Invasion of zebra mussel, Dreissena polymorpha, in Lake Simcoe

Journal of Great Lakes Research 37 (2011) 36–45

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Journal of Great Lakes Research j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j g l r

Invasion of zebra mussel, Dreissena polymorpha, in Lake Simcoe David O. Evans a,⁎, Audie J. Skinner a,1, Ron Allen b,2, Michael J. McMurtry c,3 a b c

Ontario Ministry of Natural Resources, Trent University, DNA Building, 2140 East Bank Drive, Peterborough, ON, Canada K9J 7B8 Ontario Ministry of Natural Resources, 50 Bloomington Road, Aurora, ON, Canada L4G 3G8 Ontario Ministry of Natural Resources, 300 Water Street, Peterborough, ON, Canada K9J 8M5

a r t i c l e

i n f o

Article history: Received 22 October 2009 Accepted 9 March 2011 Available online 4 May 2011 Communicated by Joelle Young Index words: Lake Simcoe Zebra mussels Invasion history Density Biomass Veliger settlement rates

a b s t r a c t This study documents the timing of invasion, and initial settlement rates, density and biomass of zebra mussels in Lake Simcoe. Pumped water samples, multi-plate tower samplers, and scuba and benthic airlift surveys were used to sample veligers, post-veligers, juveniles and adult mussels. Veligers were first detected (12 veligers/m3) at one site during August 1992, and again at three sites (6–22 veligers/m3) during August 1994. During July–August 1995 veliger density increased to 12,668–52,480 veligers/m3 at three main basin sites. Low densities of post-veligers (292–1129 individuals/m2) were observed on the multi-plate samplers in the main basin during summer 1994. Postveliger densities increased by 2–3 orders of magnitude during summer 1995. Peak settlement occurred during July– August in both 1994 and 1995. During mid June to mid August, 1995 we estimated 11,249–31,477 settlers/m2/day for sites in the main basin but only 140 and 277 settlers/m2/day in Cook's Bay and Kempenfelt Bay. Growth rates of postveligers on the tower plates were highest at the low density sites. Juvenile mussels were first detected (27–160 mussels/m2) on natural rock substrates during scuba and airlift surveys at 2–6 m in the main basin in December 1994 and March 1995. Two year-classes of zebra mussels, 1994 and 1995, were subsequently observed on rocky substrates in the main basin during February 1996. Juveniles comprised 98.0±1.8% of the population at that time. The mean density at depths of 2–6 m was 32,529 zebra mussels/m2 with a mean shell-free dry biomass of 34.8 g/m2. Crown Copyright © 2011 Published by Elsevier B.V. on behalf of International Association for Great Lakes Research. All rights reserved.

Introduction Zebra mussel, Dreissena polymorpha, is an invasive species from the Ponto-Caspian region of central Europe (Smirnova et al., 1993) that arrived in North America via ship ballast water release. Initial observations of zebra mussels in North America were reported in Lake St. Clair in 1988 (Hebert et al., 1989). By 1990 zebra mussels were found in all five of the Laurentian Great lakes and by 1994 were reported in nineteen states in the USA as well as inland waters in Ontario and Quebec (Schloesser et al., 1996; Benson and Raikow, 2009). The first documented observation in Lake Simcoe was in the fall of 1991 on the hull of a boat that had entered the lake via the Trent–Severn Waterway (OMNR, 1997). Prior to this initial observation in Lake Simcoe a monitoring program was established in 1990 to document the timing and spatial pattern of the impending invasion. Initial concerns about zebra mussels in the Great Lakes focused on the physical effects on the ecology of inshore waters, including degradation

⁎ Corresponding author. Tel.: + 1 705 755 2256. E-mail addresses: [email protected] (D.O. Evans), [email protected] (A.J. Skinner), [email protected] (R. Allen), [email protected] (M.J. McMurtry). 1 Tel.: + 1 705 755 1231; fax: + 1 705 755 2276. 2 Tel.: + 1 905 713 7394; fax: + 1 905 713 7361. 3 Tel.: + 1 705 755 2167; fax: + 1 705 755 2168.

of fish habitat (Griffiths, 1993; Leach, 1993), and impacts on domestic and industrial water supply infrastructure caused by colonization of intake pipes of municipal drinking water facilities, industrial installations and electric power generating stations (LePage, 1993; Kovalak et al., 1993). Over time, as experience and knowledge accumulated, it became apparent that ecologically significant interactions involving the interplay between zebra mussels, nutrient dynamics, and primary and secondary producers were operating in the Great Lakes and producing heretofore unseen changes in inshore and offshore communities (Hecky et al., 2004). Establishing the time of invasion of zebra mussels is a critical step towards understanding system response to trophic state disruptors, including eutrophication, additional invasive species and climate change, the primary stressors that are currently operating in Lake Simcoe (Evans et al., 1996; Winter et al., 2007; Stainsby et al., 2011). Studies of the initial stages of an invasion (e.g., Strayer et al., 1996; Lucy, 2006) and of longer-term trends (Barbiero and Tuchman, 2004; Burlakova et al., 2006; Strayer and Malcom, 2006) provide baseline data required to understand the impacts of new species on physical and biological processes that structure and facilitate the flow of energy through aquatic ecosystems. For example, the timing and temporal trajectories of invasions are potentially key factors in explaining shifts in water quality, habitat use, food web dynamics and energy flow in these systems (e.g., Fahnenstiel et al., 1995, Yu and Culver, 2000; Vanderploeg et al., 2002; Barbiero et al., 2006a; Hecky et al., 2004; Qualls et al., 2007). Understanding the ecology of these invasive species is equally important

0380-1330/$ – see front matter. Crown Copyright © 2011 Published by Elsevier B.V. on behalf of International Association for Great Lakes Research. All rights reserved. doi:10.1016/j.jglr.2011.04.002

