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Population Dynamics and
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Valerie J. Brady

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ZEBRA MUSSELS (DREISSENA POLYMORPHA)
IN A GREAT LAKES COASTAL MARSH:
POPULATION DYNAMICS AND EFFECTS ON THE INVERTEBRATES
‘ By

Valerie J. Brady

A DISSERTATION

Submitted to
Michigan State University
in partial fulﬁllment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

Zoology Department

1996

ABSTRACT
ZEBRA MUSSELS (DREISSENA POLYMORPHA)
IN A GREAT LAKES COASTAL MARSH:
POPULATION DYNAMICS AND EFFECTS ON THE INVERTEBRATES

By

Valerie J. Brady

I documented zebra mussel (Dreissena polymorpha) population dynamics in a
Saginaw Bay, Lake Huron, coastal wetland and investigated the potential effects this
ﬁlterer might have on marsh zooplankton and macroinvertebrate communities. This
research was conducted during 1993, 1994, and 1995. Clusters of mussels over-wintered
in the outer area of the emergent marsh and were the source of recruitment for the marsh
population. Recruitment was primarily onto stems of the dominant emergent plant, three-
square bulrush (Scirpus americanus). Peak larval production and settlement occurred
between 300 and 350 m from shore in July and August, respectively. Disappearance of
mussels from stems decreased abundance by up to 80% in this area by the end of
September in 1994. Lack of recruitment closer to shore and high loss of mussels in the
middle section of the marsh was probably due to very little water movement in the center
and nearshore areas.

The ability of this population to impact the wetland invertebrate community was
examined both experimentally and by comparing the pre—existing community to that
present alter the invasion. Zooplankton remains, particularly rotifer loricas, were observed

in the feces of wetland mussels. Predation by mussels on rotifers and small Bosmina

longirostris was experimentally conﬁrmed for high mussel ﬁltration capacities. Mussel
ﬁltration capacities more representative of the marsh population did not signiﬁcantly
reduce the abundance of any zooplankton. A laboratory experiment was designed to
examine the potential for mussel competition with marsh Cladocera. After being cultured
for 14 days in the presence of a range of mussel ﬁltration capacities, Ceriodaphm'a dubia
abundances were signiﬁcantly lower at higher ﬁltration capacities. Negative effects of
competition on C. dubia became apparent at mussel ﬁltration capacities higher than those
calculated for the marsh mussel population. A comparison of the Cladocera community
before (1990) and after (1994) zebra mussels colonized the marsh showed no evidence of
changes attributable to zebra mussels.

The wetland macroinvertebrate community showed more evidence of changes
potentially related to zebra mussels than did the wetland zooplankton. The abundances of
larval Tanytarsini increased on plant stems (p = 0.03) between 1990 and 1994 while at the
same time decreasing in density in the sediment (p = 0.08), perhaps indicating a habitat
shiﬁ. Abundances of tubiﬁcid oligochaetes were signiﬁcantly higher (p = 0.04) in marsh
sediments in 1994. No other groups had signiﬁcant changes in abundance, nor was there a
change in the number of taxa present between 1990 and 1994. These results indicate that

zebra mussels are not having a major impact on coastal wetland invertebrates.

To those who introduced me
to the beauty and wonder
of the natural world:

Dorsey M. Ennis

Shelby and Lora Ennis
Mr. Charles Stuermer

l1

ACKNOWLEDGMENTS

I would like to thank my major professor, Thomas M. Burton, and the members of
my committee, John P. Giesy, Donald J. Hall, Richard W. Merritt, and Frank M. D’Itri,
for their guidance, suggestions, and support throughout the course of this research. I am
indebted to John Brazner, USEPA, and Joseph Gathman, MSU, for their ideas, critiques
and general encouragement. Bradley J. Cardinale and Thomas M. Burton coauthored the
manuscript reproduced in Chapter One and made many suggestions for the improvement
of the other sections. Chapter One was further improved by our reviewers, Thomas
Nalepa, David Klarer, David Barton, and Lucinda Johnson. Many thanks are due Keith
Kintigh, Pamela Machuga, Stephen Ennis, Jon Nelson, Jennifer Rau, Catherine Dagle,
Holly Hintennan, Kurtis Peterson, Jeﬁ Oles, Stephanie Gollakner, and Carrie Thill for
many hours of assistance. 8. Jerrine Nichols, NBS, provided invaluable information on
larval mussel collection and mussel culturing. I am grateful to Brian Nagy and Lancie Dole
of the MSU Aquatic Toxicology Laboratory for providing food for the culture animals. I
am also grateful to Nathaniel Ostrom of the MSU Environmental Geochemistry
Laboratory for analyzing the carbon content of the culture food. Although the research in
this document has been funded in part by the USEPA under assistance agreement
CR821349-01-0 to T.M. Burton and the USDA under National Needs Graduate
Fellowship 91-38420-6111 to V.J. Brady, it may not necessarily reﬂect the views of either
agency and no ofﬁcial endorsement should be inferred.

V

TABLE OF CONTENTS

List of Tables
List of Figures
Introduction
Chapter One: The Seasonal and Spatial Limits of Colonization
1. Introduction
2. Site Description
3. Methods
4. Results
5. Discussion
Chapter Two: Potential Interactions with Wetland Zooplankton
1. Introduction
2. Methods
2.1 Site Description
2.2 Zooplankton Remains in Mussel Feces
2.3 Zooplankton Vulnerability to Mussel Filtration
2.4 Competition between Mussels and Ceriodaphnia dubia
2.5 In Situ Eﬁ‘ects of Mussels on Cladocera

2.6 Filtration Capacities

viii

10

17

21

21

22

22

24

24

27

32

34

Table of Contents (cont).

3. Results
3 .l Zooplankton Remains in Mussel Feces
3 .2 Zooplankton Vulnerability to Mussel Filtration
3.3 Competition between Mussels and Ceriodaphm’a dubia
3 .4 In Situ Effects of Mussels on Cladocera
3.5 Filtration Capacities
4. Discussion
4.1 Mussel Predation on Zooplankton
4.2 Mussel Competition with Cladocera
5. Summary and Conclusions
Chapter Three: Effects on Macroinvertebrates
1. Introduction
2. Methods
3. Results and Discussion
Summary and Conclusions

Literature Cited

vii

36

36

39

39

45

48

SO

50

53

55

57

57

59

62

74

78

Table 1.

Table 2.

Table 3.

Table 4.

Table 5.

Table 6.

Table 7.

Table 8.

Table 9.

LIST OF TABLES

Net change in numbers of zebra mussels attached to bulrush stems
between August and September 1994. Percent loss or gain, which
includes both survival and/or migration, was calculated with the
assumption of 2 mm growth per month.

Clusters (druses) of viable mussels found after ice-out two consecutive
winters. In 1993-1994, viability was assessed qualitatively. Thus, a plus
indicates location of viable clumps while a minus indicates dead or
absent clumps. In 1994-1995 we assessed viability quantitatively.

Experimental design used to investigate zooplankton vulnerability to
zebra mussel ﬁltration.

Sizes, densities, and ﬁltration capacities of zebra mussels cultured with
C eriodaphnia dubia.

Filtration rates used to estimate the ﬁltration capacities of selected
Cladocera.

Mean number of zooplankton remains found in the feces of individual
zebra mussels i 1 standard error. Numbers in parentheses indicate
percentage of mussels with that group in their feces.

Percent decrease in zooplankton abundance (by size fraction) due to
zebra mussel entrainment. Experiments were conducted in 2 L
containers (r = 0.075 m) and lasted for 90 (experiments 1 and 2) or 180
(experiment 3) minutes.

Results of culturing Ceriodaphnia dubia with various sizes and
densities of zebra mussels for 14 days. Initial C. dubia density was
0.02/m3.

Regressions developed from Ceriodaphnia dubia population responses

(y) to culturing for 14 days in the presence of zebra mussels (x).

viii

15

16

26

31

35

37

4O

41

44

Table 10.

Table 1 1.

Table 12.

List of Tables (cont).

Means i 1 standard error (n=8) of the number of Cladocera species and
abundances of the dominant ﬁltering species in both areas of marsh for
August through November of each year.

Means i 1 standard error (n=8) of the number of macroinvertebrate
taxa and abundances of the dominant epiphytic groups in both areas of
the marsh for August through November of each year.

Means i 1 standard error (n=8) of the number of macroinvertebrate
taxa and abundances of the dominant benthic groups in both areas of
the marsh for August through November of each year.

i)

49

70

70

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

LIST OF FIGURES

Location of study site in Vanderbilt Park Marsh, Saginaw Bay, Lake
Huron. Boxes along transect show larval sampling locations in 1993
and 1994. Black boxes represent substrates lost during storms.

Seasonal and spatial distribution of larval and attached mussels from
May - November, 1993. Notice the difference in the Y-axis scale-
larval sampling substrates beyond 350 m were lost during storms.
Water temperatures were taken at 350 m.

Seasonal and spatial distributions of larval and attached mussels from
May - November, 1994. Water temperatures were taken at 350 m.

Attached mussel density during peak abundance, August 1994. The

correlation between mussel density and Scirpus americanus density
was 0.84 (p<0.001).

Location of the study site and sampling transect in Saginaw Bay,
Lake Huron.

Composition of the marsh zooplankton community in 1994 during
experiments assessing zooplankton vulnerability to zebra mussel
ﬁltration. The community has been size-fractioned.

Ceriodaphm‘a dubia population size when cultured in the presence of
a range of zebra mussel ﬁltration capacities (top) and the regression
(with 95% CI.) based on the log of these abundances (bottom).

Top: Mean densities i 1 standard error of selected Cladocera in the
bayward area of the coastal marsh. Bottom: Filtration capacity of
four species of Cladocera and zebra mussels and the percent of the
marsh water column that each group could ﬁlter each day. In all
graphs the Y-axis is a log scale.

11

12

14

23

38

42

47

Figure 9.

Figure 10.

Figure 11.

Figure 12.

Figure 13.

List of Figures (cont).

Location of the study site and sampling transect in Saginaw Bay,
Lake Huron.

Mean densities j: 1 standard error of epiphytic and benthic
chironomid larvae from nearshore and offshore areas of a coastal
marsh.

Mean densities i 1 standard error of epiphytic and benthic
oligochaetes and nematodes ﬁom nearshore and offshore areas of a
coastal marsh.

Community composition of the epiphytic (top) and benthic (bottom)
macroinvertebrate communities in the nearshore and offshore marsh
areas. Each bar represents two samples per month for Aug-Nov. for
an n=8.

Densities of larval Tanytarsini and Tubiﬁcidae before and after zebra
mussel colonization. Top: Epiphytic Tanytarsini; p = 0.03. Center:
Benthic Tanytarsini; p = 0.08. Bottom: Benthic Tubiﬁcidae; p = 0.04.

60

64

67

68

71

INTRODUCTION

The accidental introduction of zebra mussels (Dreissena polymorpha Pallas) into
North America in 1986 (Hebert et al. 1989) has provided ecologists with the opportunity
to investigate and understand a biological invasion in progress. The effects of an invading
species depend both on the nature of the species and the structure of the invaded
community (Lewin 1987). The zebra mussel’s rapid and successful colonization of much
of the United States and Canada can be attributed in part to their high fecundity of up to 1
million eggs released per summer by a single female (Snyder et al. 1994). These tiny
planktonic (veliger) larvae are rapidly dispersed by water currents and accidental human
transport (Cooley 1991). Zebra mussels typically suffer their highest mortality during the
larval stage due to cannibalism by adult mussels and settlement onto inappropriate
substrates (Stanczykowska 1977, MacIsaac et al. 1991). Low densities of adult mussels in
newly colonized areas and an abundance of colonizable surfaces has allowed much higher
survival in many areas (MacIsaac et al. 1991). Finally, the mesotrophic condition of many
areas provided both juvenile and adult mussels with a large food resource (Snyder et al.
1994), supporting high fecundity. This match between the life history requirements of the
invader and the characteristics of the invaded ecosystem (Lewin 1987) allowed D.

polymorpha to reach very high densities in many areas of the Great Lakes.

