wt. Percentage of PFP derived from the pelagic and benthic food webs (May 1993 to May 1994)
derived separately according to the relationships of Boudreau and Dickie (1989, 1992). See text for more
detailed desription. Dreissenids were excluded. Data rounded to the nearest 5%.
1993 - Offshore
Percentage of
PFP Production
Pelagic
Benthic
20
80
Basin
West
PFP
1.2
West-Central
3.1
15
85
1.0
50
50
East
2.3
25
75
2.0
5
95
the dreissenid invasion. Boat time and sampling
support were generously given by the Ontario Ministry of Natural Resources and Coast Guard
Canada. We thank Cheryl Hopcroft for the excellent
work she did enumerating and measuring the zooplankton, Beak Consultants for the benthic enumeration, and Susan Doka and Mimi Gemininc for help
in analyzing the benthic data. The graph of Lake
Erie is from the hands (computer) of Carolynn
Bakelaar. A special thanks goes to Don Noakes who
gave me a place at the DFO laboratory in Nanaimo
to work on these data and to Collin Wallace who
shared his office with me during that period.
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1970–1991. J. Great Lakes Res. 19(2):224–236.
Borgmann, U. 1982. Particle-size-conversion efficiency
and total animals production in pelagic ecosystems.
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Editorial handling: W. Gary Sprules
Benthic and Pelagic Production in Lake Erie: Post-Dreissena
53
APPENDIX 1a. Length-weight relationships used to estimate zooplankton biomass in this study. W = aLb,
where length is in mm and weight is in µg dry weight. Biomass of Dreissena was determined using W =
a+bL+cL2 where length is in microns and weight is in 10–3 µg dry weight.
Taxon
CLADOCERA
Bosmina, Eubosmina
Daphnia, Diaphanosoma, Sida spp.
Polyphemus pediculus
Holopedium gibberum
Chydorus sphaericus
Alona sp.
Bythothrephes cederstroemi
Leptodora kindti
COPEPODA
Calanoida
Generic equation
Epischura
Senecella calanoides
Calanoid nauplii
Cyclopoida
Generic Equation
Mesocyclops edax
Cyclopoid nauplii
Harpactacoida
DREISSENA VELIGERS
a
b
c
26.6
5.00
6.93
11.21
33.23
29.70
11.13
0.44
3.13
2.84
2.15
3.04
3.21
3.48
2.77
2.67
Bottrell et al. 1976
Bottrell et al. 1976 (Dumont et al. 1975)
Dumont et al. 1975
Yan (OMEE, Dorset, pers. com.)
Malley et al. 1989
Dumont et al. 1975
Yan (OMEE, Dorset, pers. com.)
Rosen 1981
5.50
6.50
7.70
4.20
2.46
2.63
2.33
2.48
Sprules (U. of Toronto, pers. com.)
Culver et al. 1985
Culver et al. 1985
Sprules (U. of Toronto, pers. com.)
5.50
2.46
6.66
2.89
4.20
2.48
4.20
2.48
58.207 –2.636
0.037
Source
Sprules (U. of Toronto, pers. com.)
Culver et al. 1985
Sprules (U. of Toronto, pers. com.)
Sprules (U. of Toronto, pers. com.)
Hillbricht-Ilkowska and Stanczykowska 1969
APPENDIX 1b. Bëlehrádek’s co-efficients used to calculate egg development times for zooplankton production estimates by the egg-ratio
method. The calanoid coefficients were derived from the relationships in
Cooley and Minns (1978).
Species
Bosmina/Eubosmina spp.
Daphnia spp.
Diaphanosoma sp.
Diacyclops/Tropocyclops
Mesocyclops edax
Cyclops vernalis
Leptodiaptomus minutus
L. ashlandi
L.. sicilis
L. siciloides
Skistodiaptomus oregonensis
Eurytemora affinis
Epischura lacustris
a
3750848
65912
1767
18901
19318
8128
40994
40994
45284
38148
156046
38148
38148
Bëlehrádek’s Coefficients
α
β
–15.40
–3.11
–6.10
–2.12
–1.90
–1.08
–4.80
–1.77
–0.48
–1.79
–2.08
–1.67
–4.72
–2.00
–4.72
–2.00
–5.79
–2.00
–4.01
–2.00
–8.00
–2.31
–4.01
–2.00
–4.01
–2.00
54
APPENDIX 2.
1993–1994.
Johannsson et al.
Literature values for P/B ratios for the calculation of benthic production in Lake Erie
SPECIES
Coelenterata, Hydra
Nematoda, Adenophorea
Tardigrada
Turbellaria, Tricladida
Nemertea, Prostoma
Oligochaeta
Enchytraidae
Naididae
Lumbriculidae
Tubificidae
Hirudinae, Helobdella spp.
Glossiphoria complanata
Mooreobdella microstoma
Mollusca
Gastropoda, Physella spp.
Stagnicola elodes
Bithynia tentaculata
Gyraulus
Helisoma anceps
Elimia livescens
Pleurocera acuta
Amnicola spp.
Valvata spp.
Sphaeriidae, Sphaerium spp.
Sphaerium corneum
Pisidium spp.
Musculium securis
Dreisseniidae, D. polymorpha
D. bugensis
Crustacea
Harpacticoida, Canthocamptidae
Ostracoda, Candoniidae
Cyprididae
Cypridopsidae
Lymnocytheridae
Asellidae, Caecidotea
Gammaridae, Gammarus fasciatus
Crangonyx
Archnoidea, Hydracarina
a
d
g
Dermott 1995
Johnson and Brinkhurst 1971
Menzie 1981
L.E. this study
P/B
2.7
14
5
7.3
4.6
REF.
h
h
4
6.1
3
4.6
3.4
2.2
1.6
f
h
d
h
e
c
3.2
5
1.6
5
5
1.6
1.6
2.1
1.5
3.5
3.5
1.9
3.5
4.4
5.3
e
11
4
5
5
5
3.2
3.9
4.8
5
b
e
h
h
c
i
i
c
e
d
e
L.E.
L.E.
h
h
SPECIES
Insecta
Ephemeroptera, Hexagenia
Heptageniidae
Tricorythodes
Tricoptera, Oecetis
Leptostoma
Molanna
Diptera
Tanypodinae, Ablabesmyia
Coelotanypus
Procladius spp.
Diamesinae, Pagastia
Prodiamesinae, Monodiamesia
Orthocladiinae, Crictopus spp.
Heterotrissocladius changi
Parakiefferiella
Parametriocnemus
Tanytarsini, Tanytarsus spp.
Chironomini, Chironomus spp.
Chironomus anthracinus grp.
C. semireductus grp.
C. thummi
Cryptochironomus
Demicryptochironomus
Harnischia
Parachironomus
Paracladopelma
Dicrotendies
Microtendipes
Paratendipies
Polypedilum
Tribelos
Paralauterborniella
Stictochironomus
Pseudochironomus
P/B
REF.
2.2
4
3.7
5
5
5
a
e
4.5
4
2.8
5
1.5
12
3.2
4
4
6.4
4
3.6
4
4
4.7
4.7
3.9
6.7
4.7
5
5.7
4
6.4
6
6.9
6
4
e
e
b
m
f
i
b
d
i
e
c
h
c
L.E.
Dermott et al. 1977
Krueger and Waters 1983
Strayer and Likens 1986
c Edmondson and Winberg
f Lindegaard 1992
i Tudorancea et al. 1979
1969