introduction pathways, differential survival of adult and ... · the introduction pathway and...

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Lake and Reservoir Management 21(4):391-402, 2005© Copyright by the North American Lake Management Society 2005

Introduction Pathways, Differential Survival of Adult and Larval Zebra Mussels (Dreissena polymorpha),

and Possible Management Strategies, in an Adirondack Lake, Lake George, NY

Marc E. Frischer+, Brian R. McGrath*1, Andrew S. Hansen*2, Paul A. Vescio*3, Jane A.Wyllie*4, John Wimbush* and Sandra A. Nierzwicki-Bauer*+

Skidaway Institute of Oceanography 10 Ocean Science Circle

Savannah, GA 31411

*Rensselaer Polytechnic Institute and Darrin Fresh Water Institute 5060 Lake Shore Drive

Bolton Landing, NY 12814

AbstractFrischer, M.E., B.R. McGrath, A.S. Hansen, P.A. Vescio, J.A. Wyllie, J. Wimbush and S.A. Nierzwicki-Bauer. 2005. Introduction pathways, differential survival of adult and larval zebra mussels (Dreissena polymorpha), and possible management strategies, in an Adirondack lake, Lake George, NY. Lake and Reserv. Manage. 21(4):391-402.

The introduction pathway and source of zebra mussel larvae into Lake George, NY were determined and a general bioassay was developed to assess the zebra mussel colonization risk of a water body. The presence of zebra mussel larvae (veligers), recruitment, and adults were monitored in Lake George from 1995-2003. All observations of zebra mussel veligers were at marinas, boat ramps, or areas heavily used by fishing boats. Models and observation suggest that human activity is the primary mechanism by which zebra mussels are transported overland. Although one small colony of zebra mussels was discovered during this period, no evidence was found of recruitment or permanent colonization by zebra mussels in Lake George. A series of bioassays to assess both larval and adult growth and survival was developed and indicated that Lake George water limited the survival of zebra mussel larvae but not of adults. These bioassays confirmed model predictions that zebra mussel recruitment is limited by the moderate water alkalinity in Lake George, but that adults were able to survive and grow. The unique water chemistry that limits zebra mussel colonization, and the close proximity of Lake George to other mussel-populated waters, make Lake George an ideal natural laboratory to study the introduction process of zebra mussel adults and/or larvae into a landlocked lake. Although zebra mussels have colonized the major waterways of Eastern North America, the establishment of zebra mussel populations in landlocked lakes is occurring much more slowly. Public outreach and education efforts that appear to aid in limiting the introduction of zebra mussels are also discussed.

Key Words: zebra mussel; introduction pathways, risk assessment, outreach, Lake George, NY

1Current address: Woodard and Curran Inc., 980 Washington St., Dedham, MA 02026

2Current address: Univ. of Hawaii, Dept. of Oceanography, 1000 Pope Rd., MSB 611, Honolulu, HI 96822

3Current address: Regeneron Pharmaceuticals, 81 Columbia Turnpike, Rensselaer, NY 12133

4Current address: California Institute of Technology, 1200 E. California Blvd., Pasadena, CA 91125

+Corresponding Authors

Native to the drainage basins of the Black, Caspian and Aral Seas, the zebra mussel (Dreissena polymorpha Pallas 1771) was introduced to Europe by at least the mid-1700s (Archambault-Guezou 1976) and to North America in 1985 or 1986 (Roberts 1990, Carlton 1993, Ludyanskiy et al. 1993, Mills et al. 1993). Since its introduction to North America,

zebra mussels have rapidly colonized U.S. and Canadian freshwaters, achieving a range from Quebec to the Gulf of Mexico in Eastern North America, and west to Oklahoma (Benson 2002). Early predictions of the distribution of zebra mussels suggested that all North American water bodies capable of supporting zebra mussels would be colonized by the year 2000 (Ludyanskiy et al. 1993). However, these initial predictions did not consider colonization barriers imposed on non-contiguous bodies of water (Kraft and Johnson 2000).

Frischer, McGrath, Hansen, Vescio, Wyllie, Wimbush and Nierzwicki-Bauer

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Consequently, the colonization of inland lakes has been slower than initially predicted.

Water bodies considered to be capable of supporting zebra mussels are characterized by: calcium concentrations >12 mg/L; pH >7.4; salinity <3 parts per thousand; annual tem-peratures that do not exceed 30°C; sufficient nutrients to support significant photosynthetic biomass, availability of hard substrate, and extensive littoral zones (Morton 1971, Ten Winkel and Davids 1982, Sprung and Rose 1988, Kova-lak 1989, Smirnova and Vinogradov 1990, O’Neill 1996, Sprung 1993). The importance of these parameters has been confirmed and further refined by statistical analyses of the observed occurrence of zebra mussel populations in Europe (Ramcharan et al. 1992a, 1992b), and North America (Hincks and Mackie 1997).

