Associations of Epiphytic Macroinvertebrates within
Four Assemblages of Submerged Aquatic Vegetation in a
Recovering Urban Lake
Lucas J. Kirby and Neil H. Ringler
Northeastern Naturalist, Volume 22, Issue 4 (2015): 672–689
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22001155 NORTHEASTERN NATURALIST 2V2(o4l). :2627,2 N–6o8. 94
Associations of Epiphytic Macroinvertebrates within
Four Assemblages of Submerged Aquatic Vegetation in a
Recovering Urban Lake
Lucas J. Kirby1,* and Neil H. Ringler2
Abstract - Onondaga Lake in Syracuse, NY, is recovering from a century of industrial and
municipal pollution. The distribution and diversity of aquatic macrophytes have increased
significantly in the past decade, and the plants currently cover 80% of the littoral area. To
assess the effects of aquatic vegetation on aquatic biota, we employed quantitative sampling
to examine associations of epiphytic macroinvertebrates in 4 assemblages of submerged
aquatic vegetation in Onondaga Lake in 2010 and 2011. Two assemblages were predominantly
monocultures—one of Stuckenia pectinata (Sago Pondweed) and the other of Chara
sp. (stonewort). The third was dominated by Potamogeton foliosus (Leafy Pondweed) and
Potamogeton pusillus (Small Pondweed), and the fourth was a heterogeneous community
that included Ceratophyllum demersum (Coon’s Tail), Myriophyllum spicatum (Eurasian
Watermilfoil), and Elodea canadensis (Canadian Waterweed). Measures of invertebrate
community composition—which included taxa richness, ETO richness, family richness,
and NCO richness—were not consistently different in any particular macrophyte assemblage.
Overall densities of epiphytic macroinvertebrates were similar to or higher than those
reported in other quantitative studies of epiphytic macroinvertebrates. We found differences
in the abundance of specific macroinvertebrate taxa associated with a particular macrophyte
assemblage. Stonewort and the heterogeneous beds supported a similar community
of gastropods and amphipods in both years, which was distinct from the high densities of
Oligochaeta and Chironomidae associated with Sago Pondweed. Our observations suggest
that the current distribution of aquatic macrophytes and the high density of associated macroinvertebrates
provide abundant prey for sizable populations of fishes and waterfowl that
prey on macroinvertebrates.
Introduction
Aquatic macroinvertebrates are an important, but often over looked component
of the littoral-zone community. Most management of lakes and ponds is focused on
either weed control or fish production, with little consideration given to the importance
of aquatic macrophytes and epiphytic macroinvertebrates. The heterogeneity
of aquatic macrophytes provides physical structure and refuge for epiphytic algae,
macroinvertebrates, and fishes (Diehl and Kornijow 1998, Perrow et al. 1999).
Habitats with higher levels of spatial heterogeneity are more complex, which
increases the potential diversity of associated organisms (MacArthur and MacArthur
1961). Dense aquatic macrophytes have been shown to provide protection
1State University of New York College of Environmental Science and Forestry, 127 Illick
Hall, 1 Forestry Drive, Syracuse, NY 13210. 2State University of New York College of Environmental
Science and Forestry, 200 Bray Hall, 1 Forestry Drive, Syracuse, NY 13210.
*Corresponding author - lkirby@syr.edu.
Manuscript Editor: Hunter Carrick
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for macroinvertebrates from fishes and large invertebrate predators (Baker 1918,
Crowder and Cooper 1982, Diehl 1992), and the secondary production of macroinvertebrates
within the macrophytes is important for littoral fish (Osenberg et al.
1992) and dabbling duck foraging, growth, and survival (Krull 1970).
Traditionally, the value of an aquatic macrophyte species for production of epiphytic
macroinvertebrates has been determined by the density and complexity of the
macrophytes (Crowder and Cooper 1982, Dibble et al. 2006, Lillie and Bud 1992).
However, there is conflicting evidence as to which species or types of macrophytes
support the highest macroinvertebrate density or diversity. Submerged macrophytes
with finely divided leaves have greater spatial complexity and surface area, and
have been shown to support greater diversity and abundance of macroinvertebrates
than broad-leaved, floating-leaved, or emergent macrophyte species (Dibble et al.
1997, Lillie and Budd 1992, Peets et al. 1994, Rosine 1955, Schramm et al. 1987,
Watkins et al. 1983). In contrast, Brown et al. (1988) and Voigts (1976) found that
the variability of macrophyte growth forms (floating/emergent/submerged) within a
macrophyte bed had more effect on macroinvertebrate richness and abundance than
the level of leaf complexity of individual species.
Other research has indicated that the value of particular macrophyte species
for macroinvertebrate production depends on the complexity of the aquatic plants
at multiple scales (Dibble et al. 2006). The growth habit of macrophytes over the
course of the growing season may also be important (Lillie and Budd 1992). For
example, Myriophyllum spicatum L. (Eurasian Watermilfoil) is a macrophyte with
finely divided leaves, but low complexity (Cheruvelil et al. 2001, 2002; Dibble et
al 1997). The structure of Eurasian Watermilfoil shifts from even distribution of
stems and leaves in late spring to the majority of the biomass occurring at the water’s
surface by late summer (Cheruvelil et al. 2001, Lillie and Budd 1992). Low
complexity and shifting distribution would likely decrease the capacity to support
macroinvertebrates as the season progresses, when compared to diverse native plant
populations (Theel et al. 2008).
The objectives of this study were to investigate the distribution and abundance of
epiphytic macroinvertebrate communities associated within 4 distinct assemblages
of fine-leaved species of submerged aquatic macrophytes common in the eastern
US. This study investigated the epiphytic macroinvertebrate community within
2 monocultures of Stuckenia pectinata (L.) Börner (Sago Pondweed) and Chara
sp. (stonewort), an assemblage dominated by Potamogeton foliosus Raf. (Leafy
Pondweed) and Potamogeton pusillus L. (Small Pondweed), which we will refer to
as mixed pondweeds, and within a heterogeneous community that included Ceratophyllum
demersum L. (Coon’s Tail), Eurasian Watermilfoil, Elodea canadensis
Michx. (Canada Waterweed), and to a lesser extent, Najas sp. (waternymph) and
Potamogetn crispus L. (Curly Pondweed). Even though the species that comprise
the 4 aquatic macrophyte communities are all fine-leaved, we hypothesized that
there would be significant differences among the macroinvertebrate communities
because of differences in growth forms and plant densities. We hypothesized
that the heterogeneous aquatic macrophyte assemblage would support the highest
richness and abundance of macroinvertebrates because of its increased habitat
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complexity and that Sago Pondweed would support low taxa richness because of
low leaf-complexity.
