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Effects of Hydrology on Unionids (Unionidae) and Zebra Mussels (Dreissenidae) in a Lake Erie Coastal Wetland Author(s): Richard Bowers and Ferenc A. de Szalay Source: American Midland Naturalist, Vol. 151, No. 2 (Apr., 2004), pp. 286-300Published by: The University of Notre DameStable URL: http://www.jstor.org/stable/3566746Accessed: 25-06-2015 20:03 UTC

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Am. Midl. Nat. 151:286-300

Effects of Hydrology on Unionids (Unionidae) and Zebra Mussels (Dreissenidae) in a Lake Erie Coastal Wetland

RICHARD BOWERS1 AND FERENC A. DE SZALAY2 Department of Biological Sciences, Kent State University, Kent, Ohio 44242

ABsTRAcT.-Infestation by introduced zebra mussels has extirpated native unionids in many Great Lake habitats. Shallow areas in coastal wetlands are intermittently dewatered by seiches and seasonal water level changes, and we examined how water level fluctuations and sediment characteristics affected interactions among unionids and zebra mussels in a Lake Erie coastal marsh. In 2001 we sampled unionid distributions and measured zebra mussel colonization on PVC plates at 1 cm, 18 cm and >35 cm water depths. We found a diverse unionid community (15 species) with many juvenile unionids. Unionid densities (0.01 unionids/m2) were

comparable to other coastal wetlands, but are lower than reported in offshore areas before zebra mussels were introduced. Zebra mussels colonized plates at >3000 individuals/m2 in some locations. Although >60% of unionids had byssal threads on their shells, >75% of unionids had no attached zebra mussels. Therefore, zebra mussels are colonizing unionids, but are not surviving. Unionid numbers and zebra mussel colonization were low in shallow (1-35 cm) water depths, indicating that water level fluctuations limited their distributions.

Only two species of unionids were collected in 1-17 cm deep areas, and areas that became mudflats in September had almost no unionids. Numbers of zebra mussels and unionids were not correlated with organic content or silt/clay content of the sediments. Habitat characteristics shared by this wetland and other coastal wetlands that are important refuges of unionids include: a hydrological connection with the lake, areas deep enough for unionids to survive low water levels and soft sediments that allow unionid burrowing.

INTRODUCTION

Over 300 species of unionids (Bivalvia: Unionidae) occur in North America, which is the

highest unionid diversity in the world (Bogan, 1993; Bogan and Cummings, 2001). Seventy- eight species occur in Ohio, and Herdendorf (1987) lists 35 species in western Lake Erie coastal wetlands and nearshore areas. Unionid populations have declined in the United States since the 1800s from over-harvesting, impoundments, pollution and siltation

(Stansbery, 1970; Bogan, 1993; Brim-Box and Mossa, 1999; Waller et al., 1999). Although unionid populations in Lake Erie were already declining before the 1980s (Nalepa et al., 1991), the introduction of zebra mussels [Bivalvia: Dreissenidae: Dreissena polymorpha (Pallas) ] in 1988 caused sudden dramatic decreases in unionids throughout the Great Lakes (Ricciardi et al., 1996; Ricciardi et al., 1998; Strayer, 1999). As a result of the combined effects of these

factors, over 75% of unionid species are now threatened in the United States, including 49 Ohio species (Williams et al., 1993; Bogan and Cummings, 2001). This indicates that unionids are one of the most endangered group of organisms in North America (Johnson, 2001).

Zebra mussel ecology has been well studied in the Great Lakes since their introduction in the late 1980s (Chase and Bailey, 1999a, b). Zebra mussels spawn in Lake Erie in June to

September when water temperatures are >18 C (Garton and Haag, 1993). Females release

30,000 to 40,000 eggs that are fertilized in the water column and form planktonic larvae

286

1 Corresponding author present address: Edwards-Pitman Environmental, Inc., 1250 Winchester Parkway, Suite 200, Smyrna, Georgia; e-mail: [email protected] 2 e-mail: [email protected]



2004 BOWERS & DE SZALAY: HYDROLOGY AND MUSSELS 287

called veligers (Marsden, 1992). As larval zebra mussels mature, they settle out of the water column and become attached to substrates with proteinaceous strands called byssal threads. Zebra mussels are generally found on hard surfaces because they die if buried in soft substrates (Toczlowski et al., 1999; Karatayev et al., 1998; MacIsaac, 1996) and they are often found attached to unionid shells (Burlakova et al., 2000). Both unionids and zebra mussels filter feed on suspended diatoms and fine particulate organic matter (Thorp and Covich, 1991), and zebra mussels can out-compete unionids for food when they attach to unionids in

large numbers (Strayer and Smith, 1996). Surveys throughout Lake Erie and Lake St. Clair show major declines in unionid

populations after the introduction of zebra mussels (Gillis and Mackie, 1994; Ricciardi et al., 1996; Schloesser et al., 1996; Schloesser and Masteller, 1999). Ricciardi et al. (1998) reported that all unionids in areas with high zebra mussel infestations were extirpated within 4-8 y and