2
Zebra mussels change aquatic ecosystems by altering the way food resources are

allocated (Nalepa and Fahnenstiel 1995) and increasing the heterogeneity of benthic
surfaces (Grifﬁths 1993). Mussels ﬁlter bacteria, phytoplankton, and other organic
material and nutrients from the water column and deposit feces and pseudofeces in the
sediment (Nalepa and Fahnenstiel 1995). This process shifts the base of the food chain
from planktonic to benthic. Studies indicate that zebra mussels approximately 2.25 cm
long ﬁlter particles ranging from 50 - 400 pm in length (MacIsaac et al. 1991). This
particle size range, coupled with the mussel’s high ﬁltration capacity (1 L/mussel/day,
Reeders et al. 1991) and high densities, suggests that food web changes could take place
very rapidly. For example, Hebert et al. (1991) calculated that zebra mussels could ﬁlter
the entire volume of Lake St. Clair twice daily in 1989. Increased water clarity and
concomitant macrophyte grth were already apparent in Lake St. Clair by 1990, and
populations in some places had reached 341,000/m2 (MacIsaac et al. 1991, Griffiths
1993). The large decrease in Lake St. Clair phytoplankton would be expected to limit
zooplankton populations. Hebert and colleagues (1991) hypothesized that only the
importation of zooplankton from Lake Huron was keeping the Lake St. Clair
phytoplankton population from collapsing. By 1994, Lake St. Clair had shifted from a
planktonic to a benthic food web, with large changes observed in most trophic levels,
including the behavior and abundances of some species of ﬁsh and waterfowl (Ross 1994).
Increases were observed in some benthic invertebrates, but other species disappeared
(Griffiths 1993).

Impacts of D. polymorpha on invertebrates have been investigated in many areas

around the Great Lakes (Dennott et al. 1993, Griffiths 1993, Mackie 1991, Stewart and

3
Haynes 1994). However, the impacts of zebra mussels on littoral areas have received

much less attention. It is important to determine the magnitude of zebra mussel effects on
littoral zone food webs because of their importance to the overall ﬁrnctioning of lake
ecosystems. Jude and Pappas (1992) found that 75% of Great Lakes ﬁsh species are
dependent on coastal wetlands during some portion of their life history. Thirty two of 36
species collected by Stephenson (1990) were using Lake Ontario coastal marshes for
reproduction. The wetlands provided abundant food resources (phytoplankton,
zooplankton, and invertebrates) for the young ﬁsh, as well as protection from predators
(Stephenson 1990). Brown et al. (1995) found that Lake Huron littoral zone ﬁsh
assemblages were still predominantly composed of native species, indicating the
importance of these areas for native ﬁsh production. Changes at the base of the food web
have the potential to impact these populations which rely on Great Lakes coastal wetlands.

Zebra mussels could potentially alter the wetland invertebrate community in
several ways. First, zooplankton, particularly the smaller, weaker groups, might suffer
predation from zebra mussels (MacIsaac et al. 1991). Secondly, zebra mussels might
compete with planktivores for food resources (Mackie 1991). Third, the shift in energy
from the plankton to the benthos by D. polymorpha might beneﬁt benthic invertebrates
(Stewart and Haynes 1994, Izvekova and Lvova-Katchanova 1972). If these effects were
on a sufﬁcient scale, species higher up in the food web would also be affected.

A quantitative analysis of the invertebrate community in the most extensive
remaining wetland complex in Lake Huron, the Saginaw Bay east coastal wetland (Prince
and Flegel 1995, Wilcox 1995), was completed just before zebra mussels colonized this

area (Brady 1992). This dataset provided the opportunity to investigate changes to this

4
community caused by D. polymorpha. Zebra mussels were found in Saginaw Bay in 1990,

and by 1992 reached densities of 60 to 120 thousand/m2 on rocks in shallow areas
(Pillsbury and Lowe 1994). Mussels were ﬁrst observed on bulrush stems in the wetland in
1991, with one to ﬁve mussels per stem being common. My research was conducted from
1993 - 1995. The subsequent chapters 1) document the zebra mussel’s colonization,
survival, and population dynamics in a coastal wetland; 2) investigate the potential for
zebra mussel predation on and competition with the marsh zooplankton community; and
3) compare the pre-invasion macroinvertebrate community to that present after zebra
mussels became established. These results will indicate the invertebrate community
changes that can be expected in shallow lake littoral zones as zebra mussels continue to

spread.

CHAPTER ONE

THE SEASONAL AND SPATIAL LIMITS OF COLON IZATION

Introduction

Most research regarding zebra mussels (Dreissena polymorpha Pallas) in the Great
Lakes has concentrated on the open waters of the lakes and bays. It is generally accepted
that colonization in these areas is limited, at least in part, by the availability of hard
substrates. Great Lakes coastal marshes, however, provide an almost unlimited amount of
colonizable surface area in the form of emergent macrophytes. Macrophyte stems have
been shown to be good substrates for larval settlement (Lewandowski 1982), yet the
vegetation in many coastal marshes is destroyed each winter by ice scour. In addition, the
water in these shallow littoral zones often ﬁ'eezes down to the sediment. These
observations led us to two predictions: (1) mussels would not be able to maintain year-
round populations due to a lack of suitable substrate in the winter, and (2) the summer
populations often observed in these marshes were the result of recruitment from offshore
communities. In this study we examined the above predictions and characterized the extent

and abundance of the mussel population within a typical coastal marsh.

Site Description

Our study site was located in an extensive wetland complex along the southeastern
shore of Saginaw Bay, Lake Huron (Figure 1). This site was characteristic of many of the
exposed coastal marshes around Saginaw Bay, with emergent vegetation dominated by
three-square bulrush (Scirpus americanus Pers.) extending 500 m from shore. Small
patches of other emergent vegetation such as cattail (T ypha angustifolia L.), arrowhead
(Saggitaria Iatifolia Willd.), and spikerush (Eleocharis smallii Britton) were present
(Prince and Burton 1994). A characterization of the submergent vegetation in this area is
presented elsewhere (Suzuki et al. 1995).

The upper marsh sediments were primarily sand (85-97%) with much smaller
portions of clay and silt (Suzuki et al. 1995). Water depth gradually increased bayward,
but the slope was shallow and irregular. Depth at the outer edge of the emergent
vegetation ranged ﬁom 75 to 110 cm during our study, while depths closer to shore were
up to 30 cm shallower.

Methods

Larval and attached mussels were routinely sampled during the ice free seasons of
1993 and 1994 along a transect which bisected the marsh from shore to open water (500
m). Larvae were collected on 900 cm2 sheets of tulle (bridal veil mesh) placed inside
plastic mesh boxes. This material has been shown to be successful in attracting all stages
of larval and juvenile mussels (S. J. Nichols, personal communication, National Biological
Service). One box (n=5) was placed every 50 to 100 m along the transect (Figure 1). The

tulle was collected and exchanged at 14 day intervals from May through October. Larvae,

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deﬁned as mussels s 0.5 mm, were washed from the tulle into a 60 um sieve, preserved in
ethanol, and enumerated under 15x magniﬁcation.

Attached mussels were sampled monthly by collecting 4 stems of S. americanus
every 50 m along the transect. Mussels were scraped from the stems, preserved, and
divided into 4 size classes (0.6-2.0 mm, 2.1-4.0 mm, 4.1-6.0 mm, and 6.1-8.0 mm). The
abundance of each size class is generally expressed as number per stem throughout this
paper. However, during peak abundance in 1994 we also determined stem densities along
this transect using a 0.0625 m2 quadrat, allowing calculation of areal mussel densities.

We used 3-dimensional contour plots with a distance-weighted least squares
(DWLS) smoothing function (tension=0. 10, cut=50, SYSTAT 1992) to display changes in
zebra mussel density over time and space. We chose the DWLS function because the
algorithm produces a true, locally weighted curve. This, along with the low tension
setting, shows local irregularities more accurately than other methods such as linear or low
order polynomial smoothing.

We examined the net loss/gain of attached mussels relative to distance ﬁ'om shore
for each size class over the interval of August 25 - September 24, 1994. Net changes in
the attached population represent both survival and migration, as we were unable to
separate the two. August 25 was the ﬁrst date with enough attached mussels to make
such an analysis feasible.

In interpreting net loss/gain in the population, two assumptions were made: (1)
grth rates were 2 mm/month, and (2) growth rates did not differ between size classes.

These assumptions are consistent with other studies such as Dorgelo (1993) and Mackie

9

(1993) who found that growth rates for mussels of these sizes were from 1 to 3
mm/month. In addition water temperature in the marsh was very consistant during the
chosen time interval. Furthermore, Neumann et al. (1993) determined that mussels
between 4 and 7 mm displayed very similar grth rates.

In addition to routine sampling, we examined the potential for mussels to survive
in the marsh over the winter. In November 1993 we placed clumps of live mussels inside
10 small (15 x 15 x 10 cm) mesh boxes. Each clump (druse) consisted of 500 to 1000
individuals. One box was anchored to the sediment every 50 m along the transect
beginning at 100 m from shore and extending into open water. Maximum/minimum
thermometers were attached to the boxes at 100, 350, and 550 m. Boxes were retrieved
shortly after ice-out (early April 1994) and transported to the laboratory where the clumps
were placed in aquaria at 12°C to initiate ﬁltration. Live individuals were preserved in an
open position by slowly adding ethanol over a period of several hours. Clusters were
labeled as viable or nonviable and survival relative to distance from shore was examined.

To supplement this experiment with observations under natural conditions, we
searched for clumps of living mussels in the early spring of both 1994 and 1995. In 1994
the area was qualitatively searched during the retrieval of the overwintering experiment.
In 1995 we systematically searched a 3 m radius at 40 m intervals along the transect.
Clusters found within this radius were again determined to be viable or nonviable, and

survival was examined relative to distance from shore.

1 0
Results

In 1993, larvae were ﬁrst collected in June, but the highest larval densities of
300/trap occurred in July following a water temperature increase from 20 to 27°C (Figure
2). Artiﬁcial substrates beyond 350 m were repeatedly destroyed by strong seiches, thus it
was impossible to distinguish at what distance from shore peak abundance occurred.
Larval abundance decreased dramatically by the end of July, and very low numbers were
observed until September. Attached mussels were ﬁrst noted in July, despite the fact that
macrophytes had been available for colonization since June. Most of these individuals
were in the smallest size class (0.6-2.0 mm) suggesting that they were recruits from the
July larval peak. Maximum abundance of attached mussels occurred in August at 450 m
from shore with nearly 100 individuals/stem (Figure 2). By November these densities had
dropped to only 8/stem even though most of the Scirpus was still standing. Neither larvae
nor attached mussels were found shoreward of 300 m in 1993.

In 1994, larvae were ﬁrst collected in June and continued to be present in very low
numbers through August. The larval peak of 470/trap occurred in July at 300 m from
shore, and followed a sharp water temperature increase from 25 to 40°C (Figure 3). As in
1993, attached mussels were not found early in the year even though Scirpus stems were
available for colonization. The highest abundance of attached mussels again occurred in
August (77/stem) which, like the previous year, suggests recruitment from the July larval
peak (Figure 3). Attached mussel abundance decreased to 15/stem by late September and

remained at this density through November.

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l3

Attached mussel abundance in 1994 was greatest at 300 m from shore (77/stem)
and remained fairly high bayward (Figure 3). As in 1993, neither larvae nor attached
mussels were found in the shoreward half of the emergent vegetation. The areal density of
mussels was highly correlated with Scirpus density (Figure 4, p = 0.84, p < .001). Highest
overall densities occurred at 300 m from shore with nearly 55,000 mussels/m2, due in part
to the high density of bulrush in this area.