The spread of zebra mussels in connected waterways has been primarily facilitated by the advective transport of planktonic larvae (Stoeckel et al. 1997). However, dispersion either up-stream or overland is generally thought to require a different mechanism, most probably associated with human activities (Carlton and Geller 1993, Johnson and Carlton 1996, Johnson and Padilla 1996). Thus, proximity of a lake to other zebra-mussel-colonized water bodies, use-patterns associated with a particular water body, and water chemistry, all contribute to the risk of zebra mussel colonization (Koutnik and Padilla 1994, Buchan and Padilla 1999, Bossenbroek et al. 2001). Accordingly, it has been shown that zebra mussels colonize noncontiguous inland lakes significantly more slowly than connected waterways, and that large lakes are colonized more readily (Kraft and Johnson 2000), presumably due to a greater number of access points and a larger number of human users.

Lake George is a 32-mile-long glacial lake located in the southeastern corner of the Adirondack Park in New York State. Lake George is located between latitude 43° 22-51’ N and 73° 21-47’ W and is relatively large, with a surface area of 114 km2. In general, water flows from south to north and drains into Lake Champlain 68 m below the elevation of Lake George at Ticonderoga, NY. The Lake is character-ized by an irregular, steep, and rocky shoreline occupying a graben in Precambrian bedrock. The southern basin has some exposure of calcium-containing Cambrian sandstones. Based on water-quality parameters, Lake George is an oligo- to mesotrophic lake with moderate alkalinity (Momen et al. 1996, 1997). During the 10-year period 1980-1990, the average pH was 7.56 and average calcium, magnesium, ni-trate, and phosphate were 10.7, 3.5, 0.031, and 0.006 mg/L respectively (Momen et al. 1996). Based on average water chemistry using the Ramcharan et al. (1992a) and O’Neill (1996) models, Lake George is predicted to be at borderline risk for zebra mussel colonization. However, colonization risk in the southern basin is predicted to be higher than other

locations due to the presence of limestone outcrops and tributaries that deliver calcium-enriched groundwater to the Lake (Fuhs 1972, Sutherland et al. 1983).

Lake George is a major recreational resource for the region, supporting tourism, pleasure boating, fishing, and diving industries. The proximity of Lake George to within 40 km of several zebra-mussel-colonized water bodies (including Lake Champlain, the Hudson River, Glen Lake, and Saratoga Lake) increases the risk of zebra mussel introduction from these water bodies.

Previous studies have reported the detection of zebra mus-sel larvae (veligers) in Lake George (Frischer et al. 2002), indicating that zebra mussels are being transported into the lake. Other than one recent isolated detection of adult mus-sels in the lake (Wimbush et al. 2002), adult mussels have not otherwise been observed. The purpose of this study was to determine the introduction pathway and source of zebra mussel larvae into this relatively large pristine lake in the Northeastern U.S., a model landlocked lake, to develop a gen-eral bioassay capable of assessing the specific zebra mussel colonization risk of a pristine water body and, based on this information, to formulate and implement a comprehensive management program to minimize the introduction and pre-vent the establishment of zebra mussels in Lake George.

Materials and MethodsVeliger Monitoring in Lake GeorgeThe introduction of zebra mussel larvae (veligers) was studied in Lake George from 1995-2003. The presence of veligers was monitored approximately bi-weekly from May-September when water temperatures were >12°C. Plankton samples were collected from 7 locations from 1995-1996 (Snug Harbor, Coates Point, Hague Marina, Dollar Islands, DEC Docks, Norowal Marina, and Dome Island). During 1997-1999 an additional 4 locations (Hogback Reef, Crooked Tree Point, Tea Island, and Lake George Beach) were added to expand coverage in the southern basin of the lake. Begin-ning in 2000, a twelfth site in the southern basin was added to the monitoring program (King Neptune’s). In December 1999, adult mussels were found and subsequently removed from this site (Wimbush et al. 2002). Site locations (Fig. 1) provided representative coverage of both basins as well as the Narrows, and allowed a comparison between areas where boats are commonly launched into the lake, areas where boats often congregate for fishing, and areas where these activities generally do not occur.

Plankton samples were collected by filtering 200 L of a depth-integrated water sample from the top 10 m of water through a 44-µm (Ernest Case Co., Andover, NJ) or 63-µm mesh size (Wildco, Madison, WI) plankton net as previously

Introduction Pathways, Differential Survival of Adult and Larval Zebra Mussels (Dreissena polymorpha), and Possible Management Strategies, in an Adirondack Lake, Lake George, NY

393

described (Frischer et al. 2002). When the site was shal-lower than 10 m, an integrated water sample was collected from 1m below the surface to just above the bottom. Water samples were concentrated and either fixed with ethanol (25% final concentration) or left unfixed. Samples were kept dark and cool on ice and transported to the lab within 8 hours. Zebra mussel veligers were enumerated within 24 hours by cross-polarized light microscopy as described by Johnson (1995). Microscopy was facilitated using a Nikon SMZ-2T dissecting microscope equipped with two polarizing filters positioned over the fiber optic light source (Model FO-150 Chiu Technical Corp., Kings Park, NY) and the objective, so that the sample was held between the two filters. The concentration of veligers was determined by enumerating veligers in four 5-ml replicate samples from each plankton sample. The total concentration of veligers was calculated

as described by Brady et al. (1993), accounting for sample dilution in the fixed samples due to the addition of ethanol. Concurrent with collection of plankton samples, temperature and dissolved oxygen profiles of the water were determined using a YSI model 57 dissolved oxygen and temperature sonde (YSI Inc., Yellow Springs, OH). Chlorophyll a con-centrations were determined fluorometrically after extraction with acetone (Clesceri et al. 1998). When veligers were detected in a particular plankton sample, the location was re-sampled the following day to determine whether veligers could still be detected and whether spawning adults were present at the site.