Methods
Study site
Onondaga Lake is a 1200-ha urban lake north of the city of Syracuse, NY,
which was used for the discharge of municipal and industrial waste for more than a
century (Effler 1996). The discharge of industrial waste containing Cl-, Na+, Ca2+,
Hg, and PCBs, coupled with nutrient-loading from a sewage-treatment plant had a
lasting impact on habitat structure and the aquatic community (Auer et al. 1996).
The once-mesotrophic lake became hypereutrophic, with low water-clarity, high
salinity, and elevated precipitation rates of CaCO3 (Effler 1996). The combination
of low water-clarity and high-salinity levels led to low biodiversity and minimal
coverage by aquatic macrophytes (Auer et al. 1996, Madsen et al. 1996). With the
closure of the soda-ash facility in 1986, and upgrades to the Syracuse metropolitan
sewage-treatment plant in 1999, 2004, and 2006, Onondaga Lake has undergone a
transition from hypereutrophic to mesotrophic (Effler and O’Donnell 2010). Aquatic
macrophytes have increased in richness from 5 species in 1991 (Madsen et al.
1996) to 23 species in 2010 (EcoLogic et al. 2012) and littoral-zone coverage has
increased from 13% (Madsen et al. 1996) to 80% (Kirby 2009, 2013). Onondaga
Lake is currently dominated by the 4 above-mentioned aquatic plant assemblages,
with the most prevalent being a heterogeneous assemblage.
Aquatic macrophyte sampling
We conducted aquatic macrophyte-community sampling in the littoral zone of
Onondaga Lake in July of 2008, 2009, 2011, and 2012 and in June of 2010 using the
point-intercept method (Madsen 1999). We sampled aquatic macrophytes at water
depths of 0–4 m using a grid of points that were spaced every 800 m, for a total of
319 points. We imported the coordinates for the aquatic macrophyte points into a
Fisher Mark II GPS with a point accuracy of 1–3 m. We followed the method of
Madsen (1999) that allows for the collection of aquatic macrophytes to determine
species presence or absence. During each sampling event, we maneuvered the boat
over each point, attached a rope to the head of a steel thatching rake, tossed the rake
head into the water, allowed it to settle on the lake bottom, dragged it back to the
boat and collected the vegetation from the tines.
Quantitative aquatic macroinvertebrate sampling
We collected samples of aquatic macrophytes and associated aquatic macroinvertebrates
on 30 July 2010, 2 and 5 August 2010, and 27 and 31 July 2011. In
2010, we used a stratified, systematic sampling design. We identified 4 sites in the
north basin of Onondaga Lake that had large beds of the target aquatic macrophyte
assemblages (Fig. 1). High levels of pollution still occurred in the southern basin
(Parsons Inc. et al. 2010); thus, we avoided that area. At each site, we sampled 2
sets (rows) of samples separated by 100 m and collected 8 samples (10 m apart)
per set. In 2011, we sampled 1 row of 8 samples (10 m apart) in 8 macrophyte beds
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(Fig. 1). We sampled 2 separate beds of each assemblage to ensure that the macroinvertebrate
communities were associated with that plant type and not the particular
area of the lake.
We designed and built a modified Gerking sampler for the quantitative sampling
of shallow (less than 1 m) aquatic macrophytes and their associated macroinvertebrate
communities (Gerking 1957, Kirby 2013). We chose this method because it
sampled a large area of aquatic macrophytes with minimal disturbance, which
minimized escape by active aquatic macroinvertebrates. We deployed the sampler
open in water depths of ~75 cm and slowly lowered it over the aquatic macrophytes.
Once in place, we used pruning shears to cut the stem bases of the enclosed aquatic
macrophytes. We then pushed the screen closed and lifted the sampler from the
water, allowing the water to fall through the screen and retaining the macrophytes
and macroinvertebrates within the sampler. Once on the boat, we pushed the screen
open, removed the sample from the screen, and preserved it in 10% buffered formalin
in a whirl-pack bag labeled with site and date information.
Figure 1. Sampling sites in Onondaga Lake, Syracuse, NY, in 2010 and 2011. P. spp represents
the mixed pondweed sites.
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In the lab, we spread the sample of aquatic vegetation across a shallow tray
with a labeled grid of 10 cells. We randomly drew a number to identify the cell
that would comprise the subsample and removed a volume of up to 100 ml of plant
material from that cell. New cells were selected until 100 ml of plant material was
attained from that sample. We separated the remainder of the sample by species,
dried each in an oven at 50 °C for a minimum of 24 h to a constant weight, and
weighed them to the nearest milligram with a Mettler BB240 top-loading scale.
While viewing the macrophyte subsamples under a dissecting microscope, we
separated all aquatic macroinvertebrates and placed them into a labeled vial with
70% ethanol. To subsample the Chironomidae larvae, we poured the larvae into a
petri dish, lightly mixed the sample with forceps, and randomly chose 50 larvae for
removal. We mounted and cleared them on slides with CMC-10. We identified Chironomidae
and the other aquatic macroinvertebrates to the lowest taxonomic level
achievable (Jokinen 1992, Merritt et al. 2008, Peckarsky 1990). We then separated
by species, dried in an oven at 50 °C, and weighed to the nearest milligram the
aquatic macrophyte subsample from which we removed the macroinvertebrates.
Data analysis
In 2010, 1 sample in the stonewort bed had an aquatic macrophyte assemblage that
was dominated by species that were characteristic of the heterogeneous community
(waternymph, Canada Waterweed, and Cladophora sp. (filamentous green algae),
and 2 samples within the mixed pondweed bed had a larger percentage of Sago Pondweed
than Leafy Pondweed or Small Pondweed. Our analysis was based on plant type
and not site; thus, we grouped these samples based on macrophyte composition for
community metrics, principal-component analysis, and analysis of variance.
Prior to statistical analysis, we log(x+1)-transformed all data to normalize variance.
We used SAS software® to perform 1-way analysis of variance (ANOVA)
with post hoc Waller-Duncan pairwise means testing—with significance set at α
= 0.05—to detect significant differences in macroinvertebrate-community metrics
among the 4 aquatic macrophyte assemblages. Macroinvertebrate-community metrics
included: taxa richness, family richness, richness of Ephemeroptera, Trichoptera,
and Odonata (ETO) taxa, non-Chironomidae and Oligochaeta richness (NCO),
subsample abundance, and estimated abundance of macroinvertebrates using the
following equations:
abundance per m2 = (S/s)*M*5.17 Equation 1,
where: s = dry weight of 100-ml aquatic macrophyte subsample, S = dry weight
of complete aquatic macrophyte sample, M = abundance of macroinvertebrates in
100-ml subsample, and 5.17 = 1 m2/ the area of the sampler;
and
abundance per kg plant material = (S/s)*M*(kg/S) Equation 2,
where: s = dry weight of 100-ml aquatic macrophyte subsample, S = dry weight
of complete aquatic macrophyte sample, M = abundance of macroinvertebrates in
100-ml subsample, and Kg = 1 kilogram.