The relative losses or gains in the numbers of mussels on Scirpus stems from late
Aguust to late September 1994 showed a strong spatial trend (Table l), with
disproportionately high losses in the middle of the marsh (300 - 400 m) for all size classes
combined (x2 = 121.9, p < .005). Losses were most pronounced for the 2.1-4 mm size
class, followed by the 0.6-2 mm size class. We did not calculate relative losses or gains
for mussels occurring closer to shore than 300 m because their abundances were very low.

Results of the 1993-94 overwintering experiment revealed surviving mussels in the
outer third of the marsh. Clumps placed from 350 to 500 m from shore consisted almost
entirely of live individuals, while mussels placed 100 to 300 m from shore exhibited
complete mortality (Table 2). Shoreward of 300 m the mussels had obviously been frozen
as the minimum temperature recorded was -8°C. Mussels past 350 m did not experience
minimum temperatures below 0°C. Our search for naturally occurring clumps each spring
conﬁrmed the presence of viable mussels in the outer half of the marsh (Table 2). Using
the range of individuals we have previously found in clusters, we estimated densities of up
to 300 individuals/m2 in spring 1995. This represents only 5 - 10% of the areal density of

mussels found attached to stems the previous November.

l4

 

 

 

 

 

[I] 60 800 +
NE N
E E
E 30 ~ 71
s s
.92 8*
0 - a
3 ‘ l I ' ' ' l

2

Distance from Shore (m)

Figure 4. Attached mussel density during peak abundance, August 1994. The correlation
between mussel density and Scirpus americanus density was 0.84 (p < 0.001).

15

TAB LE 1. Net change in numbers of zebra mussels attached to bulrush stems between
August and September 1994. Percent loss or gain, which includes both
survival and / or migration, was calculated with the assumption of 2 mm growth

 

 

 

per month.
Size class Distance Number per stem :1: s.e. % Loss or gain
from shore (111) Aug 25 Sept 24 (survival i migration)

0.6 to 2.0 mm 300 56.3 :1: 14.5
350 7.2 i 2.5
400 32.7 i 12.7
450 28.0 i 11.0
500 8.4 :1: 4.6

2.1 to 4.0 mm 300 17.3 :1: 4.3 11.0 i 4.4 -80
350 3.4 :1: 0.5 6.2 :t 2.1 -13
400 13.7 d: 6.3 16.2 :1: 8.3 -50
450 21.7 d: 9.8 28.2 d: 10.8 +1
500 11.4i 7.0 l7.7i7.1 +111

4.1 to 6.0 mm 300 3.0 :t 1.0 1.0 :1: 0.4 -94
350 1.2 :b 0.4 1.0 d: 0.4 -71
400 3.0 :1: 1.5 5.7 i 4.1 -58
450 1.3 i 0.8 12.0 :1: 6.2 -45
500 0.6 i 0.4 6.2 :1: 3.1 -45

6.1 to 8.0 mm 300 1.0 :1: 0.7 -67
350 0.2 :1: 0.2 -83
400 0.5 :1: 0.3 -83
450 2.0 a: 0.9 +54
500 1.5 :1: 0.5 +150

 

16

TABLE 2. Clusters (druses) of viable mussels found after ice-out two consecutive
winters. In 1993-1994, viability was assessed qualitatively. Thus, a
plus indicates location of viable clumps while a minus indicates dead

or absent clumps. In 1994 - 1995 we assessed viability quantitatively.

 

 

Distance from 1993 - 1994 1994 - 1995
shore (m) Experiment Observation Clusters / m2 Individuals / m2

50 - - O O
100 - - 0 0
150 - - 0 O
200 - - O O
250 - - 0.07 35-70
300 - - 0.20 106-212
3 50 + + 0.25 124-247
400 + + 0.30 150-300
450 + + 0.18 88-177
500 + + 0.04 18-35

 

17

Discussion

Originally, we anticipated poor winter survival of zebra mussels in this coastal
wetland due to the senescence and ice scour of emergent bulrush - the primary substrate
available for colonization. We hypothesized that ice cover would result in almost
complete mortality of mussels each winter, and that summer populations would arise from
settling mussels recruited ﬁ’om oﬁshore colonies. Although a few of these small mussels
might reach reproductive size by fall, freezing would again reset the cycle for the
following year.

We now believe our hypothesis was incorrect. Our spatial analysis showed that
peak recruitment in 1994 occurred fi'om a spawning event within the wetland rather than
ﬁom offshore waters. The most likely source of this recruitment was the overwintering
clusters which contained the only adult mussels within the marsh. Reproductive size
mussels (>6mm) were only found on bulrush stems after peak larval abundance, and they
never occurred in any notable densities. Thus, we believe populations were not
replenished each summer by offshore recruitment but were instead “seeded” by the adults
within substrate independent clusters.

Our experiment suggested that clusters of mussels could over-winter in the marsh.
These results may simply indicate that the temperature extremes could be tolerated since
the boxes might have protected the clumps from ice scour. However, sampling in the
spring of both 1994 and 1995 supported our ﬁndings because viable clusters of mussels
were found under natural conditions in the outer half of the emergent zone. Using the

regression developed by Assel (1976), we calculated a maximum littoral ice depth of 37

18

cm for Saginaw Bay in 1993-94, one of the most severe winters in the last two centuries
(R.A. Assel, personal communication, Great Lakes Environmental Research Laboratory).
This depth would indicate complete freezing to approximately 300 m from shore at our
site, beyond which we noted surviving mussels. Taken collectively, these results suggest
that zebra mussels are surviving even severe winters in the outer half of the marsh as
clusters unattached to bulrush stems.

We found as many or more zebra mussels per m2 in this littoral zone as have been
reported from open waters. The density of attached mussels in the bayward half of the
marsh ranged from about 1000 to 55,000 individual/m2. These numbers are comparable to
the averages reported for Lake St. Clair (Grifﬁths 1993) and nearshore Lake Erie
(Dermott et al. 1993). Furthermore, densities were often higher than those reported for
inner Saginaw Bay (Nalepa et al. 1995). However, total biomass may be lower in the
littoral zone since mussel grth on the dominant substrate is seasonally limited by the
availability of bulrush. Instead, adults can only accrue within the less abundant clusters.
This results in a littoral population skewed toward the smallest size class (0.6-2.0 m).

We did not anticipate the spatial distribution of mussels found during peak
abundance periods, especially the lack of larvae and attached mussels in the nearshore 250
m of vegetation each year. This pattern may be the result of a unique form of stratiﬁcation
recently described for coastal wetlands. Suzuki et al. (1995) documented a conductivity
gradient which divided a coastal marsh into two horizontally adjacent water masses - a
nearshore zone and an offshore zone. The nearshore zone had approximately 60% higher

ionic conductivity due to increased concentrations of Ca2+, Mg”, and K. The stability of

19

this stratiﬁcation was maintained by the emergent vegetation, which impeded mixing from
wind or wave energy. Data from an ongoing study indicate that this form of stratiﬁcation
also occurs at our site (Cardinale and Burton 1995). Thus, we hypothesize that as clusters
of mussels spawned in the offshore half of the marsh, a lack of water movement at the
stratiﬁcation interface prevented the planktonic veligers ﬁ'om distributing into the
nearshore zone.

There was clearly a positive relationship between net loss/gain in attached mussels
and distance ﬁom shore. The net gain beyond 450 m was a function of immigration with
attached mussel numbers more than doubling in some cases. The high net loss between
300 and 400 m suggests that attached mussels had low survivorship and/or were migrating
away from this area. These two possibilities are not mutually exclusive since factors
decreasing survivorship would also probably initiate migration. Previous studies have
shown mussel survival to be positively correlated with colonizable surface area and food
availability, but negatively correlated with vegetative senescence and turbidity
(Lewandowski 1982, Stanczykowska 1977). At our study site bulrush densities were
highest in the area of highest net loss, and the stems did not begin senescence until
November - well beyond the time interval we considered. In addition, turbidity was
highest at the bayward edge of the marsh due to increased wave exposure (Cardinale and
Burton 1995). Therefore, differences in substrate and turbidity do not appear to explain
our observations.

The other alternative, food availability, may be an important factor due to

ﬂuctuating algal concentrations caused by horizontal shifts in the stratiﬁcation reported by

20

Suzuki et al. (1995). The stratiﬁcation interface was shown to move between 250 and
350 m with increasing or decreasing water levels caused by periodic seiches. Although the
offshore zone of the marsh had chlorophyll a concentrations similar to the eutrophic
waters of Saginaw Bay, the nearshore zone had 80 to 90% lower planktonic algal biomass
(Suzuki et al. 1995). Thus, the center of the marsh may be an area of constantly changing
resource availability. If true, this would represent a less than ideal environment for

mussels, particularly the smallest size classes.

CHAPTER TWO

POTENTIAL INTERACTIONS WITH WETLAND ZOOPLANKTON

Introduction

Zebra mussels (Dreissena polymorpha Pallas) have colonized lake littoral zones
along with their settlement of hard substrates in deeper waters. Because survivorship is
low and because littoral populations typically contain very few adults (Brady et al. 1995),
there has been comparatively little study of the impacts ﬁ'om these young mussels.
However, the addition of these invertebrate ﬁlterers to the coastal marsh food web could
affect littoral zooplankton. 1 Zebra mussels may compete with native ﬁlter-feeders for
planktonic food resources. For example, Leach (1992) found that zebra mussels could
Igreatly reduce ambient concentrations of chlorophyll a in offshore waters of Lake Erie.
Lewandowski (1983) calculated that the densities and ﬁltration capacities of small young
mussels in the littoral zone of a Polish lake exceeded those of the adult mussels occurring
in offshore colonies. In addition; D. polymorpha may also consume small or weak-
swimming zooplankton and change community composition through direct predation. This
potential has been demonstrated in laboratory experiments (MacIsaac et al. 1991) and in
mesocosms (Shevtsova et al. 1986) for some zooplankton taxa.

The lack of research on the potential for zebra mussels to affect these coastal
communities represents a large gap in our investigation of this invasion. In addition, while

21

_ +.'—..':—‘ ”.2; '; .'..-

22 _
decreases in phytoplankton abundance have been linked to zebra mussels, this has not yet

been demonstrated to have affected cmstacean zooplankton populations in the Great

Lakes. Thus, the purpose of this research was to determine whether zebra mussels in

lakeshore marshes were likely to have a signiﬁcant effect on the zooplankton community.
Brady and Burton (1995) determined that a Saginaw Bay coastal wetland

contained a microcrustacean community with more than 35 taxa which reached densities

of 350,000/m3. This analysis was completed just prior to colonization of the wetland by D.
polymorpha in 1991. In 1994 zebra mussel densities in this marsh reached 55,000/m2
(Brady et al. 1995). The existence of this dataset provided the opportunity to compare the
pre-existing community (1990) with the community that came to coexist with zebra
mussels (1994). I tested the following hypotheses:

1. Zebra mussels are predators on small zooplankton, and

2. Zebra mussels are competitors for food resources with Cladocera and will have
a negative impact on cladoceran populations.

Methods

1. Site Description

Field work was conducted in the most extensive wetland complex in Saginaw Bay
(Lake Huron, Michigan), the Saginaw Bay east coastal wetland, which encompasses 6754
ha. (Wilcox 1995) (Figure 5). Emergent vegetation, dominated by three-square bulrush
(Scirpus americanus Pers.), extended 500 m from shore. Other emergents included cattail
(Typha angustifolia L.), arrowhead (Saggitaria Iatifolia Willd.), and spikerush
(Eleocharis smallii Britton) (Prince and Burton 1994). Submergent vegetation was only

abundant in shallow areas near the shore. Sediments were primarily sand, particularly

23

 

 

   

6
O

Saginaw Bay °

     

 

 

 

 

Figure 5. Location of the study site and sampling transect in Saginaw Bay,
Lake Huron.

24
toward the bayward edge. Water depth gradually increased bayward, reaching 70 to 110

cm at the outer marsh edge.