regional extinction rates had increased ten-fold. Therefore, it was surprising when abundant unionid populations were recently discovered in two coastal wetland sites in the lower Great Lakes: Metzger Marsh in western Lake Erie and the St. Clair River delta in Lake St. Clair (Nichols and Amberg, 1999; Zanatta et al., 2002). These sites were termed "refuges" because

they supported diverse species assemblages with low numbers of attached zebra mussels. The reasons why unionids are able to coexist with zebra mussels in these sites are not clear. In

laboratory experiments, attached zebra mussels were killed when unionids burrowed into soft

silt/clay sediments found in coastal wetlands (Nichols and Wilcox, 1997). However, the effects of other physical factors in coastal wetlands on zebra mussel mortality have not been tested.

The Great Lakes are subject to short-term wind-driven water level fluctuations, called seiches, and seasonal water level changes. For example, mean Lake Erie water levels in 2001 peaked in June and decreased 22 cm by December (USACE, 2002). Seiches from strong storms can cause lake levels to change >1 m, and water levels will continue to fluctuate for

days afterwards (Bedford, 1992). Unlike inland wetlands, Great Lake coastal wetlands are connected with the adjacent lake, which causes their water levels to fluctuate with lake levels

(Maynard and Wilcox, 1997). Water level changes affect the vegetation in these marshes (Chow-Fraser et al., 1998), but little is known about how they affect benthic invertebrates (Gathman et al., 1999). We have not found any studies that examined how hydrology affects interactions between zebra mussels and unionids in Great Lake coastal wetlands.

Because unionid numbers are declining throughout the Great Lakes, studies that examine factors that impact unionids in these habitats are important for the preservation and

management of these species. In 2000 shells of 17 unionid species were collected on shorelines of Crane Creek Marsh in western Lake Erie (F. de Szalay, unpubl. data). However, many zebra mussel shells were also found, and it was not known whether live unionids still inhabited this coastal wetland. In summer 2001 we sampled unionids and zebra mussels in Crane Creek Marsh and tested the hypotheses that: (1) unionids still inhabited this wetland and were co-existing with zebra mussels and (2) hydrology and sediment characteristics affected unionid and zebra mussel distributions.

METHODS

Study site.---Crane Creek Marsh (CCM) is part of Ottawa National Wildlife Refuge (Ottawa and Lucas counties, Ohio) which is managed by the U.S. Fish and Wildlife Service. A dike

along Lake Erie protects the marsh from offshore waves, but a permanent opening in the dike connects the marsh to the lake (Fig. 1). The marsh also receives inputs from Crane Creek, which is a third order stream. Crane Creek's 144 km2 watershed is predominantly agricultural or residential (Ohio Department of Transportation, 1987). The 146 ha upstream portion of the wetland is intermittently flooded by seiches and has little unionid habitat



288 THE AMERICAN MIDLAND NATURALIST 151(2)

...ke Erie Stream Enters the lake

?

' "i t

oll Stream Entem 4

0

1 ~Catch per unit effort S00

00~1

[ 0.1-5 N S 5.1 - 10E

0 0.5 1 1.5 Km * 10.1-15 I + 15.1 -64

FIG. 1.-Unionid catch per unit effort and zebra mussel sampling locations in Crane Creek Marsh. Numbered locations are where we sampled zebra mussel colonization: (1) where Crane Creek enters the marsh; (2) in the creek channel 1.5 km away from where Crane Creek enters the marsh; (3) midway towards Lake Erie; and (4) where the marsh opened to Lake Erie. Striped areas were mudflats in September 2001. Map inset shows location of Crane Creek Marsh in Ohio. Note: unionids and mudflats were not sampled in the upstream portion of the wetland

except in the creek channel. The 166 ha downstream portion is mostly shallow open water and has the most potential unionid habitat. Water levels in the downstream portion of the wetland are up to 2 meters, but most areas are <50 cm deep. Benthic sediments are mostly thick deposits of soft mud. Live zebra mussels are abundant on stone rip-rap on dikes

surrounding the marsh. Unionid sampling.-We created a G.I.S. (Global Information Systems) map of CCM from

aerial photographs using ARC View software (ESRI, Redlands, California). We restricted our

sampling effort to the 166 ha downstream area of the wetland because this had the most

potential unionid habitat. Unionid sampling locations were determined by overlaying a grid onto the G.I.S. map using AutoCAD software (Autodesk, San Rafael, California). Each square in the grid was equal to a 50 m X 50 m area of the marsh. The entire grid was divided into sub-

regions that each comprised nine squares in a 3 X 3 arrangement. We randomly selected one

square from each of the sub-regions as a sample plot (77 plots total) and located the plots in the field with a G.P.S. unit (Trimble Geoexplorer3, Sunnyvale, California) (Fig. 1). Plots that were entirely out of the water were rejected. Wooden stakes were used to mark the corners of each 50 m X 50 m sample plot. Sampling was conducted from 10June to 12 August 2001, and teams of 3-6 people conducted tactile searches for 4 person hours per 50 m X 50 m plot. Search time was adjusted according to how much of the plot was in the water to standardize

sampling efforts (i.e., a plot that was one-half out of the water was only sampled for 2 person hours). We manually probed the substrate to locate live unionids and collected them in a mesh bag. Although this method did not give us an exact measure of density (e.g., we

probably missed some small unionids), more accurate methods (e.g., Quadrat and Transect line studies; Smith et al., 2001; Metcalf-Smith et al., 2000) are much more labor intensive and were not feasible due to the size of the marsh.