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Using SAS software, we conducted principal-component analysis (PCA) to
identify taxa that would be further tested with ANOVA for significance among plant
types. We excluded rare taxa from PCA if they were found in less than 10% of the
subsamples and if they represented less than 2% of the total number of organisms
counted. We analyzed 15 taxa in 2010 (n = 62) and 17 in 2011 (n = 64) (Table 1).
Taxa that had significant Pearson correlations (α = 0.01) with principle components
1 or 2 (Scree test) were further tested with one-way ANOVA with post hoc Waller-
Duncan pairwise means testing for significant differences in abundance among the
4 aquatic macrophyte assemblages.
Results
Aquatic macrophyte distribution (2008–2012) and community composition
The richness of aquatic macrophyte species increased from 10 species in 2008
to 16 species in 2012, but the distribution of aquatic macrophytes remained at
80% of littoral-zone points from 2009–2012 (Table 2). The most prevalent aquatic
macrophytes in Onondaga Lake were associated with what is termed here as the
heterogeneous macrophyte assemblage. Sago Pondweed maintained a fairly consistent
distribution from 2008–2012, and on average was located at 15% of the
sampling points. Some species increased in frequency each year; e.g., the distribution
of Heteranthera dubia (Jacq.) MacMill. (Grassleaf Mudplantain) increased
from occurring at less than 3% of points in 2008 to >40% in 2012, stonewort increased from
less than 1% in 2009 to 10% in 2012, and the invasive species Nitellopsis obtusa (Desvaux
in Louseleur) J. Groves (Starry Stonewort) increased from 0 in 2010 to 4% in 2012.
The aquatic macrophyte communities sampled in 2010 (Fig. 2) and 2011 (Fig. 3)
Table 1. Macroinvertebrate taxa that were included in principal component analysis (PCA) of epiphytic-
macroinvertebrate communities among 4 aquatic macrophyte communities in Onondaga Lake, NY,
in 2010 (n = 62) and 2011 (n = 64). * Indicates taxa that were significantly correlated (α = 0.01) with
PC 1 or 2 and subsequently examined with analysis of variance.
2010 2011
Amphipoda* Amphipoda*
Chironomidae* Ceratopogonidae*
Coenagrionidae* Chironomidae*
Dreissenidae Coenagrionidae*
Hirudinea* Culicidae
Hydrobiidae* Dreissenidae*
Hydrachnidae Hirudinea
Hydroptilidae* Hydrobiidae*
Leptoceridae* Hydrachnidae*
Oligochaeta* Hydroptilidae*
Physidae* Leptoceridae*
Planorbidae* Oligochaeta*
Tricladida Physidae*
Pyralidae* Planorbidae*
Valvatidae* Tricladida
Pyralidae*
Valvatidae*
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Table 2. Percent presence of aquatic macrophyte species in Onondaga Lake, NY, in July (2008, 2009,
2011, and 2012) and June (2010) in the littoral zone (less than 4 m water depth).
Species 2008 2009 2010 2011 2012 Average
Coon’s Tail 23.2 34.2 24.8 39.8 57.1 35.8
Stonewort 0.0 0.3 6.0 4.4 10.0 4.1
Canada Waterweed 42.0 53.3 53.3 37.3 42.0 45.6
Fontinalis sp. (an aquatic moss) 0.0 0.0 0.0 0.3 0.9 0.3
Grassleaf Mudplantain 2.5 5.0 12.2 22.3 43.3 17.1
Lemna sp. (duckweed) 1.3 2.5 0.3 0.3 0.3 0.9
Eurasian Watermilfoil 33.5 45.5 50.8 43.6 41.7 43.0
Waternymph 16.6 9.1 8.5 16.3 32.0 16.5
Starry Stonewort 0.0 0.0 0.0 3.1 4.1 1.4
Polygonum amphibium L. 0.0 0.0 0.0 0.0 0.3 0.1
(Water Knotweed)
Curly Pondweed 16.9 29.8 55.5 26.6 13.8 28.5
Mixed pondweeds 36.4 38.9 29.2 36.7 8.5 29.9
Ranunculus longirostris Godr. 0.0 0.0 0.0 0.0 1.3 0.3
(Longbeak Buttercup)
Spirodela polyrhiza (L.) Schleid. 0.0 0.9 0.0 0.0 0.0 0.2
(Common Duckmeat)
Sago Pondweed 9.4 20.1 11.6 16.0 17.9 15.0
Vallisneria americana Michx. 0.3 0.0 0.0 0.6 1.3 0.4
(American Eelgrass)
Littoral zone coverage 69.9 82.8 79.6 80.3 81.2 78.7
Figure 2. Percentage of individual species within the sampled aquatic macrophyte assemblages
based on dry-weight biomass, in Onondaga Lake, NY, in July of 2010.
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were representative of the 4 communities that were observed in Onondaga Lake
prior to sampling.
Analysis of biotic metrics among macrophyte communities
We identified a total of 47 epiphytic macroinvertebrate taxa in Onondaga Lake
in 2010 and 63 in 2011. In 2010, the 4 aquatic macrophyte communities had significantly
different levels of taxa richness (ANOVA, P = 0.001), ETO richness
(ANOVA, P = < 0.001), NCO richness (ANOVA, P = 0.013), estimated abundance
of organisms m-2 (ANOVA, P = < 0.001), and estimated abundance of organisms
per kg plant matter (ANOVA, P = < 0.001) (Table 3). Post hoc Waller Duncan
means testing indicated that the stonewort bed had significantly higher average
taxa richness than the other communities of aquatic macrophytes (Table 3). The
mixed pondweed bed had significantly higher richness of ETO taxa than the Sago
Pondweed and heterogeneous macrophyte beds (Table 3). The heterogeneous and
Sago Pondweed beds had significantly higher abundance of organisms m‑2 than the
stonewort and mixed pondweed beds (Table 3).
In 2011, with the exception of ETO richness (ANOVA, P = 0.191), significant
differences occurred among all of the biotic metrics (Table 3). Taxa richness
(ANOVA, P = 0.035) was significantly higher in the heterogeneous macrophyte
assemblage than the stonewort bed. The heterogeneous community and mixed
pondweed bed supported a significantly higher number of families (ANOVA, P =
0.042) than stonewort bed (Table 3). Subsample abundance (ANOVA, P = < 0.001),
estimated abundance m‑2 (ANOVA, P = < 0.003), and estimated abundance per kg
Figure 3. Percentage of individual species within the sampled aquatic macrophyte assemblages
based on dry-weight biomass, in Onondaga Lake, NY, in July of 2011.
