Zebra Mussel Dispersal in Lake-Stream Systems: Source-Sink Dynamics?
Author(s): Thomas G. Horvath, Gary A. Lamberti, David M. Lodge, William L. Perry
Source: Journal of the North American Benthological Society, Vol. 15, No. 4 (Dec., 1996), pp.
564-575
Published by: The North American Benthological Society
Stable URL: http://www.jstor.org/stable/1467807
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J. N. Am. Benthol.Soc.,1996,15(4):564-575
? 1996by The NorthAmericanBenthologicalSociety
Zebra mussel dispersal in lake-stream systems:
source-sink dynamics?
THOMAS G. HORVATH, GARY A. LAMBERTI, DAVID M. LODGE, AND
WILLIAM L. PERRY
Departmentof BiologicalSciences, University of Notre Dame, Notre Dame, Indiana 46556 USA
Abstract. We investigated the ability of zebra mussels (Dreissenapolymorpha)
to colonize small
streams (<30 m wide), which have been consideredto have low susceptibilityto invasion.We examined Europeanliteratureconcerningriverinemussel populationsand sampled lake and stream
sites in the St. JosephRiverbasin (Indiana-Michigan,USA) for mussels. The presenceof colonized
upstreamlakes (ratherthan streamsize) was the criticalwatershedfeaturedeterminingzebramussel
invasion of streams because such lakes served as a source of veligers that drifted into outflowing
streams.For all sites, there was a significantpositive association(p < 0.001)between zebramussel
presencein lakes and in theiroutflowingstreams.Two streamsin the St. JosephRiverbasin (average
widths: 20 m and 7 m) had mussel densities that declined exponentiallyfrom >1000/m2 at the lake
outletto about10/m2 within 1 km downstreamof the colonizedlake,althoughisolatedmusselswere
foundup to 12 km downstream.Thispatternpersistedfor3 y (1993-1995)with no substantialchange
in mussel distributionor abundance.Streampopulationsappearnot to be self-sustaining,but rather
they rely on an upstream source of larvae.Our findings suggest that zebra mussel distributionsin
flowing water ecosystems are best describedby a source-sinkmodel, wherein streams("sinks")are
the recipientfor larvalmussels producedin lakes ("sources").
lake-streamlinkages,source-sinkdynamics,larKeywords: zebra mussels, Dreissenapolymorpha,
val dispersal,exotic species.
Zebra mussels (Dreissenapolymorpha)have become familiar benthic inhabitants of aquatic ecosystems in North American east of the Mississippi
River. Since the 1988 discovery of zebra mussels
in North America (Hebert et al. 1989), studies documenting their ecological impacts and spread
have concentrated almost exclusively on lakes and
large rivers. For example, negative effects of zebra
mussels on native clams (Unionidae) in the Great
Lakes (Hunter and Bailey 1992, Haag et al. 1993,
Gillis and Mackie 1994) and colonization of unionids in the Mississippi River (Tucker et al. 1993)
have been reported. Attempts to predict the
spread of zebra mussels in North America also
have focused on lakes (Strayer 1991, Neary and
Leach 1992, Koutnik and Padilla 1994) and large
rivers (Mellina and Rasmussen 1994). In particular, these studies based susceptibility to invasion
on physical and chemical variables (e.g., water
temperature, calcium concentration,pH, availability of colonizable substrata). Predictions of mussel
population dynamics also have concentrated on
lakes. For example, Ramcharan et al. (1992) used
calcium, phosphate, and lake surface area as predictors of zebra mussel population dynamics in
lakes.
In comparison to lakes and rivers, the ecology
of zebra mussels in streams has received little attention (except for a theoretical treatment by
Mackie 1995); perhaps due in part to the suggestion by Strayer (1991) that zebra mussels are unlikely to colonize streams less than 30 m wide.
This prediction was based on Strayer'sreview of
the European literature in which he found that
only 1 of 171 riverine sampling sites less than 30
m wide contained zebra mussels. In contrast, 70%
of the European rivers larger than 30 m wide were
colonized. Although this relationship was strong
statistically, mechanisms responsible for this distribution pattern in European rivers were not proposed (Strayer 1991).