We identified all unionids in the field, visually checked for the presence of zebra mussel

byssal threads on their shell and counted live attached zebra mussels. Unionid age was estimated by counting annuli, which are the visible growth lines on their shell (Day, 1983; Metcalf-Smith and Green, 1992; Veinott and Cornett, 1995; McCuaig and Green, 1982). We used Cummings and Mayer (1992), Parmalee and Bogan (1998), Watters (1993) and a reference collection from the Cleveland Museum of Natural History to identify the unionids to species. Shells from recently dead animals and live unionids observed outside the

sample plots were also identified to document additional species inhabiting the marsh. All live unionids were released in the field, but shells from recently dead animals were sent to the Cleveland Museum of Natural History and Ohio State University as voucher specimens. Catch

per unit effort was calculated by dividing the number of unionids in each sample plot by the search time to estimate number of unionids collected per person hour. Species richness was determined by counting the number of species collected in each sample plot.

We measured sediment characteristics in sample plots to compare with unionid and zebra mussel numbers. Sediment samples were collected with a PVC pipe (5.1 cm diameter) embedded to a depth of 12 cm at three random locations in each plot. Samples were

homogenized and stored frozen until they were analyzed in the laboratory. We removed two 50-ml subsamples of each sample, dried them to a constant weight for 48 h at 70 C and measured their dry weight. One 50-ml subsample was used to determine percent organic matter by loss on ignition (Blume et al., 1990). For this, the sediments were burned in a muffle furnace at 450 C for 24 h and the inorganic ash that remained was weighed. Percent organic matter (%OM) was calculated as:

% OM = ((dry weight - inorganic ash weight)/dry weight) X 100

We used wet-sieving (Sheldrick, 1984) to measure sediment particle size in the second 50-ml

subsample. We did not do this for all 77 plots because the method is labor intensive. Therefore, 10 sub-samples were randomly chosen for analysis. Sediments were sorted by washing through three nested sieves (ASTM sizes: 4, 40 and 200) that corresponded to

gravel, coarse sand and fine sand, respectively. Material remaining in each sieve was dried at 70 C for 24 h and weighed to determine percent of total for each particle size. The amount of silt/clay was determined by subtracting the combined dry weight of sediments retained in the sieves from the initial sample dry weight.

Water level data downloaded from the National Oceanic and Atmospheric Adminis- tration's (NOAA) internet site (www.co-ops.nos.noaa.gov) showed that 2001 Lake Erie water levels were 24 cm lower than the long-term average recorded from 1918 to 2001. Levels in 2001 were the lowest they had been since 1967, and one-third of the marsh was newly exposed mudflats in the Fall. On 15 September 2001 we used a G.P.S. unit to map the

perimeter of all mudflats and incorporated this information in our G.I.S. map. Zebra mussel colonization.-We measured colonization rates of zebra mussels on PVC plates

(15 cm X 15 cm) that were roughened with sandpaper to create a suitable attachment surface (Marsden, 1992). Because zebra mussels generally settle on surfaces with attached biofilm (i.e., a matrix of bacteria and algae), colonization plates were conditioned for 14 d in 36.8-liter plastic containers filled with filtered marsh water.

On 22 June colonization plates were placed at four locations: (1) where Crane Creek enters the marsh; (2) in the creek channel 1.5 km away from where Crane Creek enters the marsh; (3) in the creek channel 1.1 km away from the mouth of the marsh at Lake Erie and; (4) at the opening of the dike where the marsh connects to Lake Erie (Fig. 1). At each location we placed 12 wooden stakes spaced 1 m apart along a transect. A colonization plate was attached to each stake at each of three water depths: 1 cm, 18 cm and 35 cm measured to




the top of the colonization plates (3 plates per stake). After 2 wk plates were removed and

preserved with ethanol in Ziploc@ bags. Some plates were lost during the 2 wk from wave action, but we recovered 23-32 plates per location. We counted zebra mussels on each plate with a dissecting scope at 20 X magnification and used Marsden (1992) to identify life cycle stages of the larvae.