Recruitment Monitoring in Lake GeorgeBeginning in 1997 a monitoring program to assess recruit-ment of zebra mussels in Lake George was initiated. Initially, recruitment collectors were placed in one location in the north basin (Hearts Bay), one in the Narrows (Dollar Islands), and two in the south basin (DEC Docks and Hogback Reef). Most sites where collectors were deployed were approximately 10 m deep. In addition to providing representative geographic coverage of the Lake, these sites were chosen for their prox-imity to locations where veligers had been detected and/or where human activity (boating and fishing) was common. In 1999 the collector at Hogback Reef disappeared, and in 2000 a new one was installed at Dark Bay. Also, following the repeated observation of veligers at Coates Point and at Snug Harbor by a public boat ramp, collectors (1 each) were installed at these locations in 2000. During the same year, two collectors were placed at the King Neptune’s site where adult zebra mussels had been found and removed.

Custom-made recruitment collectors (24.9 x 11.1 x 13.5 cm), each containing 8 stainless steel plates (7.65 x 12.65 cm), were deployed in the lake at the sites described above. The collector design conformed to criteria outlined by Marsden (1992) and Marsden and Lansky (2000). Two collectors were placed at each site, one near the surface (ca. 2 m below the surface) and a second near the bottom (ca. 1 m above the bottom). Each set of collectors was attached to an anchored submerged buoy. One set of 4 recruitment plates was removed monthly (May-September) by SCUBA divers and examined. A second set of 4 plates remained in the Lake from first de-ployment in the spring through the fall. Recruitment plates were removed and placed in individual plastic bags, cooled, and transported to the lab. The presence/absence of zebra mussel recruits was determined by microscopic examination of both sides of each plate using a Nikon SMZ-2T dissecting microscope within 24 hours of collection.

Adult Survival and Growth BioassaysThe ability of recently settled zebra mussels to grow and survive in water from Lake George was determined by

Figure 1.-Map of Lake George, NY showing veliger monitoring sites where zebra mussel veligers were occasionally detected (); monitoring sites where veligers were never detected (); and sites where zebra mussel recruitment collectors were placed ().


394

conducting bioassays in aquaria. Freshly recruited zebra mussels were collected from the Hudson River by allowing them to settle on stainless steel plates (as described above) for approximately 10 weeks (late July-mid-October, 1997). Four settlement plates containing a total of 104-187 settled zebra mussels, derived from an apparent single cohort, were placed into 20-gal aquaria containing 60 L of water from Lake George (187 total mussels), the Hudson River (104 total mus-sels), and Artificial River Water (ARW; total 148 mussels). ARW was prepared with distilled water and 12.16 mg/L MgCl2, 33.0 mg/L CaCl2, 14.7 mg/L MgSO4, and 15.0 mg/L NaHCO3 (all chemicals were obtained from Sigma Chemical Co., St. Louis, MO). Aquaria were maintained at constant temperature (22°C), aerated, and darkened to prevent algal overgrowth, from October 16, 1997 through February 20, 1998. One-third of the volume of each aquarium was replaced with fresh water weekly, and any dead mussels counted, removed from the tank, and saved for final analysis. Zebra mussels were fed with a saturating concentration (ca. 1.7 x 108 cells/L) of the diatom Thalassiosira pseudonana (Diet-C, Coast Seafoods Co. South Bend, WA) every 1-2 days. After the experiment was terminated all zebra mussels were removed from the tanks and the shell length, width, height, wet weight were determined using a dial caliper (Mitutoyo Corp, Kanagawa, Japan). Dry shell and tissue weights were measured using a digital pan balance (Mettler Toledo model PB303, Switzerland), respectively. Dry weights were deter-mined after drying in a 55ºC oven until the weight did not change between consecutive daily measurements.

Larval Survival BioassaysThe ability of zebra mussel veligers to settle in water from Lake George and Lake Champlain was investigated. Veligers were collected in late August and early September 1998 at Larrabee’s Point on the Vermont side of Lake Champlain at the Ticonderoga Ferry landing platform using a horizontally towed 44-µm mesh plankton net. Approximately 15,000 veligers were added to triplicate 20-gal aquaria with 20 removable standard glass microscope slides lining the bot-tom. Beginning one day after the addition of veligers to the aquaria, 4 slides were removed every second day during a 7-9 day period and the number of living settled larvae determined by cross-polarized light microscopy.

The effect of calcium additions and the adjustment of pH on the survival of zebra mussel larvae was determined in similar bioassays. In these studies approximately 20,000 ve-ligers were added to either duplicate or triplicate treatments. Calcium concentrations were amended by adding calcium as CaCl2 (stock, 100 mg/L; Sigma Chemical Co., St. Louis, MO) and the pH was adjusted by titration with 1N NaOH.