D.O. Evans et al. / Journal of Great Lakes Research 37 (2011) 36–45

for predicting their impacts and potentially adapting management regimes to accommodate their presence (Karatayev et al., 1998; Burlakova et al., 2006; Strayer and Malcom, 2006). The purpose of our study is to document the timing of initial invasion and population expansion, dispersal, settlement rates, spatial densities and biomass of juvenile and adult mussels in Lake Simcoe to establish a baseline for tracking population trends and for interpretation of ecological change. Methods Study site description Lake Simcoe, located between Georgian Bay of Lake Huron to the northwest and Lake Ontario to the southeast (Fig. 1), is a large, relatively shallow lake (surface area of 722 km2, maximum and mean depths of 42 and 14 m) with a flushing time of about 11 years. The Lake Simcoe watershed, excluding the lake, is 2899 km2 (LSRCA and MOE, 2009). The lake consists of a large main basin with maximum depth of 33 m and two large bays: Cook's Bay in the southwest quadrant that is relatively shallow (area 44 km2, maximum depth 15 m) and Kempenfelt Bay on the west side (area 34 km2, maximum depth 42 m). The lake water is relatively hard, with mean May to October alkalinity of 115 mg/L and calcium concentration of 41 mg/L, and is mesotrophic with mean 2004– 2008 total phosphorus in the euphotic zone of the main basin ranging from 13.5 to 14.1 μg/L and Chlorophyll a ranging from 1.9 to 2.5 μg/L (Young et al., 2010). The major tributaries enter the lake from the southern part of the watershed and the outflow is in the north via Lake Couchiching (Fig. 1). The shoreline is comprised of about 55% rock– cobble, 35% sand–gravel and 10% mud (MacCrimmon and Skobe, 1970). Rocky substrates along exposed shorelines generally occur to a depth of 6–8 m (Johnson and Nicholls, 1989). Substrates in sheltered areas are comprised of finer materials and generally below depths of about 8 m consist primarily of mud (Rawson, 1930). Monitoring Monitoring included: 1) surveys from 1990 to 1995 to determine veliger occurrence and density using pumped water samples at six locations associated with major marinas and boating traffic (OMNR, 1997), 2) sampling of settled veligers during summer and fall of 1994

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and 1995 to provide information on distribution, density and settlement rates using multi-plate tower samplers, and 3) juvenile and adult mussel surveys from 1992 to 1996 to determine their occurrence, size, density and biomass using scuba, airlift sampling and video surveys. Veliger stage Pumped water samples were collected monthly from June to October 1990–1995 at six locations: Jackson's Point (JP), Strawberry Island (SI), Trent/Talbot (TT), Kempenfelt Bay (KB), Couchiching (CC) and Cook's Bay (CB) (Fig. 1). Following the methods of Marsden (1992), ten 50-L water samples were collected at each site on each date using a bilge pump and an 80 μm-mesh plankton net at 0.5-m depth intervals from 0.5 to 5.0 m to provide a 500-L composite. Post-veliger and settler stage Vertical tower samplers with ten removable plates (Fig. 2a) were installed at the same six stations used for the pumped water samples. The towers were suspended vertically at a depth of 3 m in 6 m of water (the littoral zone) and were constructed of gray polyvinyl chloride (PVC), a favorable substrate for zebra mussels (Marsden, 1992). The towers were designed to provide similar shading for each of the sampling plates (Marsden, 1992). The height of the towers is 64 cm and the exposed surface of each plate is 12 cm × 11 cm (132 cm2). The towers were installed in mid June of 1994 and 1995 and were sampled monthly until mid October of each year. To determine settlement rates (i.e., the number of settlers/m2/day) the top three plates of the tower were removed and replaced each month (replacement plates). Mussels on the plates were termed post-veligers and, conservatively, post-veligers having a shell length b 0.44 mm were termed settlers. To monitor distribution, densities, growth rates and displacement/mortality of zebra mussels, 2–3 plates were left in the towers for two, three or four months (fixed plates). When plates were collected from the towers, they were placed into sealed plastic bags or buckets and held on ice in an insulated cooler. In the laboratory, samples were processed and preserved within 24–48 h by scraping both plate surfaces with a plastic scraper and soft brush, rinsing and filtering the water in the plastic bag through a 56-μm Nitex mesh, and placing in either 70% ethanol or 5% formalin. A

Fig. 1. Map of Lake Simcoe showing the sampling locations referenced in the text. Depth contours are shown at 5 m intervals. Diamonds are pumped water stations (1992–1995) and tower samplers (1994–1995); squares are scuba and airlift stations fall–winter 1992–1993; circles are scuba, airlift and video stations in late summer 1993; triangles are scuba, airlift and video stations, December 1994 and March 1995; stars are scuba, airlift and video stations, February 1996. Abbreviations in brackets are used in the text to designate sampling sites. K45 is a primary, long-term MOE monitoring station. Satellite image of the Lower Great Lakes Basin, April 21, 2008 is from NOAA, Great Lakes Coast Watch Program (http://coastwatch.glerl.noaa.gov).

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D.O. Evans et al. / Journal of Great Lakes Research 37 (2011) 36–45

Fig. 2. Photographs of the tower sampler (a) showing ten removable sampling plates and (b) oblique and (c) plan views of a fixed-duration sampling plate from Strawberry Island on October 18, 1995 after four months in situ, illustrating the dense packing of mussels.

dissecting microscope with cross-polarization light (Johnson, 1995) was used to count the samples and measure the greatest linear dimension of the mussel shells; however, not all mussels were counted or measured in all samples. All mussels were measured in 1994 and in most cases several hundred individuals (mean = 502) were randomly sampled and measured per plate in 1995. When samples were not counted in their entirety, the total count was estimated by weighing and counting a subsample and adjusting the count using the whole sample weight. The density of settled mussels was calculated based on the exposed upper and lower surface area of each plate, which was 264 cm2.