Water levels.-Water levels in CCM were recorded every 30 min from May-July 2001 with a water level data logger (Model WL 14X, Global Water, Gold River, California). Although unionid sampling continued through August, the logger malfunctioned on 29 July, and no water level data were collected after that date. We estimated water levels after the logger malfunctioned using Lake Erie water levels measured at a nearby United States Geological Survey gauging station (USGS gauging station #9063085, Toledo, Ohio). For this, we

compared USGS data collected from 30 May to 29 July 2001 with data we collected in CCM. Water levels in Lake Erie were closely correlated (R2 = 0.88) with water levels in CCM with a 1.5 h delay. Therefore, data from this gauging station were used to estimate water levels in Crane Creek for the remainder of the sampling season.

Water depths were measured at the deepest point in each sample plot with a meter stick and time and date were recorded. It was necessary to standardize the water depth data because water levels in the marsh fluctuated with seiches and seasonal changes. For this, we set the mean water depths measured inJune at the water level logger as our reference level. Next, we

compared the reference level to the water depth measured at the water level logger at the time when the plot was sampled and added the difference to the depth measured in the plot. For

example, if water depths were 20 cm lower at the water level data logger than the reference level, we added 20 cm to the water depth measured in the plot. We also measured the amount of time that zebra mussel colonization plates were dewatered by comparing water levels at the time when the plates were attached to the wooden stakes with subsequent water level changes.

Statistical analyses.-We grouped unionid data from sample plots found in each of the

following ranges of water levels: 1-17 cm, 18-35 cm and >35 cm. These water depth classes

corresponded with the depths that zebra mussel colonization plates were submerged. This allowed us to compare patterns of unionid distribution and zebra mussel colonization

among water depth. One-way ANOVAs were used to compare unionid catch per unit effort, species richness and numbers of zebra mussels per unionid among water depth classes. Data that were not normally distributed were transformed as loglo (X +1). Two-way ANOVAs were used to compare zebra mussel colonization among water depth classes and sampling locations. All significant (i.e., P < 0.05) ANOVA tests were followed by Tukey's multiple comparison of means tests. A log-likelihood ratio test was used to compare frequencies of unionid species among water depth classes. When the log-likelihood ratio was significant, we subdivided the contingency table to determine which taxa differed from expected frequencies (Zar, 1999). Regression analyses were used to test whether unionid numbers, species richness, number of zebra mussels per unionid and water depths in sample plots were correlated with % silt/clay or % organic matter of sediments.

RESULTS

Sediment characteristics and water levels.--Sediments in the sample plots were predominantly inorganic silt/clay. Percent organic matter ranged from 2-19% and mean ? 1 SE percent sediment organic content was 9.4% 1 0.4. Mean

_ 1 SE percent gravel, coarse sand, fine sand

and silt/clay in the sediments were 3% + 2.4, 5% ? 2.4, 10% _

3.4 and 82% + 6.5, respectively. Water depths were not correlated (P > 0.05) with either percent organic matter (df = 1,75, R2 = 0.003) or % silt/clay (df= 1,8, R2 = 0.285).




ZM Start ZM

StartEn

0.8

A

C 0.2

0 7 Jun 27 Jun 17 Jul 6 Aug 26 Aug 15 Sep

Date

FIG. 2.-Water levels in Crane Creek Marsh. Unio Start and Unio End indicate period when unionids were sampled and ZM Start and ZM End indicate period when zebra mussel colonization was measured. Solid lines show relative elevations of water depth classes: A. 1-17 cm, B. 18-35 cm, C. >35 cm. An area is flooded when water levels are above the line

Most sampling plots were in intermediate water depths; 15%, 48% and 37% of all plots were in the 1-17 cm, 18-35 cm and >35 cm water depth classes, respectively. Mean water levels at the water level logger decreased from 67 cm in June to 48 cm in September, and water levels on 15 September were 45 cm when the mudflats were mapped (Fig. 2). Seiches caused many short-term water level changes and mean ? 1 SE daily water level changes were 18 cm ? 0.9 (Fig. 2). Sample plot water depths ranged from 5-103 cm. Plots that were between 1-17 cm deep were dewatered 9% of the time, plots that were 18-35 cm deep were dewatered 1% of the time, but plots >35 cm deep were never dewatered (Fig. 2).

Unionid distributions.-Fifteen species of unionids were collected in CCM and four species are listed by Ohio as threatened species or species of special concern (Table 1). Utterbackia imbecillis was not collected in the sample plots, but two live animals were found in the marsh. The five most common species were Quadrula quadrula, Leptodea fragilis, Amblema plicata, Pyganodon grandis and Potamilus alatus, and these comprised 95% of all unionids collected. Unionids ranged in age from 1-28 y old, and several had inhabited the marsh since before zebra mussels were introduced into Lake Erie. The age structure of the five most abundant

species showed that many young (i.e., 1-5 y old animals) were present, which indicated that active recruitment was occurring (Table 2).