In each of 5 bioassay studies conducted from June through August 1999, calcium concentration, magnesium concen-

tration, pH, and temperature were monitored every other day when larvae were sampled. Calcium and magnesium concentrations were determined using a Perkin-Elmer atomic absorption spectrophotometer (Model 5100 PC, Perkin-Elmer, Norwalk, CT) from nitric-acid-acidified (0.1% final concentration) water samples following EPA methods 215.1 and 242.1, respectively (U.S. EPA 1983). The pH was de-termined using an Orion pH electrode (Model 210A, Orion Research, Boston, MA) that was calibrated before each use. Temperature was measured with a standard laboratory thermometer.

Visual Survey for Adult MusselsOver 300 person hours of visual survey by SCUBA divers, snorkel, underwater video, and shoreline observations were made to determine whether populations of adult mussels were present in the Lake. Surveys were conducted at all marinas and boat ramps. In addition, surveys near major lake tributaries, randomly selected locations in the lake, and near all areas where zebra mussel larvae had been observed in the lake were made during the study period in an effort to determine whether adult zebra mussels were present.

Statistical AnalysesAnalysis of variance (ANOVA), t-tests, and non-linear regression analysis of larval survival were facilitated using the algorithms available in the software package SigmaStat V.2.02 (SPSS, Inc.).

Figure 2.-Highest number of zebra mussel veligers observed in any single sample at any site or location for each study year in Lake George, NY.


395

ResultsDetection of Planktonic Larvae and Zebra Mussel Recruitment in Lake GeorgeVeligers were detected in plankton samples from Lake George in 5 of the 9 study years (Fig. 2). Between the years 1995-2003 the highest-estimated veliger concentration was 850 veligers per M3 of water in 1997, but usually much lower, if any, concentrations were observed. Seasonally, veligers were observed most commonly and in highest concentrations in July, but were also detected three years in June. In 1995 veligers were detected from May-September (Fig. 3). Over the 9 year study period, veligers were observed at 6 of the 12 lake sites, but at 3 of these locations (Norowal Marina, Dollar Islands, and Hague Marina) veligers were only observed in 1995 (Fig 4). Veligers were observed in three of the 9 study years at Coates Point in the northern basin (1995, 1997, and 2000), and two of the 9 years each at Snug Harbor in the northern basin (1999 and 2001) and DEC Docks in the southern basin (1995 and 2001). The total number of times that veligers were detected at any site is shown in Table 1. Except in one case (Coates Point, 1997), veligers were not detected in replicate plankton samples collected the day after an initial observation. Of the 5 locations where boats are regularly taken in and out of the Lake, veligers were de-tected at each site except Neptune’s. However, sampling at this site only began in 2000 after vigorous efforts to remove a population of approximately 20,000 adults discovered at the site in 1999 and an extensive public education effort had been made to prevent further importation of zebra mussels into the lake. Veligers were detected in one of two sites where boats commonly congregate for fishing (Coates Point). In areas not characterized by boating or fishing activity (Other), veligers were detected at one of four sites (Dollar Islands). No correlation was found between the physical, chemical, and biological parameters measured (temperature, dissolved

Figure 3.-Monthly average zebra mussel veliger density for each study year for all sites in Lake George, NY.

Figure 4.-Average observed yearly zebra mussel veliger density for each monitored site in Lake George, NY. Asterisks indicate sites where boats are introduced into the Lake. Coates Point and Hogback Reef are sites commonly occupied by recreational fishing boats. Sites are arranged from south to north. No data were collected from sites and dates indicated with light grey boxes ( ).

Table 1.-Detection of veligers at different locations in Lake George (1995-2003).

Site Location # Times Detected/ Site Category (Lake Basin) # Observations

Snug Harbor Boat Launch North 3/63Coates Point Fishing North 7/72Hague Marina Boat Launch North 1/72Dollar Islands Other Narrows 2/73DEC Docks Commercial Dock South 7/75Norowal Marina Boat Launch South 8/74Dome Island Other South 0/74Hogback Reef Fishing South 0/58Crooked Tree Point Other South 0/58Tea Island Other South 0/58King Neptune’s Boat Launch South 0/35Lake George Beach Public Beach South 0/58


396

ratio between calcium and magnesium concentrations in the two lakes (3.57 ± 1.15 and 4.52 ± 0.39) were not signifi-cantly different (p=0.127). The average pH of waters from Lake Champlain (8.18) was significantly greater than the average pH of waters from Lake George (7.88) used in the larval bioassay studies (p = 0.045). The difference between calcium concentrations and pH between calcium-amended Lake George and Lake Champlain waters was not significant (Table 3). However, since magnesium concentrations were not concurrently adjusted in these studies, the concentration of magnesium (2.38 mg/L) in the amended Lake George water was significantly less, and the ratio of calcium to mag-nesium in the amended Lake George water experiments was significantly more than that of Lake Champlain water used in these studies (p<0.001).

oxygen, and chlorophyll a) and the detection of zebra mus-sel veligers.