This pattern of distribution could be related
to the unique problems posed by lotic environments for benthic animals that produce planktonic gametes or larvae (Schneider and Lyons
1994), perhaps most importantly that propagules are carried away from their parent population by stream flow. Adult zebra mussels are
benthic, fertilization occurs externally, and
planktonic larvae remain in the water column
for 2-4 wk (Sprung 1989), during which time
they disperse by drifting and swimming (Stanczykowska 1977, Lewandowski 1982a). Although drift is an effective dispersal strategy in
564
1996]
ZEBRA MUSSELS IN LAKE-STREAM SYSTEMS
lakes, in lotic environments rapid downstream
transport might carry larvae far away from their
parent population. Unlike other stream invertebrates that can recolonize upstream reaches
(e.g., aerial adult stage of insects), zebra mussels
lack a mechanism to offset the loss of larvae to
downstream drift. Zebra mussel populations in
streams would then require an upstream source
of larvae to maintain local populations or the
populations would be lost (Mackie 1995). On the
other hand, if larvae (from the lake or stream)
can be retained and survive at least short distances downstream, and also settle, grow, and
reproduce, then zebra mussels might progressively colonize downstream areas over multiple
generations. These possibilities emphasize the
importance of considering zebra mussel populations in streams in the context of population
sources and sinks (sensu Pulliam 1988).
The role of lakes as possible upstream sources
of zebra mussels in streams has been overlooked in predictions of zebra mussel invasion
and distribution, although the importance of
reservoirs and other impoundments on rivers
has been considered (Mackie 1995). Colonized
lakes might act as a source of zebra mussel larvae for downstream habitats, and thus be important landscape features in determining basin-wide distributions of zebra mussels. At least
3 conceptual models to predict the distribution
of zebra mussels in river ecosystems emerge
from these considerations: 1) the "large-river"
model, which predicts that zebra mussels will
only inhabit rivers greater than 30 m wide
(Strayer 1991), 2) the "source-sink" model,
which predicts a short-distance dispersal from
colonized lakes to outflowing streams, and 3)
the "downstream-march" model, which also depends on an upstream source but predicts a
progressive, unrestricted spread of zebra mussels due to recruitment from instream mussels.
Proposedmodelsof dispersal
For the large-river model, we considered all
streams greater than 30 m wide to be colonizable by zebra mussels, although only 33% of the
European rivers with widths of 30-100 m were
found to contain zebra mussels whereas 83% of
rivers greater than 100 m contained mussels
(Strayer 1991). Thus, this projection is a liberal
prediction of mussel distribution. Although
stream width likely is correlated with other
565
physical characteristicsof streams (e.g., current
velocity, primary production, and suspended
sediment load), Strayer(1991)only mentioneda
stream-widthcriterion.Thus, in this model we
consideronly stream width as the variablepredicting zebra mussel distribution.
In the source-sink model, we considered
lakes to be likely points of initial zebra mussel
introductionin drainage basins. Boating traffic
is a majorvector in zebra mussel spread (Carlton 1992), and large lakes with public boat
launcheslikely receiveheavy use by recreational
boaters. Colonized lakes that have an outflowing streamcould then become points for further
spread because zebra mussel larvae can be
transported downstream by currents. Lakes
meeting the following criteriawere predictedto
be future sources for zebra mussel spread into
outflowing streams: surface area of 100 ha or
more, a public boat launch, and an outflowing
stream. Mackie (1995) proposed that the dispersal distance of veligers in rivers is the product of mean current velocity (e.g., 0.1 m/s =
8.64 km/d) and larvaldevelopmenttime (20-30
d), which suggests that larvae could be transported long distances downstream (>100 km).
However, we project that downstream colonization distancewill be short for severalreasons.