Juvenile and adult zebra mussels Replicate airlift samples were collected by Scuba divers at select locations (Fig. 1), depths and dates, with replicates separated by about 10 m at each depth as part of an investigation of macro-invertebrate densities. An airlift sampler is an effective device for quantitative sampling of invertebrates (Barton and Hynes, 1978) and detecting the presence–absence of mussels. During November and December of 1992, seven replicate 1-m2 airlift samples were collected at each of 2, 4 and 6 m at SI, and six replicate 1/4-m2 airlift samples were collected at each of 2, 3, 4, 5 and 6 m at Sibbald Point. The same number of samples was repeated at the same depths and sites under the ice in March of 1993. Between August 25 and September 17, 1993, four replicate 1/4-m2 airlift samples were collected at each of 2, 4, and 6 m at five rocky sites on the north (Black Point, Grape Island, McRae Point, Strawberry Island and Glenrest Shoal) and south coasts (Blackbird Point, Sibbald Point, Townline Shoal, Long Shoal and Big Bay Point). During December of 1994 and under the ice in March of 1995, 5–6 replicate 1/4-m2 airlift samples were collected at each of 2, 4, and 6 m depths at Strawberry Island. Finally, under the ice during February 1996, eight replicate 1/4-m2 airlift samples were collected in 2–3, 3–4, 4–5 and 5–6-m depth strata at SI, Townline Shoal (TS) and the northeast corner of Snake Island (SN). The densities of zebra mussels obtained with the air lift samples were estimated as catch per unit area vacuumed. The airlift sampler consisted of a 1-m length of 4-cm diameter PVC pipe with an 8-cm diameter vacuum head. A pressure valve was located 10 cm above the vacuum head, which allowed compressed air to be injected at a

controlled rate. A 500-μm mesh removable Nitex collecting bag was attached to an 8 cm diameter outlet collar. The surface of each quadrat was thoroughly vacuumed and each layer of rock was removed as vacuuming continued to the base (hard packed substrate), usually 1–2 rocks below the surface layer. The densities of zebra mussel were also estimated from rock counts. Ten rocks were randomly collected from each quadrat and placed in screened buckets during the 1994, 1995 and 1996 surveys. A video recording was made of each quadrat prior to the removal of the rocks. The density of zebra mussels was calculated by estimating the number of mussels on the ten sampled rocks and multiplying the average number of mussels per rock by the total number of rocks within each 1/4-m2 quadrat as observed in the video record. All mussels were counted in 1994 and 1995, but in February 1996, zebra mussel abundance was estimated for three of the eight replicates within each depth stratum by weighing the total sample and weighing and counting three sub-samples. Total wet biomass (TWBM) and shell-free dry biomass (SFDM) of zebra mussels were also determined for each site (SI, TS, SN) and depth in 1996. A random sample of about 100 small mussels b 10 mm and all large musselsN 10 mm were counted and shell lengths measured to provide a frequency distribution for both size categories at each depth and site. Length–weight relationships were determined for TWBM and SFDM by weighing and measuring 70–100 zebra mussels collected at each depth (2–3 m, 3–4 m 4–5 m and 5–6 m) at TS during February 1996. All specimens were preserved in 10% formalin prior to weighing and measuring. SFDM was obtained by removing the soft tissue from the shells, weighing wet, drying at 60 °C for 24 h, cooling in a dessicator and re-weighing. Power functions were fitted to TWBM (mg) and SFDM (mg) versus shell length (mm) relationships: TWBM = 0:08147 · shell length

3:04859

3:06963

SFDM = 0:00318 · shell length

  2 r = 0:99; n = 325 ; and   2 r = 0:99; n = 325 :

These length–weight regressions were applied to the length– frequency distributions and the mean density estimates at 1-mm shell-length intervals to obtain zebra mussel biomass per m2 for each site and depth.

D.O. Evans et al. / Journal of Great Lakes Research 37 (2011) 36–45

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Statistical analyses ANOVA was used to test for differences in sizes of settled mussels on the fixed plates of the multi-plate tower sampler over months and among sites during 1995 and was also used to test for differences in densities of juvenile mussels on natural rocky substrates among depths and between fall and winter sampling. ANCOVA was used to compare the relationships between settlement rates and veliger densities (covariate) on the tower plates between 1994 (low veliger density) and 1995 (high veliger density). The statistical package Statistica 8 was used for these tests. Regression models for zebra mussel length–weight relationships and veliger densities versus settlement rates were generated using the trendline function in Microsoft Excel. Unless otherwise stated, error terms reported in the text represent ±1 standard deviation of the mean.

Results Veligers in pumped water samples Veligers were not observed in 1990, 1991 or 1993 and only 6 (12 veligers/m3) were observed in a single pumped water sample at KB in August 1992. In 1994, 8 veligers/m3 were sampled at TT during mid July, 6, 22 and 8 veligers/m3 were sampled at SI, TT and JP, respectively, on August 16, and 16 veligers/m3 were sampled at JP on September 12. In 1995, however, veligers were observed at all six sampling locations during July, August and September with mean densities during June 16–August 16 of 12,668, 28,776 and 52,480 veligers/m3 at SI, JP and TT, respectively (Table 1). Veliger densities at CB, CC and KB during the same period were only 116, 444 and 256 veligers/m3, respectively (Table 1).