We collected 1129 unionids in the 77 plots. Mean catch per unit effort was significantly higher (F = 15.44, df=- 2,74, P < 0.001) in >35 cm water depths than in 1-17 cm and 18-35 cm water depths (Table 1). Most unionids were found in the creek channel or a deep pool in the northwestern corner of the wetland, and therefore few were in areas that became dewatered in September (Fig. 1). Unionid species richness was higher (F = 12.14, df = 2,74, P < 0.001) in >35 cm water depths than in 1-17 cm and 18-35 cm water depths (Table 1). Species assemblages were different among water depth classes (G = 241.93, df = 26,




TABLE 1.-Unionids at Crane Creek Marsh and catch per unit effort, species richness and number of zebra mussels per unionid at different water depths. Catch per unit effort = number of unionids collected per hour. Nomenclature follows Turgeon et al. 1998

Water depth 2 Zebra mussel/ Byssal

Species' Common name 1-17 cm 18-35 cm >35 cm unionid3 thread4

Quadrula quadrula mapleleaf 0 15 463 2.5 ? 0.5 382 Leptodea fragilis fragile 3 24 242 1.1 ? 0.4 69

papershell Amblema plicata threeridge 0 5 199 27.6 ? 4.5 191

Pyganodon grandis giant floater 16 41 29 0.1 ? 0.1 14 Potamilus alatus pink 0 2 33 13.7 ? 5.9 30

heelsplitter Quadrula pustulosa pimpleback 0 2 16 0.6 ? 0.2 18 Toxolasma parvus lilliput 0 0 14 0 10

*Obliquaria reflexa threehorn 0 0 10 0.3 ? 0.2 10

wartyback Fusconaia flava Wabash pigtoe 0 0 6 1.5 + 0.9 6

Lasmigona complanata white 0 2 2 0 3

heelsplitter Lampsilis siliquoidea fatmucket 0 0 2 2.0 ? 1.2 2 * Truncilla fawnsfoot 0 0 2 1.5 ? 0.9 2

donaciformis * Truncilla truncata deertoe 0 0 1 0 1 * Uniomerus tetralasmus pondhorn 0 1 0 0 0 Utterbackia imbecillis paper - - - - -

pondshell Catch per unit effort5 0.4 ? 0.2a 0.8 ? 0.4a 12.7 ? 3.4b

Species richness5 0.5 ? 0.2a 0.8 ? 0.2a 3.4 ? 0.6b Number of zebra Oa 0.01 ? 0.0a 3.3 ? 1.4b

mussels per unionid5

Note: U. imbecillis was observed in the marsh but it was not collected in a sample plot 1 State listed threatened species or species of special interest are indicated with a * 2 Numbers of unionids in different water depth classes 3 Mean ? 1 SE number of zebra mussels attached on unionids 4 Number of unionids with byssal threads

5 Values (mean _

1 SE) with different letters in each row are significantly different

P < 0.001) (Table 1). Subdividing the contingency table showed that Pyganodon grandis was more abundant in shallow water than expected and Quadrula quadrula and Amblema plicata were more abundant in deep water than expected.

The number of zebra mussels on individual unionids ranged from 0 to 400 zebra mussels, but most unionids had few attached zebra mussels. Seventy seven percent of the population had no attached zebra mussels and 92% had <10 zebra mussels on their shell. Only 4% of unionids had >50 zebra mussels on their shells. However, numbers of attached zebra mussels varied among unionid species (Table 1). For example, Amblema plicata averaged >25 zebra mussels per individual, but Pyganodon grandis had <1 zebra mussel per individual. Most unionids (>60%) had some byssal threads on their shells indicating that zebra mussels had been attached in the past, but byssal thread cover varied among species and water depth. For



elliemasters

Sticky Note

There appears to be a correlation between water depth and number of zebra mussels per unionid. Though depths of 1-35 cm are not ideal habitat for unionids they do provide them with refuge from zebra mussels.


TABLE 2.-Ages (years) of the five most common unionid species in Crane Creek Marsh

Age class'

Species 1-5 6-10 11-15 15+

Quadrula quadrula 63 283 131 0

Leptodea fragilis 193 69 7 0 Amblema plicata 9 69 120 6

Pyganodon grandis 72 13 1 0 Potamilus alatus 3 16 16 0

1 Number of unionids in each age class

example, >80% of A. plicata, R alatus and Quadrula quadrula had byssal threads on their shells, but <20% of P grandis and Leptodeafragilis had byssal threads (Table 1). In addition, 68% of unionids at >35 cm and 23% of unionids at 18-35 cm water depths had some byssal threads on their shells, but no unionids at 1-17 cm water depth had byssal threads.

There were different numbers of zebra mussels on unionids among water depths (F = 9.54, df= 2,74, P < 0.001). Unionids in >35 cm water depths had the highest numbers of zebra mussels per individual and unionids at 1-17 cm and 18-35 cm water depths had almost no attached zebra mussels (Table 1). Unionid species richness, catch per unit effort and number of zebra mussels per unionid were not correlated (P > 0.05) with % organic matter (df - 1,75; R2 - 0.048, R2 - 0.026, R2 = 0.038, respectively) or % silt/clay of the sediments (df = 1,8; R2 0.113, R2 = 0.106, R2 = 0.096, respectively).