First, zooplankton densities in lake-outlet
streams typically decline with distance downstream of lakes (Ward1975),possibly due to filtration by benthic filter-feeders(Armitage and
Capper 1976). Second, other forms of retention
in the stream (e.g., impingement on surfaces,
trapping by sediments or along stream margins) should also reduce larvalabundancewith
distance downstream (Chandler1937, Richardson 1991). Third, high mortality characterizes
the transitionfrom the planktonicto the benthic
habitat (Lewandowski1982b),which combined
with a decline in larvalnumbersshould reduce
the number of adult mussels with distance
downstream. Fourth, filter-feeder densities in
lake-outletstreamsdecline with distancedownstreambecause of declining food quality(Carlsson et al. 1977, Sheldon and Oswood 1977,
Richardson and Mackay 1991). Under the
assumptionthat streampopulationsare not selfsustaining ("sinks"), this model predicts that
zebra mussel populationsin lake-outletstreams
of "colonizable"lakes should be limited to a
short distance downstream of the source population. This model also predicts that large riv-
566
T. G. HORVATHET AL.
ers will be colonized downstream of dams because such impoundments mimic lentic conditions that likely favor larval production and maturation (Mackie 1995).
The downstream-march model also considers lakes to be primary sources of zebra mussel
larvae, but downstream colonization distance is
projected to be great. Instream mussel populations, which are sinks for upstream lake
sources, could produce veligers for recruitment
to populations further downstream. Given that
veligers can survive downstream transport under some conditions (Borcherding and De Ruyter van Steveninck 1992, Kern et al. 1994), zebra
mussels could sequentially colonize downstream reaches. Thus, this model predicts that
zebra mussel dispersal will be ad infinitum
downstream of lakes.
For all 3 models we assume that the physicochemical environment in the streams is suitable for zebra mussels. For example, acid
streams, calcium-poor streams, or streams lacking suitable substrata likely would not be colonized even if an upstream source population existed. In this paper, we evaluate these 3 models
by conducting a reanalysis of the European literature examined by Strayer (1991), a survey of
44 lake and stream sites in the St. Joseph River
basin (Indiana-Michigan, USA), and an intensive study of 2 lake-stream systems within that
basin that are currently undergoing colonization
by zebra mussels.
Methods
We first reanalyzed the literature surveyed by
Strayer (1991) (citations provided by D. L. Strayer, Institute of Ecosystem Studies, personal
communication: Jonasson 1948, Mann et al.
1972, Giudicelli et al. 1980, Bless 1981, Rosillon
1985, Bournaud et al. 1987, Braukman 1987, Doledec 1989). These papers were searched for information about: 1) the presence of zebra mussels in rivers, 2) the presence of upstream lakes,
and 3) whether those lakes contained zebra
mussels. We often had to consult maps and other literature (e.g., Becker et al. 1992) to locate
upstream lakes and to confirm zebra mussel
presence in the lakes. Each river was counted
only once even if it was mentioned in multiple
studies or had multiple sampling sites. However, we could not control for the higher probability of detecting zebra mussels in large rivers
[Volume 15
than in small rivers because large rivers were
usually sampled at multiple sites, or because
large rivers are more likely than small riversto
have a headwaterlake.
We also conducteda field survey of lakes and
streams within the St. JosephRiverbasin of Indiana-Michigan(describedbelow).Wecollected
data on presence-absenceof zebramussels from
38 streamsites and 6 lakes in Juneof 1993,1994,
and 1995.
Data on zebra mussel presence in lakes and
streams from all sources were pooled and arranged in a 2 X 2 contingencytable with variables being lake (binary states of colonized or
not colonized by zebra mussels) and stream
(also colonized or not colonized by zebra mussels). A stream lacking an upstream lake was
categorizedas having an uncolonizedupstream
lake. Data were analyzed without regard to
channel width. A Pearson'sChi-squarestatistic
with a Yate'scorrectionfor low sample size of
some cells (Sokal and Rohlf 1995) was used to
test the null hypothesis of independenceof zebra mussel presencein lakes and theiroutflows.