2. Zooplankton Remains in Mussel Feces

To determine whether marsh zebra mussels (Dreissena polymorpha) were
consuming zooplankton, I examined the fecal material from freshly collected mussels on
eight dates in the late summer and fall of 1995. Mussels were collected between 400 and
500 m ﬁom shore and chilled during transport to the laboratory. Individual mussels were
placed in cups of cool ﬁltered well water and allowed to ﬁlter and expel fecal material for
two hours. Individuals were then removed, measured, and categorized by shell length as
one (n=28), 1.5 (n=53), or two (n=46) cm mussels. Fecal material from each individual
was examined at 25x magniﬁcation for zooplankton remains, which were identiﬁed to the
lowest possible taxonomic unit. The mean number of carapaces in a mussel’s feces and the
percentage of mussels containing each taxonomic group were calculated for each of the
size classes.

3. Zooplankton Vulnerability to Mussel Filtration

Short-term experiments were performed to assess the vulnerability of various
zooplankton taxa to zebra mussel predation. The experiments, which were conducted on
site to minimize stress and damage to the zooplankton, took place on August 6
(experiment one), August 21 (experiment two), and October 15 (experiment three) of
1994. Experiments one and two exposed zooplankton to one (mean 822 mussels) or two
(mean 1827 mussels) clumps of zebra mussels which had been retrieved from the outer

section of the wetland. Experiment three exposed the zooplankton community to mussels

25
attached to S. americanus stems (mean 219 individuals). Experimental vessels were two L

plastic containers (r = 0.075 m, volume = 0.002 m3). (Table 3). The marsh zooplankton
community was concentrated for experiments one and two by ﬁltering 500 L through 60
um mesh and resuspending the zooplankton in 30 L of water, resulting in a concentration
of 17 times over ambient densities. The concentrated zooplankton still had a lower density
(about 100,000 individuals/m3) than the ambient density of 200,000 zooplankton/m3 in the
marsh in October. Because the zooplankton were more abundant on October 15, they
were not concentrated for experiment three. The collected zooplankton were
homogenized with very gentle mixing in a large container. Two L of the homogenized
200plankton were added to each experimental vessel after being passed through a one mm
sieve to remove any large invertebrate predators. Mussels in clumps (experiments one and
two) or on bulrush stems (experiment three) were added to all containers except controls
to begin each experiment (Table 3).

The mussels were allowed to ﬁlter for 1.5 (experiments one and two) or 3 hr
(experiment three), and then were removed, preserved, enumerated, and measured for
length to the nearest mm. The theoretical ﬁltration capacity of the mussels in each
container was calculated based on the published length-rate regressions of Bunt et a1.
(1993) and Reeders and Bij de Vaate (1990).

The regression from Bunt et al. (1993) was used for mussels S 1 cm:
PC = 0.057 x L‘-82

F C = ﬁltration capacity in ml/ind/hr
L = mussel shell length in mm

26

Table 3. Experimental design used to investigate zooplankton
vulnerability to zebra mussel ﬁltration.

 

 

Exp. # of zebra Zooplankton Duration
# Mussels concentration (min) Reps
0 17 x 3,5
1, 2 823 i 59' by 90 3,3
1827 i 281" Plankton tow 3,4
3 0 Ambient density 180 3
219 i 20c 14

 

“ 1 mussel clump.
b 2 mussel clumps.

° Mussels attached to S. americanus stems.

27
and the regression developed by Reeders and Bij de Vaate (1990) was used for larger

mussels:

PC = 15.63/(0.293 + 52.38am”)

PC = ﬁltration capacity in ml/ind/hr

L = mussel shell length in mm
Filtration capacities for each size class were multiplied by the number in that class for each
container and converted to m3/m2/d assuming a 16 hr daylength. Mean ﬁltration capacities
were 2.74, 5.6, and 0.17 m3/m2/d for one clump, two clumps, and mussels on stems,
respectively. Integrating mussel sizes and densities into the single variable of ﬁltration
capacity allowed the results from the various experiments to be more easily compared and
allowed for comparison with the mussel population in the wetland.
The zooplankton were ﬁltered out of each container using 60 um mesh, preserved

in 95% ethanol, then size-fractionated into categories of small (60-125 um), medium (126-
250 um), and large (251-1000 pm). These fractions were subsampled and one tenth of the
zooplankton in each category were enumerated and identiﬁed. Means and standard errors
for experiments one and two were calculated using the results from both experiments for
each treatment (control, or one or two mussel clumps). Concentrations of each taxon in
each size fraction were compared between the control and each mussel density using
Mann-Whitney’s rank sum. Finally, the percentage reduction in abundance of each taxon
was calculated. Box plots were generated to compare the percent reductions created by

mussels in clumps to those created by mussels attached to S. americanus stems.

28
4. Competition Between Mussels and Ceriodaphm‘a dubia

The potential for competition between zebra mussels and ﬁltering Cladocera was
investigated by culturing representative ﬁlter-feeder in the presence of various sizes and
densities of mussels. Ceriodaphnia dubia was selected to represent the Cladocera because
it is the planktonic ﬁlter feeder that was often abundant in the wetland. In addition,
neonate C. dubia are 300 pm at birth, making them unlikely to be ﬁltered out of the water
by mussels. This allowed the effects of competition to be examined separately from those
of predation. Finally, this species is easily cultured under laboratory conditions.

Ceriodaphnia dubia were collected from the marsh by plankton tow in October
1995 and maintained in mass culture. Cultures were fed both live algae (Selenastrum
capricomutum) and a mixture of yeast, digested Trout Chow, and dried Cerophyll (YTC)
obtained from the Michigan State University Aquatic Toxicology Laboratory. Zebra
mussels were obtained from the River Raisin at the Monroe (Michigan) power generating
facility in January 1996 and maintained in mass culture for several weeks. Cultures were
exposed to a light cycle of 16 h light:8 h dark under “warm” UV lights. Temperature was
22 to 25°C. Mussels in mass culture were fed dried Chlorella (Nichols 1993). Water for
both cultures and the experiment was well water ﬁltered through an activated charcoal
ﬁlter and then aerated overnight (initial assessment: pH 7.0, conductivity 533 uS/cm,
alkalinity 160 mg CaCO3/L).

The experiment was conducted in one L glass beakers. Cultures were fed a mixture
of S. capricomutum and YTC at a density based on summer wetland phytoplankton

production estimates of 1.7 mg carbon/L/d in mid-summer (based on unpubl. data from

29
Suzuki et al.). The amount of carbon in S. capricomutum and YTC was determined to be

39% and 34% by weight, respectively. These data were generated by the MSU
Environmental Geochemistry Laboratory. Each type of food supplied half of the daily
carbon estimate. Thus, each chamber received the equivalent of 2.2 mg S.
capricornutum/L/day and 2.5 mg YTC/L/day based on calculations from the dry weights
of each new batch of food. The food mixture was diluted in 250 mL ﬂasks, each of which
supplied two experimental chambers with 100 mL of food solution over 24 hr through a
gravity-fed continuous rrricrodrip system (Williamson et al. 1985). This continuous drip
food supply system was used to minimize food depletion over each 24 hr period. Food
ﬂasks were stirred with magnetic stirrers set on low speed to prevent settling of food
while minimizing damage to algal cells. Microtubing supplying the food had an internal
diameter of 350 pm (2 mm total diameter). Food ﬂasks were rinsed and reﬁlled every 24
hr. Food supply tubes were rinsed in culture water every 48 hr and replaced if clogged.
One of the biggest threats to successful laboratory culture of D. polymorpha is the
buildup of ammonia (Nichols 1993). Several steps were taken to reduce the possibility of
toxic ammonia buildup. First, half of the culture water was gently pumped out of each
chamber and replaced every 24 hr. The intake hose was covered with 60 um mesh and
held against the side of the container to prevent trapping zooplanktors against the screen
and damaging them. Secondly, zeolite, a mineral which absorbs ammonia, was added at 30
g/chamber. Finally, an air tube plugged with cotton and adjusted to gently produce tiny

bubbles was placed in each chamber to provide aeration. Ammonia and pH were checked

30
occasionally in the chambers containing the highest mussel densities. Ammonia did not rise

above 0.05 mg/L, while pH remained below 8.1 and was more commonly around 7.6.

The experiment began on February 8, 1996, with the addition of 20 adult female C.
dubia (density 0.02/m3) and the appropriate size and density of mussels to each chamber.
Mussel sizes and densities were selected to cover a range of ﬁltration capacities (0.04 to
0.93 m3/m2/d) so that regressions of ﬁltration versus various C. dubia population
variables could be developed (Table 4). The experiment was terminated after 14 days
because ﬁrngal grth was beginning in several of the chambers.

At the end of the experiment, zebra mussels were removed and preserved.
Ceriodaphm’a dubia were ﬁltered out of the culture water with a 60 um mesh and
preserved in chilled 10% buffered sugar formalin (Prepas 197 8). The total number of C.
dubia and the number of females with eggs were counted for each chamber. The lipid-
ovary-egg (LOE) index (T essier and Goulden 1982, Hoenicke and Goldman 1987) was
used to qualitatively assess the nutritional status of a subsample of each population.
Because the C. dubia were preserved for more than 48 hr before assessment, each sample
was immersed in a Sudan IV dye solution for 2.5 min to stain the triglycerides (Bjorkman
and Shapiro 1986). Four C. dubia in each of 3 size classes (600, 700, and 800 um) were
selected by locating the ﬁrst four individuals in each size class with intact carapaces. All
indexing was done at 30x magniﬁcation by the same person due to the subjective nature of
the analysis (Tessier and Goulden 1982).

The effects zebra mussels had on C. dubia populations were determined using

linear regressions. All dependent variables were loglo or loglo (x + 1) transformed to make

31

Table 4. Sizes, densities, and ﬁltration capacities of zebra mussels cultured with
C eriodaphm'a dubia.

 

Shell length (m) Number‘ Density (#/m2) Filtration capacity @3/m2/d)

0 (controls; n=6) 0 0 0b
5 25 3125 0.05
5 50 6250 0.11
8 50 6250 0.25
10 8 625 0.038
10 16 2000 0.12
10 30 3750 0.226
10 90 11,250 0.678
18 2 250 0.17c
18 4 500 0.34
18 11 1375 0.93
22 3 375 0.30
22 7 875 0.70
25 2 250 0.21
25 6 750 0.62

 

' Number per 1 L container.
" Based on length-rate regression of Bunt et al. (1993).
° Based on length-rate regression of Reeders and Bij de Vaate (1990).

32
the data approximately linear. A multiple linear regression was developed using the

independent variables of zebra mussel size and density versus the dependent variable of C.
dubia abundance. The validity of using the calculated ﬁltration capacity as a way of
integrating mussel size and density into a single variable was tested by comparing the
simple linear regression of ﬁltration capacity versus C. dubia abundance with the multiple
linear regression. This was necessary because the sizes and densities of mussels that could
be cultured in the laboratory did not overlap well with the size—density combinations that
were found in the wetland (Brady et al. 1995). The use of this single independent variable
provided a comparable regression, so ﬁltration capacity was regressed separately against
the mean LOE scores and the percentage of C. dubia with young. Data for all regressions
passed tests for normality and homoscedasticity.

5. In Situ Effects of Mussels on Cladocera

The question of mussel competition with marsh Cladocera was investigated by
comparing the pre-existing cladoceran community to that present after mussels had
colonized the emergent vegetation. Data on the Cladocera of this coastal wetland had been
collected in 1990 for another project (Brady and Burton 1995). To keep the data
comparable, the cladoceran community was sampled in 1993 through 1995 in the same
area using the same methods. All sampling was conducted along a single transect which
bisected the emergent zone from near shore (100 m) to open water (500 m; Figure 5).
Once a month from May through November a single sample of the epiphytic and
planktonic Cladocera was collected every 100 in along the transect with a modiﬁed

Gerking sampler (Mittelbach 1981). This sampler (21.5 cm 11)) enclosed the emergent

33
vegetation and water column to depth. At the laboratory, large vegetation within samples

was rinsed to remove any Cladocera. Samples (n=5 on each date) were sieved (250 um
mesh) and preserved in 95% ethanol with rose bengal dye to aid in sorting (Mason and
Yevich 1967). Each sample was later subsampled by dividing the sample into 6 equal parts
using a calibrated box subsampling device. One sixth of each sample was examined under
10x magniﬁcation and all Cladocera removed. Cladocera were identiﬁed using keys in
Brooks (1959), Balcer et al. (1984), and Dodson and Frey (1991). Numbers were
converted to number per cubic meter based on water depth.