Efforts to detect the recruitment of zebra mussels in Lake George began in 1997, and monitoring has been performed monthly since then each summer and fall. With the exception of the adult mussels discovered at the King Neptune’s site in 1999, no evidence of zebra mussel recruitment was observed during the 9-year study period.

Growth and Survival of Adult Zebra Mussels in Water from Lake GeorgeTo evaluate the potential for the establishment of zebra mus-sels in Lake George, a series of controlled laboratory bioassay studies were conducted to determine whether zebra mussels could settle, grow, and survive in water from Lake George and to confirm model predictions that water alkalinity was a limiting factor for zebra mussels in Lake George water. Adult zebra mussels were able to grow and survive in water from Lake George. Mussels maintained in water from Lake George survived as well or better than those maintained in artificial river or Hudson River water. After 19 weeks, 85.6% (160 of 187) of zebra mussels were still living in Lake George water as compared to 79.1% (117 of 148) in water from the Hudson River and 49% (51 of 104) in artificial river water that was formulated to support zebra mussels (Table 2). Although actual growth rates could not be determined from these studies (accurate size measurements of the freshly settled mussels were not made at the start of the bioassay study), after 19 weeks the size of zebra mussels from each treatment was compared. The animals that were maintained in Hudson River water were significantly larger and heavier than mussels grown in either water from Lake George or the artificial river water (p <0.001). Mussels raised in artificial river water and Lake George water were of equivalent size and weight (Table 2).

Water Chemistry in Larval Bioassay StudiesTemperature, dissolved oxygen, pH, calcium and magnesium concentration were monitored in each of the larval bioassay studies every other day when larvae were sampled for the duration of the study period. Conditions were kept constant throughout each experiment (data not shown). Calcium/magnesium concentrations and pH were measured for each water type and experiment (Table 3). The average calcium concentration of Lake Champlain water from all of the experiments was 17.65 mg/L, significantly greater than the calcium concentration of Lake George water (10.99 mg/L; p<0.001). The average concentration of magnesium of Lake Champlain water used in the larval bioassays was 5.18 mg/L, significantly greater than the magnesium concentration of Lake George waters (2.43 mg/L; p<0.001). However, the

Table 2.-Growth and survival of adult zebra mussels after 19 weeks in different water types.

Length (mm) Dry Weight Water Type % Survival (± SD) (mg) (± SD)

*Lake George 85.6 9.39 (1.69) 43.29 (20.17) (n=160)*Artificial River 49.0 9.92 (1.80) 48.79 (22.41) Water (n=51)Hudson River 79.1 10.52 (1.63) 65.93 (26.07) (n=117)

*No significant difference between length or dry weight (shell & tissue) n = number of mussels

Figure 5.-Larval settlement and survival bioassay, of zebra mussel larvae collected from Lake Champlain, VT in water from Lake Champlain (), and in water from Lake George, NY (). Regression coefficients for Lake Champlain and Lake George are 0.96 and 0.74, respectively. Error bars represent the standard deviation of triplicate samples.


397

Tabl

e 3.

-Effe

ct o

f cal

cium

and

pH

am

endm

ent o

n la

rval

sur

viva

l in

Lake

Geo

rge

wat

er

#

Of S

ettle

d La

rvae

Aft

er:

% S

urvi

val A

fter

Exp

erim

ent

Wat

er T

ype

(n)1

2 [Ca]

(SD

) 2 [M

g] (S

D)

pH (S

D)

1 da

y (S

D)

7

days

(SD

) 7

days

(SD

)

#1 –

No

Lak

e C

ham

plai

n (3

) 20

.48

(0.5

4)

3.82

(0.

04)

8.16

(0.

13)

107.

3 (1

3.9)

84.7

(33

.7)

77.4

(21

.8)

Man

ipul

atio

n L

ake

Geo

rge

(3)

10.6

5 (0

.32)

2.

5 (0

.00)

7.

86 (

0.02

) 26

.5 (

2.1)

0.17

(0.

014)

0.

63 (

0.6)

#2

Lak

e C

ham

plai

n (1

) 19

.10

(0.4

7)

4.93

(0.

52)

8.51

(0.

03)

495.

0

130.

5 26

.4[C

a] A

men

dmen

t L

ake

Geo

rge

(3)

10.6

9 (0

.30)

2.

36 (

0.12

) 8.

19 (

0.05

) 16

8.6

(42.

3)

0

0

Lak

e G

eorg

e (3

) 14

.58

(0.1

0)

2.29

(0.

12)

8.21

(0.

07)

371.

8 (4

.9)

0

0

Ca

to ~

14

mg/

L

Lak

e G

eorg

e (3

) 16

.39

(0.3

0)

2.30

(0.

05)

8.20

(0.

08)

329.

3 (8

8.7)

9.33

(0.

14)

0.09

(0.

1)

Ca

to ~

16

mg/

L

#3

Lak

e C

ham

plai

n (2

) 15

.0 (

0.45

) 6.

58 (

0.56

) 8.

11 (

0.16

) 95

.9 (

8.3)

45.9

(4.

1)

48.2

(8.