Zebra mussel colonization.--Portions of the top (1-17 cm water depth) zebra mussel colonization plates were dewatered 36% of the time, middle (18-35 cm) plates were dewatered 1% of the time and bottom (>35 cm) plates were never dewatered. All zebra mussels on PVC plates were >160 tm and were in the post-veliger and settling juvenile stages. There was an interaction of zebra mussel colonization among water depth and sampling location (F = 20.52, df = 6,93, P < 0.001). However, examination of the data showed that colonization increased from the shallowest to the deepest water depths at all sampling locations (Fig. 3). Zebra mussel colonization was different in all water depths (F= 413.72, df= 2,93, P < 0.001). Zebra mussel numbers (mean ? 1 SE) were highest on bottom plates (2097.6

_+ 264.9 zebra mussels/m2), intermediate on middle plates (1132.7 ? 222.8 zebra

mussels/m2) and lowest on top plates (6.9 ?- 2.5 zebra mussels/m2). Zebra mussel colonization was also different among sampling locations (F = 88.87, df = 3,93, P < 0.001). Numbers (mean ? 1 SE) at Location 2 (2167.5 + 305.5 zebra mussels/m2) and Location 3 (1783.8 ? 333.4 zebra mussels/m2) were higher than at Location 1 (88.4 ? 23.8 zebra mussels/m2) and Location 4 (533.3 + 170.1 zebra mussels/m2) and numbers at Location 1 were lower than at Location 4 (Fig. 3).

DISCUSSION

Crane Creek Marsh as a refuge habitat for unionids.-Crane Creek Marsh (CCM) provides habitat for 15 of the 35 species found in Lake Erie (Herdendorf, 1987), including four

species listed in Ohio as threatened or species of special concern. Unionid species richness at this site is similar to other coastal wetlands in the lower Great Lakes including Metzger Marsh (20 species; Nichols and Amberg, 1999), marshes in the St. Clair river delta (1-12 species; Zanatta et al., 2002) and a Presque Isle marsh (18 species; Mastellar et al., 1993). In the past, unionid beds in offshore areas of the lower Great Lakes had comparable richness (8-18 species; Schloesser et al., 1996, 1997), but few unionids survived in these areas after zebra




400 Location 1 4000 Location 2

300 3000

200 oo2000 N 100MN 1000

0 -0

0

1-17 cm 18-35 cm >35 cm 1-17 cm 18-35 cm >35 cm

Water Depth Water Depth

4000 Location 3 2000 Location 4

3000 N 1500 E

L

2000 -10000 1 T N

1000 500

0 - , 0 1-17 cm 18-35 cm >35 cm 1-17 cm 18-35 cm >35 cm

Water Depth Water Depth

FIG. 3.-Mean (? one standard error) number of zebra mussels/m2 collected on colonization plates at different water depths. Colonization was sampled at four locations: (1) where Crane Creek enters the marsh; (2) in the creek channel 1.5 km away from where Crane Creek enters the marsh; (3) midway towards Lake Erie; and (4) where the marsh opened to Lake Erie. Note: Y axes are different among graphs

mussels were introduced (Schloesser et al., 1996). However, it is likely that populations in CCM will persist because most unionids were not infested by zebra mussels. Although our search methods probably underestimated numbers of very small unionids (Strayer et al., 1981; Green, 1980), we also found abundant 1-5 y old individuals of many species. This indicates that active recruitment was occurring at this marsh. Therefore, these data show that CCM is an important refuge for unionids, 15 y after zebra mussels have eliminated most unionids in the western basin of Lake Erie (Schloesser and Nalepa, 1994). Moreover, the

importance of conservation of the remnant populations in these areas has increased because

they could serve as potential brood-stock for future reintroduction programs. Using the total number of unionids collected in the 77 sample plots (1129 unionids), we

estimate that the overall density of unionids was -0.01 unionids/m2. This estimate is

probably somewhat conservative because we may have missed some smaller unionids. This

density is comparable to numbers reported in coastal wetlands in the St. Clair river delta (0.03-0.07 unionids/m2; Zanatta et al., 2002) but is lower than reported in many historical unionid beds in Lake Erie (1.7-11/m2; Ricciardi et al., 1995) or in Lake St. Clair (1.8-2.0/ m2; Gillis and Mackie, 1994; 2/m2; Nalepa and Gauvin, 1988).

Studies have shown that some unionid species are more susceptible to zebra mussel infestations than others. For example, species with thin shells that have long brooding periods are more stressed by zebra mussel infestation than thick-shelled species with short

brooding periods (Haag et al., 1993; Baker and Hornbach, 2000; Hallac and Marsden, 2000). This may explain why populations of the subfamilies Lampsilinae and Anodontinae generally decline faster than Ambleminae after the introduction of zebra mussels (Haag et al., 1993; Gillis and Mackie, 1994; Schloesser et al., 1996, 1997). However, Lampsilinae and Anodontinae are still important components of the community at CCM. We collected seven




lampsilinae species (L. siliquoidea, L. fragilis, 0. reflexa, P alatus, T parvus, T donaciformis, T truncata) and three anodontine species (L. complanata, P grandis, U. imbecillis), and 3 of these (L. fragilis, P alatus, P grandis) were among the five most common species in the wetland. This indicates that even if zebra mussels have affected the community structure at CCM, many species considered susceptible to zebra mussel infestation are still surviving in this marsh.