St. JosephRiverbasinsurvey
The St. JosephRiverbasin flows into southern
Lake Michigan (mean annual discharge, 120
m3/s) and has a drainage area of about 12,000
km2 in northern Indiana and southwestern
Michigan (Fig. 1). The basin occupies mostly
glacial till and outwash plains, and is characterized by many kettle lakes, and streams up to
6th orderin size. Waterchemistry(dissolvedoxygen, conductivity,pH, calcium concentration;
APHA 1992) and physical variables(mid-channel depth, mid-channel velocity, substratum
composition,and watertemperature)were measured within a 3-wk period in June of 1993 at
the 44 sampling sites scatteredthroughoutthe
basin to characterizeboth streams and lakes
(Fig. 1). In addition, 3 replicatewater samples
were collected from mid-channelof streams or
epilimnion of lakes in sterile sampling bags,
subsampled (300 mL) and filtered in the laboratory,and analyzed for chlorophylla (acidification method) and total suspended solids as
dry mass (APHA 1992).
Zebra mussels were first reported in the St.
JosephRiverbasin in 1991 in Eagle Lake (Cass
County, Michigan) and Lake Wawasee (Kosciusko County,Indiana)(Fig. 1). Eachlake is con-
1996]
ZEBRA MUSSELSIN LAKE-STREAMSYSTEMS
567
St. JosephRiver
FIG. 1. Samplingsites in the St. JosephRiverbasin (SJRB)shown by black dots. Zebramussels were found
only in 2 lake complexes (A and B) and their outflowing streams. Insets: (A) Sites sampled for adult zebra
mussels in ChristianaCreekand its upstreamlakes. (B)Sites sampledfor adult zebramussels in TurkeyCreek
and its upstream lakes. Direction of water flow is shown by arrows and dams on the mainstem of the St.
JosephRiverare shown by blackbars.
nected to an outflowing stream by an intermediate lake. Christiana Creek drains the Eagle
Lake complex (Fig. 1A) and Turkey Creek
drains the Lake Wawasee complex (Fig. 1B). We
first detected zebra mussels in these outflowing
streams in September 1993. A longitudinal survey of the streams for zebra mussels was conducted in September of 1993, 1994, and 1995.
Stream sampling sites were established at distances of 10-1000 m downstream of the lake
outflows and then at easily accessible points
downstream (Fig. 1). In 1993, a single crossstream transect (1 m wide) was surveyed at each
site, whereas in 1994 and 1995 3 transects (each
1 m wide) were surveyed at each site. From each
transect, we collected 3 whole rocks (5-60 cm
diameter, haphazardly selected), all unionids
encountered, all large wood debris (>10 cm diameter), and 3 individual macrophyte stems
(where present, haphazardly selected). In 1994,
we noticed mussels colonizing fine gravel (3-5
cm diameter) in the streams; and in 1995, core
samples (15 cm diameter) also were taken to
sample finer gravel. All zebra mussels were removed from the substrata and preserved on site
in 95% ethanol. Dimensions (length x width X
height) of the exposed surface of each substratum were recorded. Overall composition of
stream bed material was estimated visually by
snorkeling in each transect. Mussels were counted in the laboratory and average mussel densities were calculated as adult mussels/m2 of exposed substratum surface. Zebra mussel densities from the 2 streams were regressed against
distance downstream. For fit to a linear model,
both mean mussel density and distance downstream were log-transformed.
The 4 colonized lakes in the basin were sampled between 28 July and 3 August in 1993,
1994, and 1995. To derive estimates of zebra
568
T. G. HORVATHET AL.
[Volume 15
TABLE 1. Zebra mussel colonization of lakes and
their outflowing streams in European studies examined by Strayer (1991) and in the St. Joseph River basin
of Indiana-Michigan.
lake density was calculated by averaging section
density estimates.
Based on criteria of the 3 models, we plotted
the predicted zebra mussel distributions on
maps of the St. Joseph River drainage. We obUncolontained stream width information from our baColonized ized lake
sin-wide survey and from maps, and data on
lake
or no lake
lake surface area and presence of public boat
Colonized outflowing
launches were obtained from publications of the
stream
5
0
Department of Natural Resources in both IndiUncolonized outflowing
ana and Michigan. The presence of a perennial
stream
0
59
outflowing stream was determined from maps
and verified with a site visit. Predictions of zebra mussel distributions in the St. Joseph River
mussel density on benthic surfaces within the basin, based on the 3 models, were compared
epilimnion,we divided each lake into 4 sections with zebra mussel distributions determined
of about equal size; each section was stratified from our basin survey.
by 0.25, 0.5, and 0.75 of the epilimneticdepth.