4)[C

a] A

men

dmen

t L

ake

Geo

rge

(2)

9.85

(0.

12)

2.45

( 0

.03)

7.

79 (

0.13

) 67

.4 (

5.1)

1.8

(0.4

) 2.

6 (0

.7)

L

ake

Geo

rge

(2)

14.6

7 (0

.37)

2.

48 (

0.03

) 7.

8 (0

.14)

81

.9 (

1.6)

18.9

(0.

1)

23.1

(0.

2)

Ca

to ~

15

mg/

L

#4

Lak

e C

ham

plai

n (2

) 17

.90

(0.0

7)

5.56

(0.

36)

8.15

(0.

16)

93.6

(1.

9)

59

.6 (

5.8)

63

.7 (

4.9)

[Ca]

Am

endm

ent

Lak

e G

eorg

e (2

) 12

.38

(0.5

4)

2.55

(0.

06)

7.90

(0.

14)

63.9

(1.

6)

0.

75 (

0.4)

1.

2 (0

.6)

L

ake

Geo

rge

(2)

30.8

9 (0

.41)

2.

40 (

0.06

) 7.

86 (

0.14

) 68

.1 (

7.95

)

22.4

(3.

4)

32.8

(1.

1)

Ca

to c

a. 3

0 m

g/L

#5

Lak

e C

ham

plai

n (3

) 15

.76

(0.0

5)

5.03

(0.

68)

7.96

(0.

04)

54.2

(3.

3)

12

.9 (

3.4)

24

.5 (

7.0)

[Ca]

& p

H

Lak

e G

eorg

e (3

) 11

.4 (

0.03

) 2.

39 (

0.08

) 7.

66 (

0.01

) 32

.3 (

1.3)

0 0

Am

endm

ent

Lak

e G

eorg

e (3

) 16

.1 (

0.42

) 2.

43 (

0.11

) 7.

97 (

0.04

) 56

.3 (

2.2)

1.3

2.4

(0.7

)

Ca

to c

a. 1

6 m

g/L

pH

to c

a. 8

.00

1 n=n

umbe

r of

rep

licat

es

2 Con

cent

ratio

n of

Mg

and

Ca,

mg/

L

SD=S

tand

ard

Dev

iatio

n


398

formulated general management strategies based on these studies to reduce future risk of zebra mussel colonization of Lake George and other lakes.

The results of a 9-year lake-wide monitoring program re-vealed that zebra mussel larvae were occasionally present in Lake George, with occurrence being highly variable inter-annually and generally at very low concentrations. However, the locations where larvae were detected were less variable. Of the total number of veliger observations (28) made during the study period, 19 of these observations were at locations near public marinas and boat launches, and 7 were made near a site commonly frequented by fishing boats (Coates Point) close to a public boat launch. Only two observations were made at locations other than marinas or areas where fishing is common (Dollar Islands). These observations provide direct evidence that spawning adults or larvae are occasionally in-troduced into Lake George, and that introductions are likely associated with the movement of boats from zebra mussel infested waters into Lake George. These conclusions are con-sistent with a number of reports in the literature suggesting that recreational boating involving boat movement between lakes, is an important overland zebra mussel transport vec-tor (Carlton 1993, Koutnik and Padilla 1994, Buchan and Padilla 1999, Kraft and Johnson 2000, Bossenbroek et al. 2001, Johnson et al., 2001, Kraft et al., 2002).

Seasonally, the detection of zebra mussel larvae was also less variable than the inter-annual patterns. Veligers were observed most commonly in June and July and less com-

Settlement and Survival of Zebra Mussel Veligers in Water from Lake George and Lake ChamplainIn contrast to adult zebra mussels, larvae do not appear to effectively settle or survive in water from Lake George (Fig. 5). Compared to settlement in water from Lake Champlain, significantly fewer larvae settled in Lake George water than in water from Lake Champlain (p<0.001). In 5 independent larval settlement and survival bioassays conducted with water collected from different locations in Lake Champlain, Lake George, and with larvae collected at different times, an average of 48±21% of the larvae settled after 1 day in Lake Champlain water and were still alive after 7 days. In con-trast, less than 2% (1.2±1.1%) of larvae that settled in Lake George water survived for the same time period (Table 3). Initial settlement was 1-2 times lower in Lake George water than in water from Lake Champlain (Table 3).

Effect of Calcium Concentration and Calcium Concentration and pH Adjustment on Zebra Mussel Veliger Settlement and SurvivalAmendment of Lake George water with calcium to concentra-tions expected to support the growth of zebra mussels (14.6 to 30.9 mg/L) led to significant improvement in the initial settle-ment (1 day) of larvae (ca. 60%) compared with unamended Lake George water (Table 3). Survival of settled larvae after 7 days was also significantly increased in calcium-amended treatments (p<0.001), but the actual improvement was only 13% relative to unamended Lake George water (Table 3). However, amendment of Lake George water with calcium alone never allowed the initial settlement or survival of lar-vae after 7 days to equal that observed in Lake Champlain water (Table 3).