Post-veligers on tower plates: distribution and density In 1994, post-veligers on the replacement plates were initially observed at low densities on August 16 but only at the main basin sites (JP, TT, SI). At these sites, post-veliger densities were maximal during mid July–mid August (1107 ± 524 post-veligers/m2) (Fig. 3a). Post-veligers were not observed on replacement plates at CB in 1994 and only occurred at KB and CC during September and October at very low densities (b30 mussels/m2) (Fig. 3a). In 1995 post-veligers on the replacement plates were also most abundant during mid July to mid August and at JP, SI and TT densities were more than three orders of magnitude greater than in 1994 (1107 ± 642 versus 1,111,578 ± 534,501 post-veligers/m2) (Fig. 3b). Unlike 1994, post-veligers in 1995 were also observed at these sites during June–July (Fig. 3). In 1995 densities during July–August increased at CB, KB, and CC to 15,795 ± 7106 post-veligers m2 but were 1–2 orders of magnitude

Fig. 3. The number of post-veligers on the monthly replacement plates at six sample sites in Lake Simcoe on four sampling dates during (a) 1994 and (b) 1995. See Fig. 1 for locations and full names of sample sites. Counts were standardized to a 30-day interval within each sampling period. Error bars represent one standard deviation and the scale of the y-axis is 3 orders of magnitude greater in (b).

lower than at the main basin sites. In both years densities on the replacement plates declined dramatically in September and October. Densities of post-veligers on the fixed plates at JP, SI and TT were about 2 times greater than on the replacement plates on the same dates, reflecting accumulation of mussels over 2–4 months (Fig. 4). In 1994, however, maximal density occurred during August–September (Fig. 4a), one month later than in 1995 (Fig. 4b), possibly reflecting less competition for space at a much lower density in 1994. Densities on all plates declined during September and October 1995, but the fixed plates at JP, SI and TT remained densely populated in mid October (168,118 ± 4642 post-veligers/m2, Figs. 2b and c). Densities were much lower at CB, KB and CC (8813 ± 5767 post-veligers m2),

Table 1 Summary of veliger densities in pumped water samples and post-veliger counts and settlement rates on the replacement plates during 1994 and 1995. Veliger density and the postveliger counts in 1994 are means for July 14–September 12 and in 1995 from June 16–August 16 corresponding to peak veliger and settler densities in each year. Post-veliger densities are based on total counts of zebra mussels on the tower plates, and settlement rates are based on settlers' b0.44 mm shell length only. Year

1994

1995

Site

Jackson's Point Strawberry Island Trent–Talbot Kempenfelt Bay Couchiching Cook's Bay Jackson's Point Strawberry Island Trent–Talbot Kempenfelt Bay Couchiching Cook's Bay

Veliger density in water samples

Post-veligers on replacement plates

Settlement rate on replacement plates

Veligers/m3

±SD

Post veligers/m2

± SD

Settlers/m2/day

12 3 11 0 0 0 28,776 12,668 52,480 256 444 116

4 3 11 0 0 0 15,672 9843 17,920 24 260 50

811 292 1129 8 8 0 617,007 378,485 1,056,439 9167 11,742 4659

283 181 227 11 11 0 24,600 35,747 96,624 9863 10,052 1134

14.9 6.5 23.4 0.04 0.04 0 19,311 11,249 31,477 277 356 140

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but were much higher than in 1994 (Figs. 4a and b). Densities on the fixed plates at JP, SI and TT declined by 82.5 ± 4.3% from mid August to mid September and 47.0 ± 18.0% from mid September to mid October with an overall decline of 90.0 ± 5.6 from August to October. Settlement rates of veligers The smallest settlers observed on the replacement plates were 0.08 mm and 95.6% of all post-veligers observed on July 21, 1995 were b0.44 mm (Fig. 5a). Settlers (shell length b 0.44 mm) represented 81.8% (n = 505) of the post-veliger population on the plates during July–August, declined to 20.9% (n = 875) from August to September and 0.14% (n = 737) from September to October. Peak settlement rates at JP, SI and TT occurred during July–August in 1994 (26.9 ± 15.4 settlers/m2/day, Fig. 3a) and 1995 (34,289 ± 16,341 settlers/m2/day, Fig. 3b). Settlement rates at CB, KB and CC were much lower (1994, 0.03 ± 0.02 settlers/m2/day and 1995, 457.7 ± 155 settlers/m2/day). Mean settlement rates at JP, SI and TT during the peak months of settlement in 1995 (mid June–mid August) were two orders of magnitude higher (11,249–31,477 settlers/m2/day) than during the peak months (mid July–mid September) in 1994 (6.5–23.4 settlers/m2/day) (Table 1). Densities of veligers in the pumped water samples versus densities of settlers on the replacement plates during 1994 and 1995 were tightly coupled during the two month period of peak settlement (Table 1). The log10 transformed relationships were similar in 1994 and 1995 even though densities were dramatically different (ANCOVA: homogeneity of slopes (F1, 5 =0.53, P=0.49); years (F1, 5 =1.08, P=0.35)). Therefore we combined the data over both years into a single relationship: Fig. 4. The number of post-veligers on fixed duration plates at six sample sites in Lake Simcoe on four sampling dates during (a) 1994 and (b) 1995. See Fig. 1 for locations and full names of sample sites. Error bars represent one standard deviation and the scale of the y-axis is 3 orders of magnitude greater in (b).

2

3

Log10 settlers=m =day = 0:8850 · Log10 veliger=m   2 + 0:3303 r = 0:99; n = 9 :

Fig. 5. The shell-length, percent frequency distribution of post-veligers at Jackson's Point over four sampling periods during 1995 on monthly-replacement plates (panels a and b) and fixed duration plates (panels c and d) of the tower sampler. Shell-length scale and intervals are different for (a) and (c) (interval is 0.04 mm) and (b) and (d) (interval is 0.4 mm).

D.O. Evans et al. / Journal of Great Lakes Research 37 (2011) 36–45

Fig. 6. Mean shell lengths of zebra mussel post-veligers on tower plates at six locations on four sampling dates during 1995. All mussels were from the fixed duration plates that were in situ for 1, 2, 3, or 4 months. Error bars represent 2 standard errors of the means.