Mean numbers of attached zebra mussels on different unionid species ranged from 0 to 28 zebra mussels per unionid, which are much lower than described in offshore sites in the lower Great Lakes. For example, unionids in the early phase of the zebra mussel invasion in Lake Erie had >10,000 zebra mussels per unionid (Schloesser and Nalepa, 1994; Schloesser et al., 1996). Schloesser et al. (1996) showed that almost total mortality of unionids occurs when there are 100 to 200 zebra mussels per unionid. In our study, Amblema plicata had the

highest zebra mussel infestation (28 zebra mussels per unionid), but this species can withstand greater zebra mussel infestation than other species (Haag et al., 1993; Baker and Hornbach, 2000). Therefore, zebra mussel infestations at CCM are below those expected to cause total unionid mortality. Zebra mussel infestations at other refugia were comparable to CCM (St. Clair river delta: 31 zebra mussels per unionid; Zanatta et al., 2001; Metzger Marsh: <1 zebra mussel per unionid; Nichols and Amberg, 1999) indicating that unionids may be able to coexist with.zebra mussels in these habitats. However, some studies have reported that as few as 10 to 50 zebra mussels per unionid can increase unionid mortality after several years of infestation (Ricciardi et al., 1996; Hart et al., 2001). Therefore, we expect that some unionids at CCM with high numbers of attached zebra mussels will die unless the zebra mussels become dislodged or killed.

Factors affecting unionid survival in coastal wetlands.--Unionids are surviving in CCM even

though they are exposed to high numbers of zebra mussel veligers. In some locations at CCM, mean numbers of zebra mussel settling on artificial substrates within two weeks were >3000 zebra mussels/m2, and these densities have been correlated with drastic die offs of unionids in other habitats (Ricciardi et al., 1998). Furthermore, we observed even higher numbers of settling veligers (>10,000 zebra mussels/m2) the following year (R. Bowers & F. A. de Szalay, unpubl. data). Settling of zebra mussel veligers was highest at the two

sampling locations in the middle of the wetland. We observed abundant adult zebra mussels on rip-rap on dikes adjacent to these locations. Therefore, our data suggested that many veligers were recruited from nearby areas within the wetland and not from the lake or

upstream areas. However, we acknowledge that the patterns of veliger settling may have been influenced by unexamined abiotic factors (e.g., water temperature, dissolved oxygen, water currents) that differed among these locations.

Most unionids at CCM had byssal threads on their shell, but relatively few had live zebra mussels. This shows that zebra mussels are colonizing unionids, but they are not surviving. Many fish and waterfowl species feed on zebra mussels (French, 1993; Tucker et al., 1996; Morrison et al., 1997; Thorp et al., 1998; Mitchell et al., 2000; Magoulick and Lewis, 2002), and

predation may be one factor controlling zebra mussel numbers in CCM. However, we did not measure predation rates or observe visible signs of predation (e.g., crushed zebra mussel shells) at CCM. Therefore, we do not know the importance of this factor in this wetland.

Another potential cause of zebra mussel mortality is that many unionids burrow into the sediments to avoid unfavorable environmental conditions (e.g., extremely cold winter

temperatures) (Watters et al., 2001; Amyot and Downing, 1997). This will physically dislodge live zebra mussels and smother attached mussels in anoxic sediments (Nichols and Wilcox, 1997). Nichols and Wilcox (1997) reported that unionids with attached zebra mussels could burrow into soft silt/clay sediments but not into coarse sand, which indicates that sediment type will influence the impact of unionid burrowing on attached zebra mussels. Although we




tested for effects of sediment characteristics, we did not detect any correlations between % silt/clay or % organic content and unionid richness, abundance and numbers of attached zebra mussels. However, sediments throughout CCM are mostly inorganic silt/clay and, therefore, the lack of a correlation may be due to low amount of variation across the wetland.

Water level fluctuations are another important factor affecting interactions among zebra mussels and unionids in coastal wetlands. Unlike many inland wetlands and lakes, water levels in coastal wetlands are dynamic and vary both within and among years. For example, seiches caused water levels at CCM to fluctuate about 18 cm each day, and this will frequently expose perimeter areas in this wetland. Although 2001 was a low water year, historic data (NOAA; www.co-ops.nos.noaa.gov) show that mean annual Lake Erie levels have been even lower on 22 y of the past 80 y, which would expose a greater portion of this wetland. Water levels in some sample plots were greater than 35 cm, but these depths were calibrated in June and water levels decreased 20 cm by September. Therefore, most areas in CCM may be aerially exposed during periods of low water, and this will limit unionid and zebra mussel distributions in this wetland.