Brady et al. (1995) previously determined that zebra mussels only become
abundant in the bayward 250 m of the marsh. The cladoceran community in this offshore
area of the marsh was compared before and after the zebra mussel invasion. The offshore
area was represented by samples collected from 400 and 500 m along the transect.
Samples collected during 1994 were used to represent the community present after mussel
colonization. The year 1994 was chosen because the mussels reached high densities in the
bayward area of the wetland (Brady et a1. 1995) and because the transect that year best
matched the 1990 transect location. Only samples from August through November were
used for each of the years because these were the only months in 1994 during which zebra
mussels were present in fairly high numbers (Brady et al. 1995). Abundances of routinely-
collected species, species richness, and the total density of the community were all
compared between 1990 and 1994.

Because the nearshore area was not colonized by the mussels, I considered this

area to be unimpacted by the invasion. This allowed differences in the communities before

34
and after mussel colonization to be conﬁrmed using BACI analysis as a conservative

statistic (Stewart-Oaten et al. 1986). Samples considered to be from the “control” area
were those collected at the 100 m and 200 m points along the transect (Figure 5) and
samples collected from 400 m and 500 m were classiﬁed as “impact” area samples,
providing an n of 8 for each of the areas each year.

6. Filtration Capacities

The potential for competition between the marsh mussel population and the
cladoceran community was ﬁlrther investigated by comparing the theoretical ﬁltration
capacities of the two groups. The ﬁltration capacity of the mussel population in the
emergent marsh was estimated based on mussel population densities from 1993 and 1994
(Brady et al. 1995) and on samples collected each month during the ice-free seasons of
1995. Samples were collected similarly in all three years. Attached mussels were scraped
ﬁom four S. americanus stems every 50 in along the transect, preserved in ethanol, and
measured to the nearest mm. Numbers per stem were converted to area] density based on
the density of S. americanus stems (1993: Brady unpubl. data; 1994: Brady et al. 1995;
1995: enumerated using a 0.025 m2 quadrat). The potential ﬁltration capacity of the
mussel population was calculated in a manner similar to the calculations for the ﬁltration
vulnerability experiment.

The ﬁltration capacities of the four most abundant ﬁltering Cladocera (Bosmina
Iongirostris, Ceriodaphnia dubia, Chydorus spp., and Sida crystallina) were calculated
for each date. Filtration rates for each taxon were obtained from the literature (Table 5).

No values could be located for Sida crystallina, so the ﬁltration rate of

35

Table 5. Filtration rates used to estimate the
ﬁltration capacities of selected Cladocera.

 

Filtration rate

 

Cladocera (ml/ind/day)
Bosmina longirostris 0. 8‘
C eriodaphnia quadrangularis 5.7'
Chydorus spp. 2.58”
Simocephalus vetulus 33'

 

b

Webster and Peters 1978
estimated from Lair 1991

36
Simocephalus vetulus was used as a surrogate. Simocephalus vetulus is another ﬁlter

feeder and is similar in size to S. crystallina. Densities of Cladocera were recalculated as
#/m2 so that the ﬁltration capacities would be comparable to those calculated for zebra
mussels. Theoretical ﬁltration capacities for each taxon on each date were calculated
based on their densities in the bayward marsh area. These capacities were summed to
obtain an estimate of the ﬁltration capacity of the dominant ﬁltering Cladocera. Finally, the
percent of the outer marsh which could be ﬁltered by these Cladocera on each date was
calculated based on the average water depth in this area. The capacity of zebra mussels to
ﬁlter this area was calculated similarly.
Results

1. Zooplankton Remains in Mussel Feces

Examination of mussel fecal material suggested that I rotifers and other small
zooplanktors might be vulnerable to mussel ﬁltration. Rotifer loricas were the most
common zooplankton remains found in zebra mussel feces for all three size classes of
mussels examined (Table 6). Similar numbers of rotifers, Bosmina Iongirostris, and
harpactacoid copepod remains in the feces of all three size classes of zebra mussels
indicated that mussels one cm and larger were capable of consuming zooplanktors 60 to
250 pm from several very different groups.

Rotifers were the dominant zooplanktors in the 60 to 125 um size class in the
wetland and were an important component of the 126 to 250 um size class (Figure 6).
Bosmina longirostris, adult copepods and copepod nauplii comprised the rest of this size

fraction. Other Cladocera, B. longirostris, and adult copepods dominated the largest size

37

Table 6. Mean number of zooplankton remains found in the feces of individual
zebra mussels ..+. 1 standard error. Numbers in parentheses indicate the
percentage of mussels with that group in their feces.

 

 

Mussel shell length
1 cm 1.5 cm 2 cm Total
Taxon (n = 28) (n = 50) (n = 43) (n = 121)
Rotifera 7.1 i 0.7 8.4 i 1 9.0 i- 1.1 8.3 i 0.6
(89%) (94%) (98%) (94%)
Bosmina 1.5 i 0.1 1.4 i 0.2 2.0 i 0.4 1.7 i 0.2
Iongirostris (7%) (22%) (23%) (19%)
Harpactacoida l .t 0 1 i 0 1.3 i 0.1 1.2 i 0.05
(7%) (10%) (33%) (17%)
Copepod 0:0 0i0 1i0 liO
nauplii (0%) (0%) (7%) (2%)
Ostracoda 0 i 0 1.5 i 0.1 2.3 i 0.2 2.1 i 0.1

(0%) (4%) (14%) Q%)

. ongirostris
er C1 doc a

38

ELu rod spuasnoql

 

 

 

 

 

 

 

 

 
 

 

 

 

cur Jed spuesnoql

60-125 126-

251-

60-125 126-

250

um

250 1000

um

Figure 6. Composition of the marsh zooplankton community in 1994 during experiments assessing their vulnerability

to zebra mussel ﬁltration. The community has been size-fractioned.

39

fraction (251-1000 um). Bosmina longirostris was the only cladoceran consistently
present in all size fractions, and was typically more abundant on these dates than all other
Cladocera combined. Composition of this community was determined in August and
October of 1994 during tests of the vulnerability of small zooplankton to mussel ﬁltration.

2. Zooplankton Vulnerability to Mussel Filtration

Vulnerability of small zooplankton to mussel predation was ﬁrrther tested by
exposing this community to several levels of mussel ﬁltration. IThere was substantial
entrainment of small zooplankton from even short-terrn exposure to the high ﬁltration
capacity (2.74 or 5.6 m3/m2/d) of mussels in clumps. All rotifers s 250 um exposed to
clumps of mussels were signiﬁcantly reduced relative to the controls (p < 0.05), with
reductions ranging from 64 to 81% (Table 7). The smallest of the B. Iongirostris (60 to
125 um) were also signiﬁcantly reduced by ﬁltration from mussel clumps (p < 0.05).
Abundances of copepod nauplii tended to be lower in the presence of mussel clumps, but
the decreases were not signiﬁcant. The lower ﬁltration capacity (0.17 m3/m2/d) of mussels
attached to S. americanus stems did not cause a signiﬁcant decrease in the abundance of
any zooplankton taxa, although rotifer and B. longirostris numbers in the 126 to 250 um
size ﬁaction tended to be reduced relative to controls (Table 7). By contrast mean
abundances of 60 to 125 um rotifers and copepod nauplii were elevated in association
with mussels on stems, suggesting that they had been added along with the mussels.

3. Competition between Mussels and Ceriodapm‘a dubia

The question of competition between zebra mussels and Cladocera was initially

tested by comparing population densities of a representative species (Ceriodaphm'a dubia)

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41
after culturing populations alone or in the presence of zebra mussels. The initial density of

20 C. dubia per beaker (0.02 ind/m3) increased to 195 to 676 ind/beaker (0.195 to
0.676/m3) in control beakers after 14 days, an increase of 10 to 30 fold. Ceriodaphnia
dubia abundances in beakers containing mussels ranged from 0 to 29l/beaker (0 to
0.29l/m3) after 14 days, representing a range from the complete loss of all individuals to
an increase of 15 fold (Table 8, Figure 7).

The regression of C. dubia abhiidance on mussel ﬁltration capacity produced a
highly signiﬁcant regression with a negative slope (Table 9), indicating that the population
densities were signiﬁcantly reduced by increasing levels of mussel ﬁltration. This
regression explained 64% of the variation in C. dubia numbers. The multiple regression
using both mussel size and density as independent variables explained even more of the
variation (82%) in population densities. Mussel size explained a larger percentage of this
variation than did mussel density because of the higher ﬁltration capacity of the larger
mussels. ’

The percentage of C. dubia with eggs and the average lipid-ovary-egg (LOE)
score both decreased with increased mussel ﬁltration capacity (Table 8). Mean LOE
scores began to decrease when mussel ﬁltration reached 0.12 m3/m2/d and reproduction
appeared to be affected at ﬁltration capacities of 0.25 m3/m2/d and higher. When each of
these variables were regressed separately on mussel ﬁltration capacity, both regressions
were highly signiﬁcant at p < 0.01 and explained 44% (LOE score) or 57% (percent with

young) of the observed variation, respectivelyf The signiﬁcant negative slopes of these

regressions indicated that the average nutritional state and the reproductive capacity of

 

 

 

 

 

 

 

 

 

 

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Figure 7. Ceriodaphnia dubia population size when cultured in the presence of a
range of zebra mussel ﬁltration capacities (top) and the regression
(with 95% C .I.) based on the log of these abundances (bottom).

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45
C. dubia populations were signiﬁcantly reduced by increasing levels of mussel ﬁltration.

These decreases, in turn, resulted in the much lower densities of C. dubia cultured in the
presence of high levels of mussel ﬁltration.

4. Filtration Capacities

The potential for competition between wetland Cladocera and zebra mussels was
also investigated by comparing the ﬁltration capacities of these two groups. The four most
abundant and common ﬁlter-feeding Cladocera were Ceriodaphm’a dubia, Chydorus spp.,
Bosmina longirostris, and Sida crystallina. In the oﬂ‘shore area, Bosmina Iongirostris had
yearly abundance peaks of 10,000 to 100,000/m3 in May or June, but was more commonly
between 100 and 1000/m3 (Figure 8). Ceriodaphnia dubia typically reached densities of
100 to 1000/m3 with a three year peak of 30,000/m3 in June 1994. Sida crystallina, one of
the largest Cladocera in the wetland, usually had highest concentrations from June through
August, reaching 30,000 to 50,000/m3 each year. Chydorus spp. reached their greatest
concentrations in the spring or fall with densities approaching 100,000/m3. Typical
abundances were between 1000 and 10,000/m3.

Filtration capacities of these species were calculated based on their densities in the
offshore area. The total theoretical ﬁltration capacity of the four cladoceran ﬁlter feeders
ranged from 0 to 1.5 m3/m2/d (Figure 8). Zebra mussel ﬁltration capacity reached 0.04
m3/m2/d in late August 1993 and 0.1 m3/m2/d in September 1994 (Figure 8). Mussel
ﬁltration capacity was much lower in 1995 and never exceeded 0.005 m3/m2/d. Thus, the
maximum capacity of the four cladoceran species was 15 times greater than the maximum

capacity calculated for D. polymorpha. In fact, cladoceran ﬁltration capacity was greater

46

Figure 8. Top: Mean densities i 1 standard error of selected Cladocera in the bayward
area of the coastal marsh. Bottom: Filtration capacity of four species of
Cladocera and zebra mussels and the percent of the marsh water column that
each group could ﬁlter per day. In all graphs the Y-axis is a log scale.