Shell growth of post-veligers The size distributions of mussels on the replacement and fixed duration plates at the main basin sites (JP, SI and TT) in 1995 overlapped during all sampling dates, but larger individuals were consistently more abundant on the fixed duration plates (Fig. 5). The mean shell length of post-veligers on the fixed plates in 1995 increased slowly from mid July to mid August while new recruits were colonizing the plates, then increased sharply from mid August to mid October (Fig. 6). There were also marked differences in shell lengths on the fixed plates among sites in 1995 (Fig. 6). Using log10 transformed shell lengths, there was a significant difference among sites and over time (two-way ANOVA: site effect F3, 10,494 = 763, P b 0.001; season effect F2, 10,494 = 5908, P b 0.001; interaction term F13, 10,494 = 96, P b 0.001). By mid October, shell lengths were largest at sites KB, CB and CC (Fig. 6), which were the sites where the settler densities were low (Table 1, Fig. 4b). Juvenile and adult zebra mussels No zebra mussels were detected in any of the airlift sampling and visual inspections by Scuba divers in 1992 or 1993. Detailed taxonomic analysis and counts of benthic invertebrates for all replicates and depths at three of the north and three of the south coast sites from late summer of 1993 also did not detect a single zebra mussel. If present, juvenile mussels would have attained 1–5 mm shell length (Fig. 6) and been easily detected, therefore we conclude that zebra mussels were absent or at non-detectible densities in 1993. Juvenile zebra mussels were first observed on natural rocky substrate during diving and airlift surveys at Strawberry Island in December of 1994 and March of 1995 (Table 2), corresponding with

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the first observation of settlers on the towers at this location during summer 1994 (Fig. 3). These individuals represented the initial detectable year-class of zebra mussels produced in Lake Simcoe. Densities were greater at 2 m than at 4 and 6 m (Table 2). Based on the rock count estimates of zebra mussel density, the depth and seasonal effect was statistically significant (two way ANOVA: season effect, F1, 31 = 29.9, P b 0.001; depth effect, F2, 31 = 18.5, P b 0.001, interaction term, F2, 31 = 1.66, P = 0.205). The seasonal difference in density suggested that significant over-winter mortality of mussels had occurred; the percent decrease in density from December 1994 to March 1995 at 2, 4 and 6 m was 51.5, 64.6 and 50.1%, respectively (Table 2). During February of 1996, zebra mussels were observed at SI, TS and SN. Mean densities of the 1994 and 1995 year-classes varied among the three study sites and among depth strata within each site, ranging from 9745–57,715 zebra mussels/m2 (Table 3). Densities decreased with depth at SI and TS and appeared to increase slightly with depth at SN. Higher density of the initial 1994 year-class at TS and SN compared to SI (Fig. 7) suggested that zebra mussels achieved higher initial success in the south. Densities of zebra mussels at SI increased by N2 orders of magnitude from March 1995 to February 1996, which in parallel with increased abundance at TS and SN, clearly indicated strong lake-wide production of zebra mussels, at least in the main basin. Density by shell length plots in 1996 were distinctly bimodal (Fig. 7), with the first mode of smaller mussels being the 1995 yearclass and the second mode of larger mussels the 1994 year-class. The high densities in 1996 were due to the abundance of juvenile mussels from the 1995 year-class (Fig. 7). The overall mean shell lengths of the 1995 and 1994 year-classes were 4.9 ± 2.1 and 21.1 ± 2.9 mm. Numerically the 1995 year-class comprised 98.0 ± 1.8% of the total population in the main basin during winter 1996 (Table 3). The distribution of shell-free biomass arrayed by 1 mm shelllength bins was also strongly bi-modal, the 1994 and 1995 yearclasses being clearly separated (Fig. 8). Biomass stored by year-class varied among sites, TS had the highest biomass in 1994 but the lowest biomass contribution of juveniles in 1995, while SI had the opposite pattern and SN was intermediate with similar biomass within both year-classes. The mean TWBM for all sites and depths was 824 ± 316 g/m2 and SFDM was 34.8 ± 14.6 g/m2 (Table 3). Discussion The initial detectable settlement of zebra mussels in Lake Simcoe occurred on the tower plates during the summer of 1994 and low density of juveniles was observed on rock substrate at Strawberry Island during December 1994. Airlift sampling in 1994 and winter 1995 demonstrated the effectiveness of airlift sampling for detecting the presence of zebra mussels at relatively low density hence, we are confident in our assessment of the absence of mussels in 1992 and 1993. Catches of zebra mussels per m2 in March 1995 based on airlifts

Table 2 Comparison of zebra mussel (zm) catch using the airlift sampler at Strawberry Island versus direct counts of zebra mussels on rock samples collected by divers during fall 1994 and under-ice during winter 1995. Each airlift sampled one 1/4 m2 quadrat. Zebra mussel counts were based on 10 rocks per quadrat expanded to the total number of rocks in each of the 1/4 m2 quadrats. The mortality estimates are from the December to March sampling dates and are based on the zebra mussel counts on rocks. In 1994 all transects were completed in two days. In 1995 each depth was sampled on separate days. Year

Date

1994

Dec. 04–05

1995

Mar. 08 Mar. 09 Mar. 11

Depth (m)

2 4 6 2 4 6

Airlift sampling # Airlifts

5 5 4 6 6 6

Rock counts Estimated density

# Quadrats

(zm/m2)

(± SD)

55.2 19.2 11.0 82.0 35.3 8.7

23.7 13.1 6.8 29.4 10.9 8.6

5 5 5 6 6 6

Estimated density

Mortality

(zm/m2)

(± SD)

(%)