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of dried plant material (ANOVA, P = < 0.001) was highest in the mixed pondweed
and Sago Pondweed beds (Tables 3, 4).
Table 3. Analysis of variance of macroinvertebrate community metrics within 4 communities of
aquatic macrophytes in Onondaga Lake, NY, in 2010 and 2011. Mean and ± SE are shown as well as
post hoc Waller-Duncan groups. Mean values within a row followed by different letters are significantly
different.
Heterogeneous Mixed
Stonewort grouping pondweeds Sago Pondweed
Mean (SE) Mean (SE) Mean (SE) Mean (SE) P-value
2010
Taxa richness 21.7 (0.6) A 17.9 (0.9) B 18.1 (0.6) B 17.2 (0.7) B 0.001
Family richness 12.6 (0.4) A 12.2 (0.5) A 12.2 (0.5) A 11.4 (0.5) A 0.270
ETO 3.8 (0.4) AB 1.8 (0.4) C 4.6 (0.2) A 3.1 (0.4) B less than 0.001
NCO 13.6 (0.6) A 11.8 (0.5) AB 13.4 (0.5) A 11.3 (0.7) B 0.013
Subsample abund. 417.0 (63.6) A 411.6 (69.8) A 542.9 (86.9 A 452.3 (37.1) A 0.278
Est. abundance
m-2 6051.8 17,079.5 3876.4 15,862.0 less than 0.001
(1201.2) B (2273.2) A (780.6) B (1798.6) A
per kg plant 62,568.4 70,393.5 C 184,052.5 86,912.2 less than 0.001
(11,416.3) C (8926.4) B (36,424.6) A (8701.3) B
2011
Taxa richness 12.4 (0.9) B 17.1 (1.0) A 14.8 (1.0) AB 14.4 (1.3) AB 0.035
Family richness 9.8 (0.5) B 12.9 (0.5) A 11.8 (0.5) A 10.3 (1.0) B 0.042
ETO 1.6 (0.3) A 2.6 (0.4) A 1.9 (0.4) A 2.2 (0.3) A 0.191
NCO 9.5 (0.6) AB 12.1 (0.8) A 10.9 (0.5) A 8.8 (1.1) B 0.009
Subsample abund. 103.5 (11.8) C 152.2 (19.5) BC 225.8 (20.6) A 199.2 (34.2) AB less than 0.001
Est. abundance
m-2 4634.7 6493.8 7431.0 11,534.6 0.003
(880.2) C (1174.2) BC (870.8) AB (1885.3) A
per kg plant 20,213.3 45,874.8 78,150.8 63,798.9 less than 0.001
(2934.6) C (7744.4) B (8074.8) A (12,146.1) B
Table 4. Total density (m-2 and per kg dried plant) of epiphytic macroinvertebrates in Onondaga Lake,
NY, compared to similar studies.
Source Site Density
Current study Onondaga Lake, NY, 2010 3876–17,080/m2
Current study Onondaga Lake, NY, 2011 4645–11,635/m2
Brown et al. 1998 Lake St. Clair, MI less than 5000/m2
Watkins et al. 1983 Orange Lake, FL less than 5000/m2
Thorp et al. 1997 Potomac River, MD 27,960/m2
Peets et al. 1994 Lake Seminole, GA 12,855 /m2
Schramm et al. 1987 Orange and Henderson Lakes, FL 12,257–17,596/m2
Van den Berg et al. 1997 Lake Veluwerneer, The Netherlands 6000/m2
Van den Berg et al. 1997 Lake Worlderwijd, The Netherlands 15000/m2
Current study Onondaga Lake, NY, 2010 62,568–184,052/kg
Current study Onondaga Lake, NY, 2011 20,213–78,151/kg
Andrews and Haster 1943 Lake Mendota, WI 20,000–52,000/kg
Krull 1970 Montezum, NY 3060–20,590/kg
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Analysis of macroinvertebrate communities among macrophyte communities
In 2010, 47% of the variance was explained by the first 2 PCA axes. We identified
2 groupings: the stonewort (C) and the heterogeneous (H) sites formed
groups that overlapped and Sago Pondweed (S) and mixed pondweeds (F) clustered
together (Fig. 4). Principal component (PC) 1 (31.5% of variance) separated
the stonewort and the heterogeneous sites from the mixed pondweed and Sago
Pondweed sites (Fig. 4). Physidae, Valvatidae, Tricladida, Planorbidae, Hydrobiidae,
and Amphipoda had positive loadings (>0.25) with PC 1 and the stonewort
and the heterogeneous community. Chironomidae and Pyralidae had negative
loadings (less than -0.25) with PC1, and were more representative of the macroinvertebrate
community associated with mixed pondweeds and Sago Pondweed.
PC 2 (15% of variance) separated the stonewort from the heterogeneous sites
(Fig. 4). Leptoceridae, Hydroptilidae, Oligochaeta, and Chironomidae had positive
loadings (>0.25) with PC 2; greater abundances were associated with stonewort
and mixed pondweeds.
Thirteen of the 15 macroinvertebrate taxa used in PCA from 2010 had significant
Pearson correlations (α = 0.01) with PC 1 or 2, and we individually tested
them for significant differences among plant communities. Hirudinea, Valvatidae
, and Leptoceridae were significantly more abundant (ANOVA, P < 0.001) in the
stonewort sites than the other 3 plant assemblages. The heterogeneous assemblages
Figure 4. Principal component analysis of epiphytic macroinvertebrate communities associated
with aquatic macrophytes (S = Sago Pondweed, F = mixed pondweeds, C = Stonewort,
and H = heterogeneous community) in Onondaga Lake, NY, in 2010.
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and stonewort supported significantly higher abundance (ANOVA, P ≤ 0.001) of
Physidae, Tricladida, and Amphipoda (Table 5). Sago Pondweed and mixed pondweeds
had a significantly higher abundance of Oligochaeta (ANOVA, P = 0.005)
and Chironomidae (ANOVA, P = < 0.001) (Table 5).
In 2011, 43% of the variance was explained in the first 2 PC axes. The
stonewort and Sago Pondweed formed relatively distinct clusters, while mixed
pondweeds and the heterogeneous macrophyte assemblages were mostly
grouped together (Fig. 5). Sago Pondweed was associated with negative
scores along PC 1 (24% of the variance); Chironomidae and Oligochaeta had
negative loadings of less than -0.25. Dreissena sp., Planorbidae, Hydrobiidae,
Valvatidae, and Amphipoda all had positive loadings (>0.25) with PC 1 and
were associated with mixed pondweeds, stonewort, and the heterogeneous
community. PC 2 (19% of the variance) separated the stonewort sites from
the mixed pondweed and heterogeneous sites (Fig. 5). Coenagrionidae, Hydroptilidae,
Hydrachnidae, Physidae, Pyralidae, Planorbidae, Oligochaeta, and
Planorbidae had positive loadings (>0.25) with PC 2 and had higher abundance
in mixed pondweed and heterogeneous sites (Fig. 5).