At each of the 3 depths, SCUBA divers made
visual estimates of the bottom composition
along one 50-m long x 1-m wide transect
aligned parallelto the shore.Becauseof the predominantly mud and sand bottom of these
lakes, macrophyteswere the primary substratum for zebra mussel attachment.From 1 randomly selected transectof each section,all macrophytes from a 0.0625-m2quadrat dropped
haphazardlywere collected and bagged underwater.In the laboratory,macrophyteswere separatedby species, zebra mussels were removed
from the macrophytes, and wet weight was
measured for each macrophytespecies. Surface
area of macrophytes was determined from
mass-areaequationsin Brownand Lodge (1993)
and zebra mussel density was calculated per
unit of macrophytesurface area. Mean whole-
Results
From our analysis of the European literature
and our survey of the St. Joseph River basin (Table 1), we rejected the null hypothesis that
stream and lake invasions are independent
events. There was a significant association between zebra mussel presence in streams and
their presence in upstream lakes (X2 = 64.0, df
= 1, p < 0.001). No streams lacking an upstream lake source were colonized by zebra
mussels, whereas all streams below colonized
lakes contained zebra mussels (Table 1).
Water chemistry throughout the St. Joseph
River basin was suitable for zebra mussels (Table 2). However, by 1995 zebra mussels had colonized only 2 lake-stream complexes of the basin (Fig. 1). The colonized lakes had little hard
TABLE 2. Physical and chemical attributes of tributaries to the St. Joseph River during June 1993. Literature
values are ranges suitable for D. polymorpha.NK = not known from the literature.
Parameter
Mean
Range
Literature
Dissolved oxygen (mg/L)
Conductivity (JiS/cm)
pH
Mid-channel depth (m)
Mid-channel velocity (m/s)
Water temperature (?C)
Calcium (mg/L)
Suspended chlorophyll a (j.g/L)
Suspended phaeophytin a (,ig/L)
Total suspended solids (JLg/L)
8.4
501
8.0
0.91
0.41
19.1
177
9.2
60.0
538.6
2.9-11.0
351-715
7.5-8.5
0.14-4.30
0.01-0.76
13.2-26.9
96-268
0.7-41.7
0-151.4
1.8-2639.1
>1.8a
NK
7.4-9.4a
NK
NK
2-30 (Adults)b
>12c
a
c
Sprung 1987, b Smirnova et al. 1993, Vinogradov et al. 1993, d Jantz and Neumann 1992
>3d
NK
NK
569
ZEBRAMUSSELSIN LAKE-STREAMSYSTEMS
1996]
TABLE3. Characteristics
of the lake-streamcomplexesin the St.JosephRiverbasin containingzebramussels.
Streamsites are distancesdownstreamof lake outlets.Soft substratumis mud and sand, and hard substratum
includes rock particlesizes >2 mm diameter(graveland larger)and large wood debris.Macrophyteincludes
macroalgae(Chara,Nitella).Percentcoverestimatesdo not include sedimentsunder macrophytes.