160.3 77.3 67.7 77.8 27.4 33.8

31.7 31.6 30.3 35.4 36.1 17.3

– – – 51.5 64.6 50.1

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Table 3 Density and biomass of zebra mussels during February 1996 at Strawberry Island, Townline Shoal and Snake Island. Year-class density estimates are based on complete counts of all mussels N 12 mm and total population estimates based on triplicate sub-sample counts for each of three replicates at each site and depth. Biomass estimates are based on length– weight regressions of zebra mussels at Townline Shoal during 1996 and size frequency distributions at 1-mm shell length intervals at each site and depth. Site

Date

Strawberry Island

Feb. 21

Townline Shoal

Feb. 07

Snake Island

Feb. 14

Depth (m)

2–3 3–4 4–5 5–6 2–3 3–4 4–5 5–6 2–3 3–4 4–5 5–6

Density (zebra mussels/m2) 1995 yr class

1994 yr class

Total population mean ± SD

48,116 51,028 9528 12,205 24,855 13,521 14,637 10,170 36,954 54,635 52,739 57,414

260 237 217 157 672 596 861 413 257 495 324 301

48,376 51,265 9745 12,362 25,527 14,117 15,498 10,583 37,211 55,130 53,063 57,715

were similar to density estimates based on actual counts of mussels on rocks, whereas airlift estimates during December were lower than counts. It is possible that airlifting in late winter recovered both alive and dead mussels, thereby inflating the airlift counts. Our direct counts of mussels suggested 50–65% mortality of juveniles between December 1994 and March 1995.

The pelagic and settlement phase Veliger density and settlement rates in Lake Simcoe were tightly coupled during the initial two years of detectable zebra mussel production. Tight coupling of late veliger densities and settlement rates in Lake Erie was observed at fine spatial and temporal scales as abundance of veligers waxed and waned with changing wind and hydrodynamic conditions (Martel et al., 1994). Our results integrate across much larger spatial (N20 km) and temporal scales (30 days) to effectively capture the lake-wide relationship between pelagic veliger density and settlement rates during the earliest stages of a zebra mussel invasion. Veliger densities in recently established populations varied widely from 1000–50,000 veligers/m3 in river and lake settings (Strayer et al., 1996; Lucy, 2006), 500–10,000 veligers/m3 in Saginaw Bay, Lake Huron (Nalepa et al., 1995) and 2500–360,000 veligers/m3 in Lake Erie (Fraleigh et al., 1993; Leach, 1993). Our observations of very low densities in the main basin of Lake Simcoe (3–12 veligers/ m3) and associated low settlement rates (6.5–23.4 settlers/m2/day) during 1994 are evidence of the earliest stage of invasion. This was followed by rapid expansion of the population (12,668–52,480

580 11,251 3462 2031 7501 3164 1025 4358 9296 16,996 13,204 20,294

Total wet biomass with shell (kg/m2)

Shell-free dry biomass (g/m2)

1.248 1.175 0.315 0.446 0.797 0.675 1.014 0.539 0.743 1.303 0.721 0.909

50.9 47.9 12.9 18.9 32.9 27.9 42.1 22.3 30.5 64.3 29.6 37.3

veligers/m3 and 11,249–31,477 settlers/m2/day) during July and August of the following year. Settlers were present at low density in the main basin (sites SI, TT and JP) during 1994 and widely distributed and abundant in the main basin during summer 1995. The near absence of zebra mussel settlers on the tower plates at CB, KB and CC in 1994 and low densities in 1995 suggested that the origin of the invasion was within the main basin and not in the two large bays or Lake Couchiching, despite the initial observation of six veligers in a 500 L sample near the head of KB during August 1992. Given that veligers can disperse rapidly (Johnson and Carleton, 1996; Strayer et al., 1996), the order-of-magnitude lower densities in Kempenfelt and Cook's bays also suggests very limited, if any, transport of veligers from the main basin to the head of the bays where our samplers were located. Settlement of veligers was not detected during mid June to mid July in 1994 but was observed during this period in 1995, although at lower densities than during July and August. The later appearance of veligers in 1994 might reflect cooler temperatures, as volumeweighted surface temperatures at 0–6 m in the main basin were cooler during spring 1994 than in 1995, reaching 15 °C 11 days later (MOE station K45; D.O. Evans, unpublished data). In Lake Erie, veligers were undetectable at 12.8 °C but were very abundant at 18 °C (Fraleigh et al., 1993). Leach (1993) reported the first occurrence of veligers in Lake Erie at 14.5–24.1 °C and many European studies cited in Karatayev et al. (1998) indicate that spawning is initiated at 15–18 °C. The optimum temperature for successful development is 18 °C and the pelagic stage extends for 18–33 days (Sprung, 1993). In 1994 and 1995, settlement rates in Lake Simcoe peaked during mid

Fig. 7. Density of zebra mussels at 1-mm shell-length intervals at three study sites (SI, TS, SN) in February 1996 for the 1995 (a) and 1994 (b) year-classes. Zebra mussels were collected by scuba from rock samples at four depth strata at each site. The distributions were determined separately for each depth at each site and the mean density over depths for each size class at each site is plotted. The scale of the y-axis is 100 fold larger in (a).

D.O. Evans et al. / Journal of Great Lakes Research 37 (2011) 36–45

43

The importance of habitat limitation was also suggested by the among site differences in the shell growth rates of zebra mussels on the fixed plates during 1995. Growth was greatest at the sites with lowest post-veliger density (CB, KB and CC). Displacement or losses were low (12.3%) at the low density sites from September to October, in contrast to the 90% losses at the high density sites. The largest mussels and highest growth rate occurred in Cook's Bay, which is known to have had the highest total phosphorus and Chlorophyll a concentrations during 1994–95 (Young et al., 2010). This is consistent with Strayer and Malcom's (2006) finding that shell growth was positively correlated with phytoplankton biomass. Similarly, growth of zebra mussels in Saginaw Bay, Lake Huron was positively affected by temperature, total suspended solids and most importantly Chlorophyll a (Chakraborti et al., 2002). Colonization of natural rocky substrates Fig. 8. Shell-free dry biomass for zebra mussels at 1-mm shell length intervals at three study sites (SI, TS, SN) in February 1996 for the 1995 (a) and 1994 (b) year-classes. Biomass is based on the density distributions in Fig. 7 and weights of individual zebra mussels within the 1-mm size bins. Weights were determined using the length–weight power function for SFDM of zebra mussels sampled at 2–6 m at Townline Shoal during February 1996.