Zebra mussels can survive aerial exposure of 5-10 d in cool moist environments, but survival decreases rapidly when air temperatures are above 20 C (Ricciardi et al., 1995; Paukstis et al., 1999). Therefore, most zebra mussels would die in areas that are dewatered by seiches during warm summer days. Likewise, we found that colonization on PVC plates that were intermittently exposed for as little as 1% of the time was much less than colonization on

permanently flooded plates. Moreover, colonization in shallow areas would probably decrease later in the year when water levels decreased further. Therefore, unionids in shallow areas are exposed to less zebra mussel colonization than unionids in deeper depths. This was

supported by our observations that unionids in <35 cm water depths had almost no zebra mussels or byssal threads on their shells.

Fluctuating water levels also limit the amount of unionid habitat in coastal wetlands. Although unionids can survive much longer periods of aerial exposure than zebra mussels, they will die if exposed at high temperatures and low relative humidity (Tucker et al., 1997). Low water levels probably also increase the risk of predation and freezing to unionids on

exposed mudflats. This can explain why we found >90% of unionids in sample plots that were >35 cm deep, even though these areas only comprised 37% of all plots. Moreover, many unionids were located in the creek channel. This may be an important refuge for unionids because it could remain inundated when the rest of the wetland is dewatered during periods of low water. Although deep areas in the creek channel provide a stable habitat for unionids, they are also where the highest numbers of zebra mussels veligers are settling. Therefore, future research is needed to determine why zebra mussels are not killing unionids in these areas.

Our results also show that community structure was different among water depths. Only two unionid species (Pyganodon grandis, Leptodea fragilis) were found in areas that were mudflats in September. These thin-shelled species are not tolerant of desiccation (Tucker et al., 1997), and the methods they use to survive in these areas are not clear. Although little is known about unionid behavior, it has been suggested that unionids may burrow into the sediments or crawl to deeper areas to survive periods of low water (Tucker et al., 1997; Amyot and Downing, 1997). Furthermore, most of the unionids found on the mudflats were less than 5 years old. Therefore, these individuals may simply represent colonists since the last time these areas were dewatered.

Identifying key characteristics of habitats where unionids survive in areas with zebra mussels will assist managers to develop strategies to preserve unionid populations. This study and other recent papers have identified several refuge sites with viable populations of




unionids in coastal areas of the lower Great Lakes (Schloesser et al., 1997; Nichols and

Amberg, 1999; Schloesser and Masteller, 1999; Zanatta et al., 2002). One common characteristic of all sites is that they are hydrologically connected to the adjoining lake. This exposes these habitats to wave action, ice scour and fluctuating water levels that

intermittently dewater the sediments and kill zebra mussels. Lake-connected habitats also allow entry of fish that are predators of zebra mussels or are hosts of unionid glochidia. A second characteristic of these sites is that almost all unionids were found in shallow (<2 m) areas. For example, Zanatta et al. (2002) collected only one out of 2356 unionids in depths >2 m. These studies did not report on the upper limit of water depths that had unionids, but our results indicate that most animals will be restricted to areas that are >35 cm deep. Therefore, unionid habitat in coastal areas is restricted to a narrow zone that is shallow

enough to allow water level fluctuations to limit zebra mussels, but deep enough for unionid survival. A third habitat characteristic described in several coastal wetlands was that abundant unionids inhabited soft silt/clay sediments (this study; Nichols and Amberg, 1999; Zanatta et al., 2002). Although some studies have suggested that soft muddy areas in streams and lakes are poor quality habitats for unionids (Strayer et al., 1981; Hinch et al., 1986; Huehner, 1987), other have found that some species will select silt/clay substrates (Downing et al., 2000; Watters, 1993). Soft silt/clay sediments in coastal wetlands may promote unionid survival because they allow unionid burrowing and because zebra mussels have low survival on these substrates (Toczylowski et al., 1999).

In summary, our results demonstrate that although there is potential spatial overlap of unionid and zebra mussel habitats at CCM, unionids are surviving in this coastal wetland.

Although hydrology is one important factor, additional research is needed to determine the mechanisms of other abiotic and biotic factors that limit zebra mussel infestation on unionids in this and other refugia.

Acknowledgments. -We thank the U.S. Fish and Wildlife Service personnel at Ottawa National Wildlife Refuge for their support. Invaluable assistance in the field and the laboratory was provided by K. Popa, S. Knapp, T. Prior, J. Sudomir, G. Zimmerman, J. Deeds, J. Bowers, D. Bricker and J. Smith. Comments by G. T. Watters, D. Pearce, M. Kershner, R. Hoeh and two anonymous reviewers greatly improved this manuscript. We thankJ. Keiper of the Cleveland Museum of Natural History for access to the Unionidae collection. Funding was provided by a grant from the Lake Erie Protection Fund.

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