47

 

     

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48
than that of mussels on almost all dates, the only exceptions occurring in the fall of 1993

and 1994. Calculations based on the average water depth in this area indicated that these
four Cladocera were probably able to ﬁlter as much or more of the outer marsh per day as
the zebra mussels (Figure 8). In June 1994 they could have ﬁltered the entire water
column almost 2 times per day. The highest mussel ﬁltration (in August and September of
1994) would have only ﬁltered one sixth of the water column per day, and this capacity
was not routinely achieved by the mussels. More commonly, the mussel population would
have been able to ﬁlter 1 to 10% of the marsh water column per day in 1993 and 1994 and
less than 1% per day in 1995.

5. In Situ Effects of Mussels on Cladocera

To determine whether this level of mussel ﬁltration had an effect on the wetland
cladoceran community, I compared species richness, total abundance, and the abundance
of the four abundant ﬁltering species before and aﬁer mussels colonized the wetland.
There was no difference in the number of cladoceran taxa or the total abundance of the
Cladocera in the offshore area between the late summer and fall of the two years, 1990
and 1994 (Table 10). In the offshore area abundances of Bosmina longirostris were higher
in 1994 and abundances of Sida mystallina were lower. However, these same changes
also occurred in the nearshore area, indicating that some factor other than zebra mussel
presence was probably the cause. These observations were statistically conﬁrmed using
BACI analysis. None of the BACI comparisons were signiﬁcant for the number of taxa,
total abundance, or individual abundances of the ﬁlterers Ceriodaphm'a dubia, Chydorus

spp., Bosmina longirostris, and Sida crystallina. This conservative statistic controlled for

49

 

 

 

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50
any changes occurring in both areas of the marsh by giving a signiﬁcant rating only to

large changes which occurred in only the impaCted area.
Discussion

The densities that Dreissena polymorpha can reach in lake littoral zones (Brady et
al. 1995, Lewandowski 1983) suggests the potential for them to affect the zooplankton
community in these areas. Zebra mussels have been demonstrated to be very effective in
removing small particles from the plankton and depositing them in the sediment
(Stanczykowska 1977). Thus, this food resource becomes unavailable to planktonic ﬁlter
feeders even if it is not eﬂiciently assimilated by the mussels (Sprung and Rose 1988). In
addition zOOpIankton may themselves make up some fraction of the particulate matter
consumed by the mussels (Shevtsova et al. 1986).

1. Mussel Predation on Zooplankton

l

{\The presence of zooplankton remains in the fecal material of zebra mussels
collected from the marsh suggested that mussels were consuming live zooplankton,
particularly the smaller, weak-swimming taxa such as rotifers and Bosmina longirostris.
Other researchers have noted that small, weak-swimming zooplankton are vulnerable to
Dreissena polymorpha ﬁltration (MacIsaac et al. 1991, Shevtsova et al. 1986). Rotifers
were the most abundant zooplankton in the 60 - 125 um size fraction of the wetland
community (Figure 6). They are considered weak swimmers which are not capable of
escaping from mussel ﬁltration currents (MacIsaac et a1. 1991). One of the smallest

Cladocera present in the marsh, Bosmina longirostris, is also considered to be a weak

swimmer (MacIsaac et al. 1991). The vulnerability of these zooplankton to zebra mussel

51
ﬁltration was conﬁrmed in short-term experiments in which one or two clumps of mussels

were able to reduce the abundance of rotifers and small B. Iongirostris by 55 to 80% in
only 1.5 hr. Copepod nauplii and slightly larger B. longirostris (126 - 250 um) were much
less vulnerable to mussel predation, probably because they possess better swimming
abilities than do rotifers of comparable size (MacIsaac et a1. 1991). No zooplankton larger
than 250 um were affected. This may reﬂect both size selectivity on the part of the
mussels (Ten Winkel and Davids 1982) and/or stronger escape swimming by the larger
zooplankton.

These experiments exposed the zooplankton to very high levels of mussel
ﬁltration: mussels in a single clump had the capacity to completely ﬁlter the water twice
during the 90 min experiment, while two clumps of mussels could ﬁlter all the water four
times. In similar experiments Shevtsova et al. (1986) found that D. polymorpha 1.5-2.0
cm could remove 15% of juvenile cyclopoids, 63-65% of B. longirostris, and 90% of the
dominant rotifer in 12 hr while not affecting larger species such as Chydorus sphaericus
and Sida crystallina. MacIsaac et al. (1991) found that 2.25 cm mussels could
signiﬁcantly reduce the densities of several species of rotifers. They did not ﬁnd any
evidence of mussel consumption of B. longirostris, but the individuals they used were >
250 pm in size.

The vulnerability of rotifers and small B. longirostris to mussel ﬁltration raised the

—/

[iquestion of whether mussels in the marsh could prey upon these zooplankton to a

H‘

signiﬁcant extent under natural conditions. Predation on rotifers has been suggested for

western Lake Erie by MacIsaac et al. (1992), who determined that a 75% reduction in

52
rotifer densities was likely due to direct predation by dense mussel communities. Mussel

densities in the marsh ranged from 1000 to 55,000/m2 during August of 1994 (Brady et al.
1995). The highest density was very close to the density of a single mussel clump in the
ﬁltration vulnerability experiments (48,000/m2). The marsh population was not comprised
primarily of mussels in clumps, however, as there were an average of < 0.5 clumps/m2
(Brady et al. 1995). Instead, most mussels were attached to stems of the dominant
emergent plant, three-square bulrush (Scirpus americanus). In addition, the mussels on
bulrush stems were quite small, most < 6 mm (Brady et al. 1995). At least 10% of mussels
in clumps, by contrast, had shell lengths 2 1 cm. Thus, the highest theoretical ﬁltration
capacity for the marsh population was only 0.1 m3/m2/d, much lower than the 2.74
m3/m2/d for a single clump in the experiment. Had the sizes of mussels been similar to the
size distribution found in clumps, their ﬁltration capacity would have been 10 times
greater.

The ﬁltration capacity for the marsh mussel population was more closely
approximated by the third ﬁltration vulnerability experiment. This experiment used mussels
attached to bulrush stems at densities similar to those occurring in the wetland, leading to
an average ﬁltration capacity of 0.17 m3/m2/d. Although these smaller mussels were
allowed to ﬁlter twice as long as the mussels in clumps, they would only have been able to
ﬁlter about 1/3 of the water in the chamber by the end of the experiment. The much lower
ﬁltration capacity of these less numerous and smaller mussels was still greater than the
highest capacity calculated for the marsh population. This mussel density did not cause

signiﬁcant reductions in the abundances of any zooplankton group. These results indicated

53
that zebra mussels were unlikely to reduce the population size of even the vulnerable

marsh rotifer community by direct predation, given the size structure and densities at
which mussels occurred in the wetland.

2. Mussel Competition with Cladocera

Another mode of interaction between D. polymorpha and zooplankton is through
competition for food. This potential has been suggested by evidence of phytoplankton
reduction by zebra mussels in other areas around the Great Lakes. For example, zebra
mussels in western Lake Erie caused an 80% reduction in planktonic diatoms (Holland-
Beeton 1990) and a 50% decrease in chlorophyll a concentrations (Leach 1992), moving
the lake into an oligotrophic classiﬁcation based on its chlorophyll a levels}-

I investigated mussel competition with a ﬁltering Cladocera by culturing
Ceriodaphnia dubia in the presence of various sizes and densities of mussels.
Ceriodaphnia dubia neonates are too large (> 300 pm) to be ﬁltered from the water by
zebra mussels, removing predation as a possible factor in the experiment. Increasing levels
of mussel ﬁltration caused C. dubia population sizes to be signiﬁcantly reduced, indicating
competition between the zooplanktors and zebra mussels. An alternative explanation is
that C. dubia populations were repressed by some substance released by the mussels,
representing a toxic effect of mussels on the zooplankton. Ammonia is the most likely
substance that could cause the observed density-dependent effect. However, ammonia
levels remained s 0.05 mg/L, well below the level of 2 mg/L that has been shown to cause
reproductive impairment in C. dubia (Nimmo et al. 1989).?! Thus, competition for food

between mussels and C. dubia was the most likely cause of the signiﬁcant decrease in '

54
population density with increasing exposure to mussels. The large decrease in nutritional

status of C. dubia with increasing exposure to mussel ﬁltration indicates increasing food
limitation for these cladoceran populations. These C. dubia populations also exhibited
much reduced reproduction as mussel ﬁltration capacity increased, indicating that food
limitation was severe enough to greatly limit the ability of C. dubia to produce eggs.
Taken together, the decreased survivorship, nutritional status, and reproduction of C.

dubia indicates they were losing in the competition with zebra mussels for food. I;
The laboratory results indicating competition between zebra mussels and large
ﬁlterers such as Ceriodaphnia dubia were not supported by ﬁeld observations. A
comparison of the densities and community composition of cladoceran ﬁlter-feeders
before and after mussel colonization failed to yield any evidence of effects attributable to
the invasion, perhaps because of the high variability associated with the ﬁeld observations.
An alternative explanation, however, is that mussel ﬁltration in the marsh was not
great enough to have an observable effect on the Cladocera. The small size and relatively
low numbers of mussels in the wetland (Brady et al. 1995) caused mussel ﬁltration
capacities to be low, rarely reaching 0.1 m3/m2/d. This is just below the level of ﬁltration at
which C. dubia abundances, nutritional status, and reproduction began to be reduced in
the microcosm experiment. Instead, the ﬁltration capacity of the four dominant cladoceran
ﬁlterers equaled or exceeded that of the zebra mussels on most dates. At their greatest
density, zebra mussels could only ﬁlter one sixth of the bayward section of the marsh per

day, while these four Cladocera had the capacity to ﬁlter at least half of the water column

per day on several occasions. In many of the offshore areas of the Great Lakes the

55
opposite result has been found, with mussels representing a ﬁltration capacity many times

greater than that of the zooplankton and capable of ﬁltering the water column many times
over during a single day (MacIsaac et al. 1992). For example, offshore colonies of mussels
in inner Saginaw Bay had the capacity to ﬁlter all of the water in less than a day in 1992
(Fanslow et al. 1995), while pelagic zooplankton required 37 days to ﬁlter the water
column (Bridgeman et al. 1995). In contrast, marsh mussels required 17 to 70 days to
ﬁlter the water column in 1993 and 14 to 196 days to accomplish this same task in 1995.
Summary and Conclusions

Zebra mussels have the capacity to both prey upon and compete with zooplankton.
The presence of zooplankton exoskeletons within the fecal material of zebra mussels
collected from a Saginaw Bay coastal emergent marsh suggested that these mussels were
consuming live zooplankton. Experiments to assess the vulnerability of wetland
zooplankton to mussel predation demonstrated that the ﬁltration capacities of high
densities of mussel clumps (2.74 to 5.6 m3/m2/d) could remove up to 80% of small
rotifers and 73% of small Bosmina longirostris. However, the mussel communities
naturally occurring in the wetland primarily consisted of mussels < 1 cm which were
attached to bulrush stems. At these lower ﬁltration capacities (0.17 m3/m2/d) more
representative of the wetland population, there were no signiﬁcant decreases in any
zooplankton taxa. These results suggest that while mussels are capable of consuming
small, weak-swimming zooplankton, the existing wetland mussel community will exert

only minimal predatory pressure on the zooplankton.

56
The potential for mussels to compete with wetland ﬁlter feeders was investigated

by culturing Ceriodaphnia dubia with zebra mussels across a range of ﬁltration capacities.
Regressions indicated that C. dubia population densities, reproduction, and average
nutritional state were all signiﬁcantly reduced with increasing levels of zebra mussel
ﬁltration. These negative effects of mussel competition with C. dubia began to be evident
at mussel ﬁltration capacities of 0.12 to 0.17 m3/m2/d. Thus, even fairly low levels of
mussel ﬁltration were sufficient to induce competition for food between mussels and C.
dubia in the laboratory.