July to mid August at 20–23.5 °C, which is similar to the time of peak density of veligers in Lake Erie (Fraleigh et al., 1993; Garton and Haag, 1993; Leach, 1993). The size of settlers, which we defined to be b0.44 mm in Lake Simcoe, was similar to other systems. Stańczykowska and Lewandowski (1993) reported that most veligers in a Polish lake settled at a shell length N 0.20 mm, but a few settled at 0.14 mm. Martel et al. (1994) also showed a sharp transition from veliger to settler at 0.20 mm, where settlers varied in size from 0.18–0.37 mm with 95% between 0.20–0.30 mm. The smallest settlers on the tower plates in Lake Simcoe were 0.08–0.12 mm, which represented 2.5% of all postveligers on July 21, 1995. Post-veligers 0.12–0.16 mm represented 12.5% of the population in mid July and the modal size was 0.24– 0.28 mm, although post-veligers 0.20–0.24 mm were similarly abundant, and together these two size classes represented 45% of all individuals on the tower plates on July 21. This size range, 0.20–0.28 probably best describes the size of transition from veliger to settler in Lake Simcoe. Settler density declined steeply from mid August and settlers were very rare after September 13, 1995, hence settlement of veligers was effectively complete by mid September. The similarity in size distribution of post-veligers observed on the replacement and fixed plates can be explained by movement of individual mussels after settlement probably due to competition caused by crowding and limited availability of substrate. Zebra mussels attach to a firm substratum by secretion of byssal threads, but small mussels often detach temporary byssal threads and move to new locations (Eckroat et al., 1993). Movement of larger individuals to the unoccupied habitat of the newly replaced plates could have occurred. Colonization of the blank replacement plates by mussels of 3–12 mm shell length, during September, 13 to October 18, 1995, indicated that juvenile mussels have the capacity to move for several months after initial settlement. Further evidence of movement was provided by the 90% decline in settler density from August to October of 1995 on the fixed plates at SI, JP and TT. This decline could also have occurred due to mortality, caused by predation (Molloy et al., 1997), high temperature N 30 °C (Spidle et al., 1995) or high ammonia levels N 1.0 mg/L (Nichols, 1993), although temperature and ammonia levels at nearby stations were not elevated (Young et al., 2010). The extent of predation, if any, is unknown. Densities on the fixed plates at these three sites were very similar (16.9 ± 0.47 mussels/cm2) and shell lengths were relatively large (2.2– 4.3 mm) during mid October 1995 after four months in situ. Similar density at these geographically widely-separated sites suggests abandonment of the plates due to space limitation as the mussels increased in size (Strayer et al., 1996; Burlakova et al., 2006).

Following the initial low production of zebra mussels in Lake Simcoe in 1994, the population on rocky substrates at 2–6 m depths in the main basin expanded dramatically in 1995 to a mean density of 32,549 ± 7764 mussels/m2. This type of rapid expansion in population size within one or two years after initial colonization has also been observed in the Laurentian Great Lakes. For example, Dermott et al. (1993) reported that densities in northeastern Lake Erie increased from 384 mussels/m2 in May following the initial year of colonization to 54,317 mussels/m2 by November of that year. Similar high densities, 28,244 and 75,296 mussels/m2 were also observed on cobble rock in inner Saginaw Bay of Lake Huron in the second and third years after establishment. Juvenile zebra mussels were initially detected on rocky habitats at Strawberry Island in December 1994, but this was the only site examined at that time. Given the occurrence of settlers on the tower plates at three sites in the main basin during October 1994, low densities of zebra mussels were probably present on littoral zone substrates throughout the main basin of the lake during December of that year. The 50.1–64.6% reduction in density of mussels observed from December 1994 to March 1995 at Strawberry Island was probably due to mortality during this interval. Annual mortality rates of zebra mussels in two European lakes varied from 28–57% for juvenile and 31–70% for 1-year old mussels (Smit et al., 1993). In the Hudson River estuary 49% mean annual mortality was reported for three adult cohorts of zebra mussels (Strayer and Malcom, 2006). Winter storms and physical displacement in Lake Simcoe could have contributed to mortality until ice cover was established on January 9, 1995. From ice-on to the time of our March observations, the lake remained frozen (ice-out occurred on April 13, 1995) therefore storms or ice scour would not have contributed to mortality. Predation is a possible cause of overwinter mortality. Martin and Corkum (1994) reported that crayfish, Orconectes propinquus, consumed zebra mussels in laboratory experiments at 20 °C, mussels b8 mm shell length being preferred, although larger mussels were also eaten. Mean density of crayfish, Orconectes propinquus, at our Strawberry Island study site during fall 1992 was 22.6 ± 11.8 crayfish/ m2 (Mason and Evans, 2011) suggesting the potential for significant zebra mussel predation mortality, although predation rates would be relatively low at cold winter temperatures (1–6 °C). Losses during winter 1994–95 ranged from 34–82 zebra mussels/m2 which, at densities observed for crayfish N16 mm carapace length (12 O. propinquus/m2), would equal only 2.8–6.8 mussels consumed per crayfish over the entire 93 day observation period. Density of mussels reached relatively high levels in 1996, following the initial two year-classes in 1994 and 1995. Unfortunately, abundance information is not available again until the summer of 2005 when a study of the benthic macro-invertebrate fauna, including zebra mussels, was conducted (Stantec Consulting Ltd., 2005). Densities of zebra mussels at depths of 4–9 m based on petite Ponar grab samples were 11,304, 10,090 and 5142 zebra mussels/m2 in Cook's Bay, Kempenfelt