Fourteen of the 17 taxa used in PC analysis from 2011 had significant Pearson
correlations (α = 0.01) with PC 1 or 2, and we individually tested for significant
differences among plant communities (Table 6). Dreissenidae (ANOVA, P = 0.003)
and Planorbidae (ANOVA, P = less than 0.001) were significantly highest in the stonewort
beds (Table 6). Physidae (ANOVA, P = less than 0.001) and Pyralidae (ANOVA,
P = < 0.001) were significantly highest in mixed pondweeds, while Oligochaeta
(ANOVA, P = < 0.001) and Chironomidae (ANOVA, P = < 0.001) were highest in
Sago Pondweed (Table 6).
Table 5. Analysis of variance of macroinvertebrate taxa that were found to have significant correlations
with PCA axes in Onondaga Lake, NY, in 2010. Mean values within a row followed by different
letters are significantly different.
Heterogeneous Mixed
Macroinvertebrate Stonewort grouping pondweeds Sago Pondweed
taxon Mean (SE) Mean (SE) Mean (SE) Mean (SE) P- value
Amphipoda 119.7 (36.9) A 72.9 (16.7) A 9.7 (3.2) B 13.6 (10.7) B less than 0.001
Chironomidae 71.9 (11.6) B 97.5 (27.6) B 302.6 (56.6) A 209.6 (30.1) A less than 0.001
Coenagrionidae 2.5 (0.6) B 1.2 (0.5) C 2.0 (0.5) BC 4.2 (0.6) A 0.006
Hirudinea 3.7 (1.0) A 1.4 (0.4) B 0.7 (0.5) BC 0.4 (0.2) C less than 0.001
Hydrobiidae 21.8 (3.2) A 27.4 (5.5) AB 13.8 (3.9) B 3.7 (1.9) C less than 0.001
Hydroptilidae 3.9 (0.8) B 1.1 (0.4) C 25.1 (7.9) A 5.8 (3.6) BC less than 0.001
Leptoceridae 3.6 (0.7) A 1.6 (0.5) BC 4.0 (1.6) AB 1.3 (0.4) C 0.016
Oligochaeta 32.1 (6.0) B 30.5 (9.2) B 71.8 (17.5) A 88.3 (13.2) A 0.005
Physidae 5.0 (1.2) A 8.8 (1.8) A 0.9 (0.6) B 2.3 (1.0) B less than 0.001
Planorbidae 5.9 (1.2) B 26.8 (4.0) A 6.3 (1.6) B 3.3 (0.7) B less than 0.001
Pyralidae 0.6 (0.3) D 2.2 (0.7) C 6.1 (1.6) B 11.9 (1.9) A less than 0.001
Tricladida 23.6 (7.9) A 10.3 (3.0) A 4.0 (1.8) B 2.9 (1.5) B 0.001
Valvatidae 19.7 (5.8) A 8.0 (2.1) B 4.9 (2.4) B 1.1 (0.4) C less than 0.001
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Table 6. Analysis of variance of macroinvertebrate taxa that were found to have significant correlations
with PCA axes in Onondaga Lake, NY, in 2011.
Heterogeneous Mixed
Macroinvertebrate Stonewort grouping pondweeds Sago Pondweed
taxon Mean (SE) Mean (SE) Mean (SE) Mean (SE) P- value
Amphipoda 18.4 (3.9) A 25.8 (5.1) A 25.9 (9.2) A 1.6 (0.5) B less than 0.001
Ceratopogonidae 0.0 (0.0) A 0.3 (0.2) A 0.0 (0.0) A 0.6 (0.4) A 0.116
Chironomidae 7.1 (2.3) B 9.7 (2.1) B 10.2 (2.6) B 110.6 (30.5) A less than 0.001
Coenagrionidae 0.3 (0.2) C 1.4 (1.0) B 0.9 (0.6) BC 2.8 (0.7) A less than 0.001
Dreissenidae 14.9 (3.7) A 9.4 (3.2) B 5.7 (3.0) B 4.4 (1.9) B 0.003
Hydrachnidae 0.3 (0.2) C 3.6 (2.1) BC 10.8 (3.7) A 4.1 (1.4) AB 0.001
Hydrobiidae 19.0 (4.6) B 16.4 (4.1) B 45.9 (7.6) A 4.7 (1.6) C less than 0.001
Hydroptilidae 1.6 (1.0) A 3.5 (1.0) A 1.9 (0.6) A 4.1 (0.7) A 0.130
Leptoceridae 1.8 (0.5) A 1.4 (0.4) A 1.0 (0.5) A 0.6 (0.3) A 0.067
Oligochaeta 2.4 (0.7) C 11.9 (1.7) B 11.1 (3.1) B 30.8 (7.0) A less than 0.001
Physidae 1.1 (0.4) C 4.1 (0.6) B 11.7 (2.7) A 2.3 (0.5) C less than 0.001
Planorbidae 14.3 (2.3) A 26.5 (7.7) B 74.6 (10.5) B 8.1 (2.4) C less than 0.001
Pyralidae 0.1 (0.8) D 2.3 (0.5) C 10.7 (1.6) A 7.0 (1.9) B less than 0.001
Valvatidae 13.4 (2.7) A 12.7 (3.1) A 13.5 (4.1) A 5.4 (2.7) B less than 0.001
Figure 5. Principal component analysis of epiphytic macroinvertebrate communities associated
with aquatic macrophytes macrophytes (S = Sago Pondweed, F = mixed pondweeds, C
= Stonewort, and H = heterogeneous community) in Onondaga Lake, NY, in 2011.
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Discussion
Epiphytic macroinvertebrate community
We hypothesized that increased heterogeneity within the heterogeneous macrophyte
bed would lead to higher macroinvertebrate richness—a result reported
in other studies (Andrews and Hasler 1943, Brown et al. 1988, Krecker 1939,
Mormule et al. 2011, Rosine 1955). The results of this study did not support our
hypothesis, but were similar to those of Theel et al. (2008) and Van den Berg et al.