Adjustment of both pH (to 7.97) and calcium concentration (to 16.1 mg/L) of Lake George water to match Lake Cham-plain water improved initial larval settlement to equal that in Lake Champlain water (Fig. 6). However, in this bioassay, larval survival declined more rapidly in the pH and calcium amended Lake George water as compared to Lake Champlain water, such that after 7 days only 2.4% of the larvae in the amended Lake George water survived while 24.5% survived in Lake Champlain water (Table 3). After 9 days all of the larvae in the amended Lake George water had either died or been dissolved (Fig. 6).

DiscussionIn this study we investigated the patterns of introduction of zebra mussel larvae into Lake George, NY, conducted bioassays to determine water quality parameters that cur-rently limit zebra mussel colonization of Lake George, and

Figure 6.-Effect of calcium and pH adjustment on larval settlement and survival in water from Lake George, NY. Settlement and survival of zebra mussel larvae collected from Lake Champlain, VT in water from Lake Champlain (), unamended water from Lake George (), and in Lake George water amended with respect to calcium and pH (final calcium concentration = 16.1 mg/L, pH = 7.97: ). Regression coefficients for unamended Lake Champlain, Lake George, and amended Lake George water are 0.97, 0.99, and 0.99, respectively. Error bars represent the standard deviation of triplicate samples.


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monly in May, August, and September. Spawning peaks of zebra mussels regionally, including Lake Champlain, generally occur in late July and early August, but larvae are detected from June through September (Garton and Haag 1993, M. Stickney, Vermont DEC, pers. comm.) Thus, de-tection of zebra mussel larvae in Lake George is consistent with either the direct introduction of larvae or the introduc-tion of reproductively mature adults. However, based on the observations made during this study, it was not possible to conclude whether larvae or adult mussels were transported and introduced into Lake George. Alternatively, it is possible that small colonies of zebra mussels are present in the lake, although during extensive survey efforts for mussels, adults were never observed in the lake except at King Neptune’s in 1999 (where veligers were never observed). The lack of adults, or even shells, in the lake might suggest that larvae were introduced directly. However, it seems implausible that a sufficient number of veligers could have been introduced directly such that they would be observed in a randomly collected 200-L plankton sample. Other investigators have speculated that introductions of adult mussels is a more likely pathway than the introduction of larvae since spawning adults could produce large numbers of larvae once they were introduced (Carlton and Geller 1993, Johnson and Carlton 1996, Johnson et al., 2001). However, to our knowledge no studies have established how many larvae are required to initiate successful new colonization by zebra mussels, or any other veliger-producing bivalve, in a pristine habitat. Miller and Haynes (1997) reported that zebra mussel populations failed to become established in a creek (Salmon Creek) that drains the Erie Barge Canal in New York State, even though this creek apparently provides suitable habitat structure, water quality, and nutrients to support zebra mussels. Although the Erie Barge Canal is heavily populated with zebra mussels and contains high larval concentrations, Miller and Haynes (1997) found that <1% of the larvae present in the Erie Barge were transported into Salmon Creek, even though this creek was only 100 m from the canal. It was hypothesized by these authors that larvae were retained by an intervening wetland between the canal and the creek. These observations sug-gest that relatively large numbers of zebra mussel larvae are required to ensure colonization by zebra mussels, even when apparently ideal habitat and water quality conditions exist.

Bioassay studies demonstrated that larval survival and growth is a limiting factor for zebra mussels in Lake George. Adult mussels survived as well as or better in Lake George water than mussels maintained under identical conditions in water from either the Hudson River or in Artificial River Water. However, animals maintained in Lake George water did not grow as large as those in Hudson River water, implying that differences between the water chemistry and/or supplemental food resources present in Hudson River water were respon-sible for observed differences between growth. Qualitative visual comparison between zebra mussels from these studies

suggested higher shell erosion rates in the animals from Lake George water (the shells appeared to be much thinner in the mussels grown in Lake George water). This observation suggests that had the experiment been continued for a longer time period, higher mortality rates may have occurred in the Lake George water.

Although adult mussels were able to grow and survive in water from Lake George, the survival of larvae was marginal compared to survival in water from Lake Champlain. Initial larval settlement in Lake George water was approximately half that of Lake Champlain water, and survival after one week was <2%. Calcium supplementation and pH adjust-ments of Lake George water improved initial settlement but did not significantly increase larval survival compared to survival in Lake Champlain water under identical experi-mental conditions. These observations suggest that in addi-tion to calcium and pH, other factors also limit survival of zebra mussels in Lake George. Magnesium is essential for the growth and development of zebra mussel shells (Dietz et al. 1994); thus the low availability of magnesium may have reduced the survival of zebra mussels in Lake George water. Although calcium limitation was relieved in amendment bioassay treatments, no additional magnesium was added so that the calcium-to-magnesium ratio in these studies was significantly higher than that normally present in either water from Lake Champlain or unamended Lake George water (Table 3). Alternatively, trace nutrients or specific algal and bacterial prey may have been limiting to zebra mussel larvae in Lake George water.