44

D.O. Evans et al. / Journal of Great Lakes Research 37 (2011) 36–45

Bay and the main basin, respectively. Estimation of the biomass of zebra mussels and quagga mussels, Dreissena rostriformis bugensis, was also undertaken during 2006–2008 using a video-based method (Ozersky et al., 2011). Quagga mussels were first reported in Lake Simcoe in 2004 (OMNR, 2004) and were at low abundance in 2006–2008. Ozersky et al. (2011) reported SFDM of dreissenids (mainly zebra mussels) on hard substrates in the main basin and Kempenfelt Bay during 2006–2008 as 35.7 g/m2 (based on observations at 2 and 5 m), which is very similar to our 1996 estimate of 34.8 ± 14.7 g/m2 on rocky habitat in the main basin at depths of 2–6 m. Similarly, the average SFDM of zebra mussels in north-eastern Lake Erie during the first and second years after colonization was 30.8 g/m2 (Dermott et al., 1993). The mean shell length and SFDM of dreissenids in 2006–2008 was 13.0 mm and 6.6 mg (Ozersky et al., 2011) compared to only 4.97 mm and 0.43 mg in 1996. Based on the mean body mass of dreissenids (0.0066 g) and mean SFDM (35.7 g/m2) on rocky substrates in 2006– 2008 (Ozersky et al., 2011), the average density on rocky substrates would have been approximately 5409 mussels/m2, which is within the range observed for well established dreissenid populations in Lake Erie (Patterson et al., 2005) and similar to the mean density (7694± 6463 mussels/m2) recorded at 15 lake-wide stations at depths of 4–9 m in Lake Simcoe during 2005 (Stantec Consulting Ltd., 2005). The higher densities that we observed in 1996 were due to the high abundance of juveniles after the initial year of lake-wide production. Biomass in shallow rocky areas of the main basin, however, was similar in 1996 to that estimated during 2006–2008 by Ozersky et al. (2011). Soft tissue weight in 1996 was much higher, at a common shell length, than reported by Ozersky et al. in 2006–2008, indicating that growth and condition of juvenile mussels was higher during the initial year of invasion (1994), possibly corresponding to the elevated phytoplankton volumes observed during that year (Young et al., 2010). It is not presently possible to determine the annual trend in densities of zebra mussels since initial colonization due to the monitoring gap following 1996. Inter-annual variation in densities in the order of 2–10 fold have been observed in other populations (Nalepa et al., 1995; Strayer and Malcom, 2006, Burlakova et al., 2006) and similar fluctuations could potentially have occurred in Lake Simcoe. Retrospective analysis of phytoplankton abundance records (Winter et al., 2011) might provide a way to reconstruct annual fluctuations in zebra mussel densities (Strayer and Malcom, 2006). In Lake Simcoe, algal biovolumes in the main basin were very stable from 1996–2003, which suggests that there was little fluctuation in zebra mussel densities during the initial eight years after zebra mussel establishment; however, an increase in variability and density of pelagic algae occurred from 2004–2007 (Winter et al., 2011), suggesting that changes in zebra mussel densities might have occurred during this period. Conclusions and management implications Our studies clearly establish the timing of the zebra mussel invasion in Lake Simcoe. The initial year of detectable natural production was 1994, and 1995 was the first year of high-density production of veligers and settlers. The initial year with colonies of juvenile and adult mussels on rocky substrates throughout the spring and summer growing season was 1996. Zebra mussels are most successful in mesotrophic lakes (Karatayev et al., 1998) and, with reference to lake size, calcium and phosphate concentrations, modeling studies on other lakes (Ramcharan et al., 1992) suggest that Lake Simcoe offers ideal conditions for stable dreissenid populations. Major shifts in water transparency, and phytoplankton bio-volumes (Eimers et al., 2005) and community structure (Winter et al., 2011) occurred following zebra mussel invasion in Lake Simcoe, although the influence of other concurrent stressors, including nutrient loading, food web interactions and climate change, have not yet been resolved. System-wide effects associated with the invasion of zebra mussel on transparency and phytoplankton biomass have been widely observed in

the Laurentian Great Lakes (Nicholls and Hopkins, 1993; Holland, 1993; Howell et al., 1996; Yu and Culver, 2000; Barbiero and Tuchman, 2004; Barbiero et al., 2006a; Barbiero et al., 2006b). The near-shore phosphorus shunt hypothesis (Hecky et al., 2004) includes these types of changes as a result of lake-wide effects of zebra mussel filtration and re-engineering of littoral zone substrates that alter the way in which nutrients and materials are processed. Our documentation of the timing of the zebra mussel invasion in Lake Simcoe provides a precise time mark for retrospective analysis and interpretation of the impacts of zebra mussels on physical processes, tropho-dynamics and community ecology within the context of the multi-stressor state of the lake. Finally, the major influence of zebra and quagga mussel invasions on the ecology of lakes and rivers (e.g., Strayer et al., 2006; Campbell et al., 2009; Higgins and Vander Zanden, 2010; Kerfoot et al., 2010) emphasizes the need for comprehensive ecological monitoring of these and other invasive species in large, complex and socioeconomically important freshwater ecosystems.

Acknowledgments We thank Yvonne C. Allen, Colin Stewart and Katrina Wisniewski for the detailed work of processing samples, sorting, counting and measuring zebra mussels in the laboratory. We also thank the staff of the Lake Simcoe Fisheries Assessment Unit for providing logistical and technical support and assistance in the field. We also thank Dr. Joelle Young, and two anonymous reviewers whose helpful comments and editing suggestions greatly improved the manuscript. Financial support for this research was generously provided to DOE and the LSFAU by the Ontario Ministry of Natural Resources.

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