Channel Average Average
Surface width discharge velocity
Site
area (ha)
Eagle Lake
Christiana Lake
153
72
()
-
ChristianaCreek
10 m
100 m
400 m
1740 m
1750 m
3880 m
10,470m
-
20
21
15
34
34
17
19
2.23
1.99
1.80
0.80
1.58
2.39
2.20
7
2.96
18,330 m
Lake Wawasee
Syracuse Lake
1238
167
((m3
--
-
Percentcover of bottom
Average
MacroSoft
Hard
phyte
2
53
89
<<1
<<1
47
11
0.21
0.15
0.14
0.07
0.25
0.24
0.26
0.84
0.78
0.76
0.52
0.27
0.77
0.55
33
10
30
80
<1
47
48
31
50
10
<1
90
53
2
36
40
60
20
10
0
50
0.86
-
0.43
7
4
5
31
23
95
<1
<1
0
69
77
0.10
0
0
10
100
50
20
100
100
30
0
50
80
0
0
60
0
0
0
(m
(m/s)
depth (m)
-6
TurkeyCreek
10 m
100 m
400 m
1000 m
3700 m
6800 m
-7
-9
-
6
3
7
7
-
substrata available for zebra mussel colonization
(Table 3). In contrast, the colonized outflowing
streams had plentiful hard substrata, with the
exception of an area immediately upstream of a
small dam in Christiana Creek and at the 400-m
and 1000-m sites in Turkey Creek (Table 3). The
abundant macrophytes in the lakes (Table 3)
were colonized by zebra mussels, but mussels
rarely were found on lotic macrophytes. Zebra
mussels covered entire exposed surfaces of rare
hard substrata in the lakes, whereas they were
found mainly on the sides and underside of
hard substrata in streams.
In both outflowing streams, zebra mussel
densities were highest near the lake outlet and
declined exponentially with distance downstream (Fig. 2). Maximum densities of zebra
mussels in the streams were 1400/m2 in Christiana Creek and 3300/ m2 in Turkey Creek. Mussel densities in 1994 generally were lower than
in 1993 in both streams, but densities recovered
in Christiana Creek in 1995. No mussels were
found below 400 m in Turkey Creek in 1993 but
we collected isolated mussels 10 km down-
-0.15
-
0.60
0.35
-0.55
-0.60
stream in 1994 and 12 km downstream in 1995.
Mussels were found only 2 km downstream of
the lake in 1993 in Christiana Creek, but were
detected 4 km downstream of the lake in both
1994 and 1995.
Models of dispersal
The large-river model, which is based only on
the 30-m width criterion, predicts that zebra
mussels will colonize about 80% of the mainstem of the St. Joseph River and about 50% of 2
large tributaries (Paw Paw and Elkhart rivers)
(Fig. 3A). However, our sampling has detected
neither adult nor larval zebra mussels in these
rivers. The source-sink model predicts that zebra mussel distribution in the streams of the St.
Joseph River basin will be restricted to short distances (10 km used for this drainage, based on
Fig. 2) downstream of colonized lakes and
downstream of dams in the mainstem of the St.
Joseph River (Fig. 3B). In contrast, the downstream-march model predicts that zebra mussels will colonize most of the St. Joseph River
570
T. G. HORVATHET AL.
TurkeyCreekComplex
ChristianaCreekComplex
5
\
3 -
v^
2-
1 -
1-
-
OI
I
I
I
1994
4 -
0(^
0)
(0
0)
Cn
3-
E
2-
L.
1-
N
6
y=3.41-0.90x
p=0.041
~
I
I
I
I
W
I
1994
0
y=3.02-0.52x
p=0.429
5
4
3
'?
\
2
-
1
1*4
-
o1
-1
-1
7
I
C)
y=4.32-0.81x
p=0.014
\.K
i
3-
I
O1993
~(DT)?
4-
2-
-1
5
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5
1993
y=4.39-0.94x
p=0.039
-i-
[Volume 15
I
I
I
I
I
-9L
9I I
0
-1
0
0
Ah
-1
3
_
4
3
2
2
1
1
0
0
-1
-1
ELCL-2
-1
0
1
2
LWSL-2
1
2
Lakesand log distancedownstream(km)
FIG.2. Adult zebra mussel densities in the 2 lake-streamcomplexesin the St. JosephRiverbasin in 1993,
1994, and 1995. Errorbars are +1 SE. Filled circles are stream sites; open circles are lake sites. Regression
analysis was restrictedto stream sites. EL = Eagle Lake,CL = ChristianaLake,LW= LakeWawasee,and SL
= Syracuse Lake.
and its main tributaries because of numerous
headwater lakes and the model's assumption of
unlimited downstream dispersal (Fig. 3C). Thus
far, 2 streams (Christiana Creek and Turkey
Creek) have been colonized in the St. Joseph
River basin, but both streams are colonized only
within a short distance downstream of their
lake source. We did not sample for adult mussels in the mainstem of the St. Joseph River
downstream of the dams, but veligers have not
been observed in plankton samples.