However, comparisons of the cladoceran community before and after mussels
colonized this coastal wetland showed no evidence of changes attributable to the invasion.
Species richness, total abundance, and the densities of four common species of ﬁltering
Cladocera were not different after mussels colonized the bayward area of the marsh. This
was probably because the ﬁltration capacity of the marsh mussel community was always
lower than the levels at which competitive effects became apparent under experimental
conditions. Instead, the combined ﬁltration capacity of just four cladoceran species was
almost always greater than that of the mussels.

These results indicate that the mussel population in this Saginaw Bay coastal marsh
was having neither a large predatory nor a large competitive effect on the wetland
zooplankton community. Mussel densities and ﬁltration capacities would probably have to
be 10 to 100 times greater than those seen thus far before effects on the zooplankton

would become noticeable.

CHAPTER THREE

EFFECTS ON MACROINVERTEBRATES

Introduction

Zebra mussels (Dreissena polymorpha Pallas) have altered the way in which
energy is transferred through the food web in many of the areas they have colonized
(MacIsaac et al. 1992, Mackie 1991). In some instances researchers have been able to
demonstrate that this has caused fairly substantial changes in the macroinvertebrate
community. For example, benthic detritivores such as oligochaetes, chironomids, and
amphipods, have been shown to increase (Dermott et al. 1993, Griﬁiths 1993, Stewart
and Haynes 1994). These studies have typically been conducted in the offshore areas of
lakes where zebra mussels form large shoals on the bottom substrate. Young mussels,
however, oﬁen settle onto the vegetation in lake littoral areas, sometimes reaching high
densities (Lewandowski 1982, 1983). Because these littoral zone studies were conducted
in Europe long aﬁer zebra mussel colonization, researchers were unable to investigate
whether zebra mussels had changed the macroinvertebrate community of these areas.

The macroinvertebrates of coastal wetlands around the Great Lakes may provide
crucial food resources to many Great Lakes ﬁsh, waterfowl, and shorebirds. Fifty-one
species of ﬁsh are associated with Lake Huron wetlands (Wilcox 1995). At least 28

species of waterfowl use Lake Huron wetlands for postbreeding foraging and as staging

57

58
areas and migration stopovers (Wilcox 1995). Prince and Flegel (1995) estimated that 16

species of avifauna forage in emergent marshes while 9 species use them for breeding
habitat. The macroinvertebrate food resources required by these groups are found in
abundance in coastal wetlands. Duffy er al. (1991) reported invertebrate densities of
19,3OO/m2 in northern Lake Huron wetlands, while Brady (1992) reported an estimated
biomass of 3-4 g/m2 in Saginaw Bay coastal marshes. Macroinvertebrates play an
additional important role in these ecosystems by helping to process the abundant detrital
matter which accumulates (Krieger and Klarer 1992). Given the importance of this
invertebrate community and the fact that so few coastal wetlands remain around the Great
Lakes (Krieger et al. 1992), major changes in the ﬁmctioning of these ecosystems could
have far-reaching impacts.

1 completed a characterization of the macroinvertebrate community in a Great
Lakes coastal marsh in 1990 (Brady 1992), just before the area was colonized by zebra
mussels in 1991. This dataset provided the opportunity to examine the impacts that this
large ﬁlter feeder might have on this community. Because other researchers (Grifﬁths
1993, Stewart and Haynes 1994) have reported increases in some benthic invertebrates, I
hypothesized that detritivores would increase in abundance in the area colonized by
mussels. An additional hypothesis was that there would be changes in the epiphytic
invertebrate community due to the attachment of mussels to the wetland vegetation.
Methods

The study site was located in a large wetland complex that extended along the

southeastern shore of Saginaw Bay, Lake Huron, Michigan (Figure 9). This location was

59

 

 

D
6‘

Saginaw Bay

 

 

 

Figure 9. Location of the study site and sampling transect in Saginaw Bay,
Lake Huron.

6O .
chosen because the macroinvertebrates of this area were studied in 1990 (Brady 1992),

before zebra mussels had colonized the emergent marsh. Emergent vegetation, principally
three-square bulrush (Scirpus americanus Pers.) extended approximately 500 m offshore.
The marsh substrate was predominantly sand. Water depth gradually increased bayward,
reaching 75 to 125 cm at the bayward edge of the emergent zone.

The macroinvertebrate community was sampled in 1993, 1994, and 1995 in the
same area using the same methods as were used in 1990 to ensure that the data would be
comparable (Brady 1992). In both years all samples were collected along a 400 m transect
which extended from near shore (100 m) to the bayward edge of the emergent zone (500
m; Figure 9). Epiphytic and benthic invertebrates were sampled every 100 m along the
transect once a month ﬁom May through November of each year. Epiphytic invertebrates
were collected with a modiﬁed Gerking sampler (Mittelbach 1981). This sampler consisted
of a 21.5 cm diameter Plexiglas tube with 250 um mesh on one end and sliding doors on
the other. The sampler was designed to enclose aquatic vegetation, the surrounding water
column, and associated littoral invertebrates. The entire length of the water column ﬁ'om
surface to bottom was included in each sample. Benthic invertebrates were sampled using
a 4.5 cm diameter plexiglas tube which was used to collect a 15 cm long sediment core.
One sample was taken with the modiﬁed Gerking sampler and two with the coring device
at each of the ﬁve stations along the transect on each sampling date. The paired core
samples were pooled for analysis.

Large vegetation was scrubbed, then examined with the unaided eye and any

remaining invertebrates removed. These invertebrates were added to the rest of the

61
Gerking sample. The Gerking sample and the entire contents of theisediment cores were

preserved separately in 95% ethanol containing rose bengal dye (Mason and Yevich
1967). Gerking samples were subsampled by dividing the sample into 6 equal parts using a
calibrated box subsampling device. Sediment cores were sugar ﬂoated (Anderson 1959)
then subsampled. One sixth of each sample was examined under 10x magniﬁcation for
invertebrates. Invertebrate identiﬁcation was based on Merritt and Cummins (1984),
Thorp and Covich (1991), and Simpson and Bode (1980).

It was previously determined that zebra mussels only became abundant in the
bayward 250 m of the marsh (Brady et a1. 1995). Thus, samples collected at 400 and 500
m along the transect were used to investigate changes occurring after zebra mussels
became part of the community. The macroinvertebrates in this offshore area of the marsh
(n=2/date) were compared before (1990) and after (1994) zebra mussels colonized the
emergent vegetation. The year 1994 was chosen as the comparison year because zebra
mussels reached high densities in the bayward area of the wetland in 1994 (Brady et al.
1995) and because the transect that year best matched the 1990 transect location. Only
samples from August through November were used for each of the years because these
were the only months in 1994 during which zebra mussels were present in fairly high
numbers (Brady er al. 1995). The epiphytic and benthic communities were considered to
be separate and discrete entities and were analyzed separately. For each community, taxa
richness and the abundances of species making up at least 10% of total community

abundance were compared between years.

62
Because the nearshore area was not colonized by mussels, I considered this area to

be unimpacted by the invasion. This allowed me to conﬁrm changes seen in the before-
aﬁer community comparison using a fairly conservative statistic, BACI analysis (Stewart-
Oaten et al. 1986). BACI analyses are conservative because they compare the variability
between the control and impact areas before and after the impact, thus controlling for
changes that have occurred in both areas and should not be considered a result of the
impact. Samples considered to be from the “control” area were those collected at the 100
m and 200 m points along the transect (Figure 9).
Results and Discussion

The earlier research in this Saginaw Bay coastal wetland documented 54 insect
taxa, many of them Chironomidae, and 11 other macroinvertebrate groups (Brady 1992).
These invertebrates reached abundances approaching 50,000/m2 in both epiphytic and
benthic communities (Brady 1992). In all years, the epiphytic community primarily
consisted of chironomid larvae, larval Ephemeroptera, oligochaetes in the family Naididae,
amphipods and isopods. The benthic community was made up of chironomid and mayﬂy
larvae, both naidid and tubiﬁcid oligochaetes, nematodes, amphipods and isopods.

Abundance trends over time were observed for some of these taxa. Chironornid
larvae in the tribe Tanytarsini were more abundant in the benthos than on plant stems in
the offshore area in 1990 (Figure 10). This trend somewhat reversed in 1994 when
epiphytic densities were greater than benthic abundances. Overall, larval densities in the
benthos were lower in 1993 through 1995 than they were in 1990. Trends in the

abundance of other larval chironomids were not particularly obvious, although benthic

63

Figure 10. Mean densities i 1 standard error of epiphytic and benthic chironomid
larvae from nearshore and offshore areas of a coastal marsh.

64

l

l

l

l

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Epiphytic Tanytarsini larvae ,

Benthic Tanytarsini larvae

 

mxjﬁrﬁ 14 J1 1.; ﬂéjﬂé mjm4

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1995

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1990

  

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1995

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65 .
densities appeared slightly higher in 1990 than in subsequent years (Figure 10). There was

no apparent trend in the abundances of epiphytic naidid oligochaetes (Figure 11).
Densities of benthic Naididae were lower in 1995 than they had been in preceding years.
Tubiﬁcid oligochaetes were primarily benthic; their densities were high in the offshore area
of the marsh in 1994 (Figure 11). They also had high densities in the nearshore area in the
fall of 1993. Benthic nematodes were generally less abundant in 1993 through 1995 than
they were in 1990 (Figure 11).

Samples collected in the late summer and fall (August through November) of 1990
and 1994 were chosen for a comparison of the invertebrate community before and after
zebra mussel colonization. This decision was based on zebra mussel densities ﬁ'om
samples collected separately and on the ability to match sampling sites between 1990 and
1994. The choice was made before data on the macroinvertebrate community were
analyzed to preclude these results ﬁom inﬂuencing the decision.

A comparison of the communities in each habitat, epiphytic and benthic, between
the nearshore and offshore areas of the wetland revealed more similarities than differences.
"if? most noticeable differences were that larval Tanytarsini were particularly abundant in
the bayward area, and amphipods, isopods, and ephemeropteran larvae were more
abundant nearshore (Figure 12).

Differences in the two nearshore habitats between 1990 and 1994 were compared
to changes that had occurred in the two communities in the offshore area over this same
time period. The number of taxa and community composition in both nearshore habitats

..——/

were almost identical between years (Figure 12). There was an increase in the abundance

66

Figure 11. Mean densities i 1 standard error of epiphytic and benthic oligochaetes
and nematodes from nearshore and offshore areas of a coastal marsh.

67

 

 

 

 

 

 

 

 

       
    

     

 

  

       

  

 

 

 

 

 

 

 

 

 

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1995

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1990

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68

Epiphytic Community

 

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1990
Offshore

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I Other invertebrates
Dreissena polymorpha
Ill Amphipoda & Isopoda
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Dreissena polymorpha
llll Amphipoda & Isopoda
E Nematoda

Tubiﬁcidae

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I Tanytarsini
Ephemeroptera

 

Figure 12. Community composition of the epiphytic (top) and benthic (bottom)

macroinvertebrate communities in the nearshore and oﬂ‘shore marsh areas.
Each bar represents 2 samples per month for Aug.- Nov. for an n=8.

 

 

69
of amphipods and isopods, a decrease in the numbers of epiphytic naidids, and a switch in

chironomid larvae from higher abundance in the sediment to greater abundance on stems.
In the offshore area there was no change in taxa richness in either community. In the
epiphytic community chironomid larvae and naidid oligochaetes both increased in
abundance. Zebra mussels only comprised about 5% of this community in 1994.
Chironomid larval abundances decreased in the sediment between 1990 and 1994 and
tubiﬁcid densities increased (Figure 12). Zebra mussels made up about 4% of the benthic
community in 1994.