(1997) in that the richness of macroinvertebrates was not significantly different
among macrophyte assemblages. We found that no particular plant community supported
higher richness of macroinvertebrate taxa, families, NCO taxa, or ETO taxa
in both years. Our findings were likely caused by the fact that although different
species were dominant in each assemblage, all 4 aquatic macrophyte assemblages
were dominated by macrophytes with similar morphology (i.e., small leaves). The
macrophyte assemblages in Onondaga Lake, including the heterogeneous bed, lack
variability in growth forms (emergent/floating) that have been found to increase
macroinvertebrate richness (Brown et al. 1988, Voigts 1976). Assemblages of
small-leaved macrophytes have less niche diversity than those with more variability
in macrophyte structure, and therefore may support less richness of specialized
taxa. Another factor that likely contributed to the low richness of macroinvertebrates
we observed is that the community does not appear to have fully recovered
from the extensive pollution to which the area was exposed for much of the past
century (Kirby 2013). Using the same sampling techniques, Kirby (2013) found that
adjacent unpolluted aquatic systems (Otisco Lake, Seneca River/Onondaga Outlet,
and Oneida Lake) had higher taxa richness per subsample than we found in Onondaga
Lake subsamples in 2011. A larger number of pollution-intolerant taxa were also
documented in these systems than we recorded in Onondaga Lake (Kirby 2013).
Even though there was no apparent relationship between macroinvertebrate
richness and macrophyte assemblage, we detected differences in the abundance
of particular macroinvertebrates within the different macrophyte assemblages.
PCA analysis explained a low proportion of variability, but provided a visual representation
of sites with similar macroinvertebrate assemblages that we verified
with ANOVA. The most distinct macroinvertebrate community was associated
with Sago Pondweed, which supported the lowest richness of NCO taxa in both
years. The assemblage was characterized by low abundance of Gastropoda and
Amphipoda and a significantly higher abundance of Chironomidae (mainly Tanytarsini
Paratanytarsus sp. and Orthocladiinae Cricotopus sylvestris [Fabricious]),
Oligochaeta, and Coenagrionidae in both years. The value of Sago Pondweed to
macroinvertebrates is debatable; Berg (1949) suggested that Sago Pondweed has
limited value because its leaves are too small to support leaf miners or case-making
Trichoptera. Krecker (1939) found that Sago Pondweed supported a high number
of macroinvertebrates that were likely using the plant for cover, and Dibble et al.
(1997) indicated that the plant has high structural complexity. Sago Pondweed in
Onondaga Lake was associated with silt/fine sand sediment substrates (L. Kirby,
pers. observ.), a finding reported from other lakes (Case and Madsen 2004), and in
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L.J. Kirby and N.H. Ringler
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both years there was a large amount of silt/sand sediment on the plant leaves. It is
possible that the sediment that we observed on Sago Pondweed contributed to the
associated macroinvertebrate community. The 2 most abundant Chironomidae in
the Sago Pondweed bed were Paratanytarsus sp. and Cricotopus sylvestris, which
are tube-dwelling grazers that construct ridged tubes of sediment and silk—used
primarily as retreats from predation—along stems and branches of aquatic macrophytes
(Hershey 1987). We observed many Chironomidae using sand retreats when
we examined our Sago Pondweed samples. The high abundance of Coenagrionidae
within Sago Pondweed beds can be attributed to the large abundance of small prey
(Chironomidae and Oligochaeta) associated with this macrophyte type. Coenagrionidae
and other Zygoptera feed predominantly on Chironomidae larvae (Hershey
1987, Lawton 1971). Lawton (1971) found that Oligochaeta were also heavily
preyed on by an early instar Zygoptera Pyrrhosoma nymphula (Sulzer). The low
abundance of gastropods and amphipods we detected in Sago Pondweed samples
indicates that this macrophyte community does not support strong development of
periphyton in Onondaga Lake.
In 2010, the mixed pondweed sites supported the same abundance of Chironomidae
and Oligochaeta as the Sago Pondweed beds. In that year, the mixed
pondweed sites were located in an area dominated by silt/sand substrate (L. Kirby,
pers. observ.); Sago Pondweed was found intermixed with half of the mixed pondweed
samples, and the samples had sediment on the leaves. In 2011, the mixed
pondweed at the initial site senesced and decayed before sampling, so we sampled
2 other sites where mixed pondweed was the dominant assemblage. The substrate
at these new sites was an even mix of sand and gravel substrate, with no sedimentation
noted on the plant leaves; also Sago Pondweed was not intermixed. In 2011,
the mixed pondweed beds supported significantly higher abundance of Gastropoda
(Hydrobiidae and Physidae) and Pyralidae than the other macrophyte communities
and had significantly less Chironomidae and Oligochaeta than were found in the
Sago Pondweed beds (Table 4). It is likely that the change in macroinvertebrate
communities was not caused entirely by site differences, because in both 2010 and
2011 the mixed pondweed sites were located in areas with moderately high-wave
energy (Kirby 2009, Parsons Inc. et al. 2010). The presence of Sago Pondweed and
possibly sediment on the leaves in the mixed pondweed samples from 2010 may
have contributed to the large number of tube-dwelling Chironomidae and Oligochaeta.
We did not investigate the possible relationship between sedimentation on
macrophytes and its influence on aquatic macroinvertebrate communities in our
study, but it should be examined in the future.
The macroinvertebrate communities associated with stonewort and the heterogeneous
macrophyte bed were similar and practically indistinguishable in both
years. They were characterized by high numbers of amphipods and gastropods
with low abundance of Chironomidae and Oligochaeta. This macroinvertebrate
community is comparable to those observed in other studies of similar macrophyte
communities, and along with Chironomidae, are often the most dominant taxa
associated with Coon’s Tail and Eurasian Watermilfoil (Andrews and Hasler 1943,
Brown et al. 1988) and stonewort (Van den Berg et al. 1997). The high abundance
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2015 Vol. 22, No. 4
of grazers within these aquatic macrophyte assemblages indicates a higher availability
of periphyton on the submerged vegetation. The relationship between
aquatic macrophytes, epiphytes/periphyton, and macroinvertebrate grazers is well
documented (Allen 1971, Cattaneo 1983, Cattaneo and Kalff 1980, Cattaneo and
Mousseau 1995, Jaschinski et al. 2011). The abundance of macroinvertebrate grazers
is determined by the development of epiphytic algae (Osenberg 1989, Van den
Berg et al. 1997), and aquatic plants have a positive response to the removal of attached
epiphytes (Underwood et al. 1992).
Epiphytic macroinvertebrate abundance
One of the primary benefits of using a modified Gerking sampler was the
ability to estimate densities of macroinvertebrates per area and plant biomass.
Sago Pondweed had the highest estimated abundance of macroinvertebrates m-2
of bottom area in both 2010 and 2011 (Table 3) mainly because these sites had
high biomass of aquatic vegetation in each sample. The abundance of macroinvertebrates
m-2 was similar to what has been found in other systems, while the
abundance of organisms per kg of dried plant biomass was higher (Table 4).