The results of these bioassay studies provide experimental confirmation of predictions based on the physiological re-quirements of zebra mussels that suggest Lake George is not an ideal habitat for zebra mussels. These results are remark-ably consistent with predictions made using the principle component model developed by Ramcharan et al. (1992a) us-ing 10-year average water chemistry data from Lake George (pH, calcium, magnesium, and nutrient concentrations). In this statistical model, Lake George is placed at borderline-to-low risk for zebra mussel colonization due to moderate water alkalinity. However, other risk factors not considered by this model, including human activity levels and the proximity of Lake George to zebra-mussel-inhabited lakes and rivers, are likely to have increased the probability of zebra mussel introductions into the lake (Koutnik and Padilla 1994, Buchan and Padilla 1999, Kraft and Johnson 2000, Bossenbroek et al. 2001). Additionally, microhabitats in the lake may have elevated calcium and magnesium concentrations that would permit the establishment of zebra mussels in Lake George. For example, tributaries and culverts that drain groundwater and/or surface runoff into the lake often contain substantially higher calcium concentrations than average lake conditions (Fuhs 1972, Sutherland et al. 1983). Similarly, areas where Cambrian calcium-containing sandstones are exposed, and


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areas where high numbers of native unionid mussels are found, may provide suitable habitat and sufficient calcium to permit zebra mussel colonization. Alternatively, although it is not known whether zebra mussels might be able to ac-climate to slightly lower calcium concentrations, as they have been able to acclimate to seasonal temperatures in North America (McMahon 1996), this possibility seems within the realm of possibility for D. polymorpha and is worthy of further research.

Since the first report of zebra mussel veligers in Lake George in 1995 followed by the discovery of a small population of adult mussels in the southern part of the lake, an active local education and outreach program was developed and imple-mented. Activities have included posting signage at all public boat launches and public marinas, development and distribu-tion of educational information about zebra mussels and other invasive species, presentation of numerous public lectures, publication of newspaper articles, and informal discussions with local residents, organizations, and tourists.

Interestingly, although it is difficult to quantitatively assess the efficacy of education and outreach programs, after these efforts to increase public awareness were begun, the fre-quency of zebra mussel veliger observations in Lake George decreased from 21 individual veliger sightings in 1995 to only 7 from 1996-2003. These results are at least consistent, if not supportive, of the hypothesis that education and outreach efforts are effective for limiting introductions of zebra mus-sels into Lake George. Similarly, other investigators have concluded that education and outreach programs are effective for slowing the spread of exotic species in general (Dove and Wallis 1981), and zebra mussels in particular (Buchan and Padilla 1999).

Based on the results of these studies, a comprehensive general management strategy for reducing the risk of zebra mussel colonization in Lake George was formulated and imple-mented (Lake George Park Commission 2003, 2004). Over the period of this study, ad hoc education and zebra mussel watch programs, initiated to respond to the threat of zebra mussel colonization of Lake George, were consolidated under the auspices of a lake-wide “Zebra Mussel Task Force.” This group incorporates a broad-based partnership between pub-lic, private, and academic organizations united by a shared interest in the preservation of Lake George. Activities being carried out include continued lake-wide monitoring, a public education and reporting program, maintenance of public boat washing and inspection stations, and a rapid remedia-tion response plan if sightings of zebra mussels are reported in the lake. Results of this current study, demonstrating the importance of calcium in limiting recruitment of zebra mus-sels in the lake, have heightened awareness regarding the use of calcium-based road de-icers that drain into Lake George and the importance for development and construction plans

that mitigate calcium input from groundwater culverts or construction projects.

However, despite aggressive education and prevention programs, some level of zebra mussel introduction in Lake George is perhaps inevitable; therefore, the possibility exists of the establishment of zebra mussel populations. Because in this study we were able to identify the most probable intro-duction points and demonstrate poor survival of introduced and autochthonously produced larvae, we concluded that if introductions could be limited and colonization events detected early, even moderately successful removal efforts would considerably reduce the possibility of permanent estab-lishment of zebra mussel populations in the lake. Therefore, in addition to monitoring for the presence of zebra mussel larvae, recruitment, and adult populations, a rapid response plan to remove any adult zebra mussels has been developed. Although such an approach may not be successful in bodies of water with highly favorable water quality conditions, or a very large number of at risk introduction sites, in water bodies with borderline water quality conditions such as Lake George, this strategy may ultimately prevent the permanent establishment of zebra mussels.

AcknowledgmentsWe gratefully acknowledge Larry Eichler, Geoff Sowan, and Bahram Momen for technical assistance. Several under-graduate research interns including Aaron Williams, Bryce King, David Dunlop, Christin Reynolds, Laura Hanlon, Eric Paparatto, and Alicia Olson contributed to these studies. This work is the result of research funded by the National Oceanic and Atmospheric Administration (award Nos. NA76RG0499 and NA46RG0090) to M.E. Frischer and S.A. Nierzwicki-Bauer through the auspices of the Research Foundation of the State University of New York for New York Sea Grant. The Helen V. Froehlich Foundation also provided substantial support for this research. The U.S. Government is autho-rized to produce and distribute reprints for governmental purposes notwithstanding any copyright notation that may appear herein. The views expressed herein are those of the authors and do not necessarily reflect the views of the Na-tional Oceanic and Atmospheric Administration or any of its sub-agencies.

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