Some of the observed changes occurred in both areas of the wetland irregardless
of the presence of zebra mussels. Because of this, BACI analysis was used to provide a
conservative indication of the signiﬁcant changes that occurred only in the “impacted”
area in conjunction with zebra mussel colonization. BACI analyses indicated no signiﬁcant
differences for taxa richness or the abundances of most groups in the offshore area of the
wetland following zebra mussel colonization (Tables 11 and 12). There was a signiﬁcant
increase in the abundance of epiphytic larval Tanytarsini (p = 0.03) and a marginally
signiﬁcant decrease in their abundances in the benthos (p = 0.08) (Figure 13). The change
in tanytarsinid density between the two communities was similar: 12,000/m2 more in the
vegetation and 9000/m2 less in the sediments.'Other researchers have found increases in
chironomid larvae, including Tanytarsini (Stewart and Haynes 1994), in association with
zebra mussels. In an elegant series of experiments, Stewart (1996) demonstrated that
chironomid larvae were responding to the presence and activity of living mussels rather

than simply to the increased complexity created by their shells. Many larval tanytarsinids

70

Table 11. Means : 1 standard error (n=8) of the number of macroinvertebrate taxa and
abundances of the dominant epiphytic groups in both areas of the marsh for

August through November of each year.-

 

 

Nearshore Offshore
1990 1994 1990 1994
Number oftaxa 21.5 :2.0 18.0:0.9 15.0: 1.5 14.8 :1.3
Chironomidae 1393 : 446 2064 : 573 2245 : 1406 4505 : 1516
(other)

Tanytarsini 570 : 254 327 : 63 2591 : 1021 14,598 : 7475*
Naididae 3580 : 1774 2114 : 1107 2066 :1102 2819 : 1046
Caenis spp. 3746 : 2843 5034 : 1505 1384 : 242 1736 : 495

 

+ Indicates signiﬁcance at p < 0.1 by BACI analysis.
* Indicates signiﬁcance at p < 0.05 by BACI analysis.

Table 12. Means : 1 standard error (n=8) of the number of macroinvertebrate taxa and
abundances of the dominant benthic groups in both areas of the marsh for

August through November of each year.

 

 

Nearshore Oﬂ‘shore
1990 1994 1990 1994
Number oftaxa 11.8 : 0.8 11.8 : 0.9 7.5 :1.7 8.3 : 1.3
Chironomidae 5076 : 1871 2176 : 684 9323 : 4234 2176 : 764
(other)

Tanytarsini 4248 : 642 2382 : 818 11,292 : 4278 2279 : 1489+
Naididae 3833 i 1212 4765 : 1480 5076 : 4665 3644 : 1016
Tubiﬁcidae 2072 : 1465 3730 : 1122 622 : 493 4662 : 1236*
Nematoda 7044 : 2785 4455 : 1378 6733 : 2782 6526 : 1545
Caenis spp. 5801 i 3142 7148 : 2340 1140 i 459 1036 i 766

 

+ Indicates signiﬁcance at p < 0.1 by BACI analysis.
* Indicates signiﬁcance at p < 0.05 by BACI analysis.

71

 

 

 

 

 

 

20 ‘ Epiphytic Tanytarsini
10 -
O ,__.T.__, r
90 94
N 20 -a

Benthic Tanytarsini

—-——l

 

Thousands per m
S
l

 

 

 

 

 

 

 

 

 

0 I * .

90 90

 

- Benthic Tubifrcidae

94 94
i l t
0 . l—L—l

l
90 9O
Near sh ore Offshore

 

 

 

 

 

 

 

Figure 13. Densities of larval Tanytarsini and Tubiﬁcidae before and after zebra
mussel colonization. Top: Epiphytic Tanytarsini; p= 0.03. Center:
Benthic Tanytarsini; p= 0.08. Bottom: Benthic Tubificidae; p= 0.04.

72
are ﬁlterers, particularly Rheotanytarsus, a dominant genus in the offshore area (Cardinale

et al. submitted). These larvae were the only other macroinvertebrate ﬁlter feeders present
in the wetland prior to the arrival of the zebra mussel. Filtering larvae may be beneﬁting
from the ﬁltration currents created by the mussels. Collector-gathering larvae may be
consuming mussel feces and psuedofeces, a nutritious and digestible food source for larval
chironomids (Izvekova and Lvova-Katchanova 1972).

The only other signiﬁcant change in macroinvertebrates in the offshore area
following mussel colonization was an increase in the densities of tubiﬁcid oligochaetes in
the sediment (p = 0.04) (Figure 13). Grifﬁths (1993) and Stewart and Haynes (1994)
noted increases in oligochaete densities after mussels colonized Lake St. Clair and Lake
Erie. Other researchers (Griﬂiths 1993, Izvekova and Lvova-Katchanova 1972, Stewart
and Haynes 1994) have indicated that these detritivores respond positively to the presence
of mussel fecal and pseudofecal material. The organic content of the sandy sediments in
the offshore area of the marsh, although not measured, may have been fairly low prior to
the arrival of zebra mussels. The addition of mussel fecal and pseudofecal material likely
increased the organic content, providing these detritivores with an additional source of
nutrition and resulting in the observed increases.

,/
f This shift in energy from planktonic to benthic by zebra mussels has been observed

in manywareas of the Great Lakes. The result has been a major alteration of the ecosystem
in Lake St. Clair (Grifﬁths 1993). Abundances of benthic detritivores have increased,

water clarity has increased greatly, leading to highly expanded macrophyte cover, and

73
phytoplankton abundances have greatly decreased (Griffiths 1993). This has shifted the

ﬁsh assemblage to a community typical for a littoral zone (Ross 1994).

As hypothesized, there were increases in benthic detritivores (tubiﬁcid
oligochaetes) aﬁer mussels invaded the Saginaw Bay wetland. There was also a change in
the epiphytic community with the apparent habitat shiﬁ of tanytarsinid larvae from benthic
to epiphytic. The changes observed in the wetland were not as large nor as encompassing
as those seen in Lake St. Clair or western Lake Erie (Dermott et al. 1993). This is not
surprising because zebra mussels densities were much lower in the marsh than the 300,000
to 1 million/m2 reported for these other areas (Dermott et al. 1993, Grifﬁths 1993). In
addition the mussel population in the marsh was predominantly composed of mussels < 2
mm, resulting in much lower ﬁltration capacities than those of similar densities of larger
mussels. This lower level of impact is encouraging given the importance of coastal wetland

food webs to Great Lakes ﬁsh and waterfowl.

SUMMARY AND CONCLUSIONS

Zebra mussels (Dreissena polymorpha) colonized a Saginaw Bay coastal wetland
in 1991 and were studied in 1993 through 1995. The marsh mussel population consisted
primarily of mussels attached to stems of the dominant emergent plant, three-square
bulrush (Scirpus americanus). Much lower densities of mussels existed as substrate-
independent clumps resting on the sediment, but these clusters contained most of the
reproductive mussels in the marsh. The population varied both seasonally and spatially in
1993 and 1994. Mussel densities were low in the spring and early summer (300/m2),
represented only by the mussel clumps that had survived the winter in the bayward half of
the wetland where the water was deep enough for them to avoid ice scour. Abundances
did not increase until recruitment of young-of-the-year mussels onto bulrush stems in
August. Recruitment only occurred in the outer 250 m of the 500 m wide emergent zone
because there was little water movement to carry veligers into the nearshore area. Highest
densities of larval and juvenile mussels were found between 300 and 400 m from shore,
indicating that the substrate-independent clumps of mussels in the marsh rather than
deeper water populations were serving as the source of the larvae. Mussel densities
reached lOO/bulrush stem with areal densities as high as 55,000/m2 near the center of the
marsh in August 1994. These areas experienced high losses by September, however, and

densities were much lower in the fall. Over the winter most of the remaining mussels on

74

75
stems apparently succumbed due to senescence of the vegetation and ice scour. Thus, the

marsh mussel population consisted primarily of mussels 2 mm and smaller that were
abundant only in the bayward half of the wetland ﬁom August through November of each
year.

I investigated whether this population was large enough to have an impact on
wetland zooplankton or macroinvertebrates. The ability of these mussels to prey upon
wetland zooplankton was investigated both observationally and experimentally.
Observation of the remains of rotifers, Bosmina longirostris, copepod nauplii, and other
zooplankton in the fecal material of wetland mussels suggested that these groups were
experiencing predation. This was experimentally tested in short term experiments. Rotifers
smaller than 250 um and B. longirostris smaller than 125 um were signiﬁcantly reduced by
just 90 min of ﬁltration by zebra mussel clumps. Larger B. longirostris and taxa that were
stronger swimmers, such as copepod nauplii, were not affected by this ﬁltration. Mussels
attached to bulrush stems represented a much lower ﬁltration capacity than that of mussel
clumps, but one that was more representative of the wetland population. Mussels on
bulrush stems did not signiﬁcantly reduce the abundances of any zooplankton taxa during
180 min of exposure.

The potential for competition between zebra mussels and ﬁltering Cladocera was
also tested experimentally. A common wetland species, Ceriodaphm’a dubia, was cultured
with zebra mussels for 14 days. Population densities of C. dubia decreased signiﬁcantly
with increasing levels of mussel ﬁltration. The reproductive and nutritional status of these

populations showed signiﬁcant reduction with greater mussel ﬁltration capacities. The

76
effects of mussel competition began to be apparent at ﬁltration capacities of O. 12 to O. 17

m3/m2/d in this experiment. These levels were higher than the highest ﬁltration capacities
calculated for marsh mussel population. There was no evidence that wetland mussels were
having a competitive effect on the marsh Cladocera. Comparisons of cladoceran species
richness, total abundance, and the abundance of common taxa before and aﬁer mussel
colonization showed no apparent changes attributable to the invasion. Instead, the
combined calculated ﬁltration capacities of the four abundant ﬁltering Cladocera were
usually higher than the ﬁltration capacity of the mussel population.

The epiphytic and benthic macroinvertebrate communities were compared before
and after zebra mussel colonization of the marsh. BACI analyses indicated several changes
potentially attributable to zebra mussels. Larval chironomids in the tribe Tanytarsini were
signiﬁcantly more abundant on bulrush stems after mussels invaded the wetland. This was
accompanied by an almost signiﬁcant decrease in the densities of these larvae in the
sediments. The magnitude of both changes was similar and resulted in no overall change in
the numbers of these larvae in the marsh. These larvae may have beneﬁted ﬁom ﬁltration
currents generated by the mussels attached to bulrush stems. These currents would have
increased water circulation, thus bringing additional food to the larvae. It is also possible
that some of the larvae may have been utilizing the fecal material of mussels as a source of
food. Another difference occurring in conjunction with zebra mussel colonization was a
signiﬁcant increase in tubiﬁcid oligochaete abundance in the sediment, perhaps due to the

use of mussel feces and pseudofeces as an additional source of nutrition.

77
In summary, zebra mussels were able to maintain a year-round reproducing

population in the offshore half of this coastal emergent marsh. Their densities were low
during most of the year, and high abundances consisted almost entirely of very small
mussels. The ﬁltration capacity of this population was insufﬁcient to reduce the
populations of even the vulnerable rotifer community through predation under
experimental conditions. Although competition between Cladocera and mussels was
demonstrated in the laboratory, there was no evidence of change in the wetland cladoceran
community with the arrival of the mussels. Only two macroinvertebrate groups exhibited
any changes potentially related to the zebra mussel invasion. Larval tanytarsinid
chironomids shifted from a predominantly benthic to a primarily epiphytic habitat in
conjunction with zebra mussel colonization. Benthic tubiﬁcids signiﬁcantly increased in
abundance in the sediment, perhaps beneﬁting from the input of mussel feces and
pseudofeces. If the mussel population in this wetland is representative of populations in
shallow coastal marshes, it appears unlikely that they will cause dramatic changes such as

those seen in some of the open water areas around the Great Lakes.

LITERATURE CITED

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