The estimated abundance of organisms per kg of dried plant-biomass is likely a
conservative estimate because a portion of the attached sediment remained on
the samples/subsamples when they were weighed. The high density of macroinvertebrates,
whether expressed as m-2 or per kg of dried plant biomass, suggests
that the macrophyte beds in Onondaga Lake provide a large amount of prey for
fish, ducks, and other wildlife. We predict that the heterogeneous macrophyte
assemblage (~40% of the littoral area), stonewort (~10% as of 2012), and mixed
pondweed (~30%) support high levels of fish production because of the high
abundance of macroinvertebrates and moderate macrophyte density which tends
to allow high levels of foraging by fish (Crowder and Cooper 1982, Gotceitas
1990). Kirby (2009), studying fish diets in Onondaga Lake, found that Lepomis
gibbosus (L.) (Pumpkinseed Sunfish) fed predominantly on Amphipoda, Lepidoptera,
and Gastropoda, and Lepomis macrochirus Raf. (Bluegill Sunfish) mainly
fed on amphipods. Lepomis sp. (sunfish) are currently a dominant littoral-zone
fish in Onondaga Lake; they are major components in the littoral food web and
are instrumental to the future of recreational fishing at the site.
We suggest that the epiphytic macroinvertebrate community associated with
Sago Pondweed has limited direct value for larger-adult fish because this plant
tended to grow at very high densities and the community is numerically dominated
by small macroinvertebrates (Chironomidae and Oligochaeta). However,
Sago Pondweed beds provide quality habitat and forage for young-of-the-year fish
and invertebrate predators, so these assemblages are important components of the
Onondaga Lake food web. Sago Pondweed also provides high-quality forage for
dabbling ducks (Martin and Ulher 1939, Wersal et al. 2005), and the high abundance
of attached macroinvertebrates would supply ducks with an excellent source
of additional protein (Krull 1970). At its current and apparently stable distribution
of approximately 15% of the littoral zone, the Sago Pondweed assemblage provides
a large area of quality forage for ducks and young fish.
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Acknowledgments
We thank Allison Muehe, Danielle Hurley, Jackie Sivalia, Mike Patton, Stephanie Johnson,
Nicholas Griffin, Nicholas Kirby, and Vincent Mangino for assistance with field research.
Literature Cited
Allen, H. 1971. Primary productivity, chemo-organotrophy, and nutritional interactions of
epiphytic algae and bacteria on macrophytes in the littoral of a lake. Ecological Monographs
41(2):98–127.
Andrews, J.D., and A.D. Hasler. 1943. Fluctuations in the animal populations of the littoral
zone in Lake Mendota. Transactions of the Wisconsin Academy of Sciences, Arts, and
Letters 35:175–185.
Auer, M.T., S.W. Effler, M.L. Storey, S.D. Conners, P. Sze, C.A. Siegfried, N.A. Auer,
J.D. Madsen, R.M. Smart, and L.W. Eichler. 1996. Biology. Pp. 384–534, In S.W. Effler
(Ed.). Limnological and Engineering Analysis of a Polluted Urban Lake. Springer-
Verlag, New York, NY. 831 pp.
Baker, F.C. 1918. The Productivity of Invertebrate Fish Food on the Bottom of Oneida
Lake, with Special Reference to Mollusks. Technical publication no. 9. The New York
State College of Forestry and Syracuse University, Syracuse, NY. 264 pp.
Berg, C.O. 1949. Limnological relations of insects to plants of the genus Potamogeton.
Transactions of American Microscopical Society 58(4):279–291.
Brown, C.L., T.P. Poe, J.R.P. French III, and D.W. Schloesser. 1988. Relationships of phytomacrofauna
to surface area in naturally occurring macrophyte stands. Journal of the
North American Benthological Society 7(2):129–139.
Case, M.L., and J.D. Madsen. 2004. Factors limiting the growth of Stuckenia pectinata
(Sago Pondweed) in Heron Lake, Minnesota. Journal of Freshwater Ecology
19(1):17–23.
Cattaneo, A. 1983. Grazing on epiphytes. Limnology and Oceanography 28(1) :124–132.
Cattaneo, A., and J. Kalff. 1980. The relative contribution of aquatic macrophytes and
their epiphytes to the production of macrophyte beds. Limnology Oceanographer
25(2):280–289.
Cattaneo, A., and B. Mousseau. 1995. Empirical analysis of the removal rate of periphyton
by grazers. Oecologia 103(2):249–254.
Cheruvelil, K.S., P.A. Soranno, and J.D. Madsen. 2001. Epiphytic macroinvertebrates
along a gradient of Eurasian Watermilfoil cover. Journal of Aquatic Plant Management
39:67–72.
Cheruvelil, K.S., P.A. Soranno, J.D. Madsen, and M.J. Roberson. 2002. Plant architecture
and epiphytic macroinvertebrate communities: The role of an exotic dissected macrophyte.
Journal of the North American Benthological Society 21(2):261–277.
Crowder, L.B., and W.E. Cooper. 1982. Habitat structural complexity and the interaction
between Bluegills and their prey. Ecology 63(6):1802–1813.
Dibble, E.D., K.J. Killgore, and G.O. Dick. 1997. Measurement of plant architecture in
seven aquatic plants. Aquatic Plant Control Research Program. US Army Corps of Engineers,
Vicksburg, MS.
Dibble, E.D., S.M. Thomaz, and A.A. Padial. 2006. Spatial complexity measured at a multiscale
in three aquatic plant species. Journal of Freshwater Eco logy 21(2):239–247.
Diehl, S. 1992. Fish predation and benthic-community structure: The role of omnivory and
habitat complexity. Ecology 73:1646–1661.
Northeastern Naturalist
688
L.J. Kirby and N.H. Ringler
2015 Vol. 22, No. 4
Diehl, S., and R. Kornijow. 1998. Influence of submerged macrophytes on trophic interactions
among fish and macroinvertebrates. Pp. 91–114, In E. Jeppesen, M. Sondergaard,
M. Sondergaard, and K. Christoffersen (Eds.). The Structuring Role of Submerged Macrophytes
in Lakes. Springer Verlag, New York, NY. 423 pp.
EcoLogic LLC, Anchor QEA LLC, L. Rudstam, Onondaga County Department of Water
Environment Protection, and W.W. Walker. 2012. Onondaga Lake Ambient Monitoring
Program 2010. Available online at http://static.ongov.net/WEP/wepdf/AMP_Annual-
Reports/2010/Document/AMP_Report_2010_FINAL.htm. Accesse1 July 2012.
Effler, S.W. (Ed.). 1996. Limnological and Engineering Analysis of a Polluted Urban Lake.
Springer-Verlag, New York, NY. 831 pp.
Effler, S.W., and S.M. O’Donnell. 2010. A long-term record of epilimnetic phosphorus patterns
in recovering Onondaga Lake, New York. Fundamentals of Applied Limnology
177(1):1–18.
Gerking, S.D. 1957. A method of sampling the littoral macrofauna and its application. Ecology
38(2):219–226.
Gotceitas, V. 1990. Variation in plant-stem density and its effects on foraging success of
juvenile Bluegill Sunfish. Environmental Biology of Fishes 27:67 –70.
Hershey, A.E. 1987. Tubes and foraging behavior in larval Chironomidae: Implications for
predator avoidance. Oecologia 73(2):236–241.
Jaschinski, S., D.C. Brepohl, and U. Sommer. 2011. The trophic importance of epiphytic
algae in a freshwater-macrophyte system (Potamogeton perfoliatus L.): Stable isotope
and fatty-acid analysis. Aquatic Sciences 73:91–101.
Jokinen, E.H. 1992. The Freshwater Snails (Mollusca: Gastropoda) of New York State. Bulletin
482. New York State Museum, Albany, NY. 112 pp.
Kirby, L.J. 2009. Nesting and recruitment of centrarchids and the oligotrophication of
Onondaga Lake, New York. M.Sc. Thesis. State University of New York College of
Environmental Science and Forestry, Syracuse, NY. 78 pp.
Kirby, L.J. 2013. Recolonization of macroinvertebrates in a recovering urban lake (Onondaga
Lake, Syracuse, NY): Analysis within communities of distinct aquatic macrophytes.
Ph.D. Dissertation. State University of New York College of Environmental Science and
Forestry, Syracuse, NY. 147 pp.
Krecker, F.H. 1939. A comparative study of the animal population of certain submerged
aquatic plants. Ecology 20(4):552–562.
Krull, J.N. 1970. Aquatic plant–macroinvertebrate associations and waterfowl. The Journal
of Wildlife Management 34(4):707–718.
Lawton, J.H. 1971. Maximum and actual field-feeding rates in larvae of the damselfly Pyrrhosoma
nymphula (Sulzer) (Odonata: Zygoptera). Freshwater Biology 1(1):99–11.
Lillie, R., and J. Budd. 1992. Habitat architecture of Myriophyllum spicatum L. as an index
to habitat quality for fish and macroinvertebrates. Journal of Freshwater Ecology
7(2):113–125.
MacArthur, R.H., and J.W. MacArthur. 1961. On bird-species diversity. Ecology 42(3):
594–598.
Madsen, J.D. 1999. Point-intercept and line-intercept methods for aquatic-plant management.
Aquatic Plant Control Technical Note MI-02. Army Corp of Engineers. Available
online at http://el.erdc.usace.army.mil/elpubs/pdf/apcmi-02.pdf. Accessed 12
Februrary 2008.
Madsen, J.D., J.A. Bloomfield, and J.W. Sutherland, L.W. Eichler, and C.W. Boylen. 1996.
The aquatic macrophyte community of Onondaga Lake: Field survey and plant-growth
bioassays of lake sediments. Lake and Reservoir Management 12(1 ):73–79.
Northeastern Naturalist Vol. 22, No. 4
L.J. Kirby and N.H. Ringler
2015
689
Martin, A., and M. Uhler. 1939. Food of game ducks in the United States and Canada. US
Department of Agriculture Technical Bulletin 934. Washington, DC. 308 pp.
Merritt, R.W., K.W. Cummins, and M.B. Berg. 2008. An Introduction to the Aquatic Insects
of North America. 4th Edition. Kendall/Hunt Publishing Company, Dubuque, IA.
1214 pp.
Mormul, R.P., S.M. Thomaz, A.M. Takeda, and R.D. Behrend. 2011. Structural complexity
and distance from source habitat determine invertebrate abundance and diversity.
Biotropica 43(6):738–745.
Osenberg, C.W. 1989. Resource limitation, competition, and the influence of life history in
a freshwater-snail community. Oecologia 79:512–519.
Osenberg, C.W., G.G. Mittelbach, and P.C. Wainwright. 1992. Two-stage life histories in
fish: The interaction between juvenile competition and adult performance. Ecology
73(1):255–267.
Parsons Inc., Exponent Inc., and Anchor QEA LLC. 2010. Onondaga Lake Baseline Monitoring
Report. Prepared for Honeywell Inc. Available online at http://www.dec.ny.gov/
docs/regions_pdf/olbase2010.pdf . Accessed 15 July 2011
Peckarsky, B.L., P.R. Fraissinet, M.A. Penton, and D.J. Conklin Jr. 1990. Freshwater Macroinvertebrates
of Northeastern North America. Cornell University Press, Ithaca, NY.
422 pp.
Peets, R., A.C. Miller, and D.C. Beckett. 1994. Effects of three species of aquatic plants
on macroinvertebrates in Lake Seminole, Georgia. Technical Report A-94-5. US Army
Corps of Engineers, Vicksburg, MS.
Perrow, M.R., A.J.D. Jowitt, J.H. Stansfield, and G.L. Phillips. 1999. Practical importance
of the interactions between fish, zooplankton, and macrophytes in shallow-lake restoration.
Hydrobiologia 395/396:199–210.
Rosine, W.N. 1955. The distribution of invertebrates on submerged aquatic-plant surfaces
in Muskee Lake, Colorado. Ecology 3(2):308–314.
Schramm, H.L., K.J. Jirka, and M.V. Hoyer. 1987. Epiphytic macroinvertebrates on
dominant macrophytes in two Central Florida Lakes. Journal of Freshwater Ecology
4(2):151–165.
Theel, H.J., E.D. Dibble, and J.D. Madsen. 2008. Differential influence of a monotypic
diverse native aquatic plant bed on a macroinvertebrate assemblage: An experimental
implication of exotic plant induced habitat. Hydrobiologia. 600:77–87.
Thorp, A.G., R.C. Jones, and D.P. Kelso. 1997. A comparison of water-column macroinvertebrate
communities in beds of differing submersed aquatic vegetation in the tidal
freshwater Potomac River. Estuaries 20(1):86–95.
Underwood, G.J.C., J.D. Thomas, and J.H. Baker. 1992. An experimental investigation of
interactions in snail–macrophyte–epiphyte systems. Oecologia 91:587–595.
Van den Berg, M.S., H. Coops, R. Noordhuis, J. Van Schie, and J. Simons. 1997. Macroinvertebrate
communities in relation to submerged vegetation in two Chara-dominated
Lakes. Hydrobiologia 342/343:143–150.
Voigts, D.K. 1976. Aquatic invertebrate abundance in relation to changing marsh vegetation.
American Midland Naturalist. 95:312–322.
Watkins, C.E., J.V. Shireman, and W.T. Haller. 1983. The influence of aquatic vegetation
upon zooplankton and benthic macroinvertebrates in Orange Lake, Florida. Journal of
Aquatic Plant Management 21:78–83.
Wersal, R.M., B.R. McMillan, and J.D. Madsen. 2005. Food habits of dabbling ducks during
fall migration in a prairie-pothole system, Heron Lake, Minnesota. The Canadian
Field-Naturalist 119(4):546–550.