Discussion
A source-sink modelfor lotic systems
Our data from the St. Joseph River basin are
more consistent with the source-sink model than
1996]
ZEBRA MUSSELS IN LAKE-STREAM SYSTEMS
A. Large river
FIG. 3. Predicted zebra mussel distribution (heavy
lines) in the St. Joseph River basin based on (A) the
minimum channel width of 30 m suggested by Strayer
(1991), (B) our criteria of the presence of a colonizable
headwater lake and a short downstream dispersal distance (10 km used for this drainage, but distance
downstream will vary depending on stream size and
other characteristics) from lakes and impoundments
(see Fig. 1 for location of dams), and (C) our criteria
of the presence of a colonizable headwater lake and
unlimited downstream dispersal distance due to recruitment from instream populations.
571
with the other 2 models, but a definitivetest of
the source-sinkmodel cannotbe made untilmore
systems are invadedby zebramussels.Dispersal
of zebramussels in basin streamsappearsto be
limited to a short distance(ca. 10 km; see Fig. 2)
from the source population.Only maturelarvae
donatedby lakes are likely to settle and survive
in the outflowenvironment.Immaturelarvaethat
enterthe streamlikelywill be transportedout of
the system before maturing(Mackie1995).Continued exposure to turbulence during downstreamtransportmay cause larvalmortalityand
thus decreasethe numberof viablelarvaedownstream (T. Horvath,unpublisheddata), and the
harsh hydrodynamicenvironmentfound on the
streambed(Silvesterand Sleigh 1985)may affect
survival of newly settled larvae. Although the
source-sinkmodel predictsthat mussels will be
present only a short distance downstream of
dams in the St. JosephRiver,evidencefrom Europeanriverssuggests that mussels can colonize
the entirelengthsof largerrivers(Jantzand Neumann 1992).
Larvaldriftfromheadwaterlakesinto outflowing streams could result in the colonizationof
many streamsand, potentially,downstreamlakes
withindrainagesystems.If zebramusselsareable
to colonizethe entirelengthof streams,a drainage
systemcontainingheadwaterlakescouldbe completelycolonizedin a shorttime (e.g.,see Fig.3C).
However, zebra mussels have been present in
ChristianaCreekand TurkeyCreekfor at least 3
y and they areonly foundin appreciabledensities
within 1 km of theirlenticsourcepopulation.This
distributionis consistentwith other filter-feeders
at lake-outlets,such as hydropsychidcaddisfly
species(Oswood1979)andblackfly speces (Sheldon and Oswood 1977,Wotton1979),and could
be due to food limitationfurtherdownstream.
However,growth rates of enclosed adult zebra
mussels were not significantlydifferentamong
sitesup to 10 km downstreamin ChristianaCreek
(T.Horvath,unpublisheddata).Thus, it appears
that zebramussels are somehow limited in their
ability to colonize or persist long distances in
these streams.
The downstream-marchmodel assumes instream zebra mussel reproduction,but it is unclear if zebra mussels can reproducein lotic environments. Within the stream, successful reproductionmay be low because the planktonic
gametes may be quicklydiluted or may not mix
in unidirectionalflow if there are even small
572
T. G. HORVATHET AL.
spatial or temporal differences in gamete release
(Pennington 1985). If larvae are produced by
stream-dwelling mussels, they likely would be
transported out of the system before maturing
(Mackie 1995). Zebra mussels have been present
in the lake-stream complexes of the St. Joseph
River basin for about 5 y and we have observed
only a slow downstream movement, which suggests that stream mussels are not contributing
to recruitment further downstream. We cannot
rule out the possibility, however, that over a longer time frame (e.g., decades) the source-sink
dynamics may shift to a downstream march.
Stream populations of zebra mussels probably
are not self-sustaining (Neumann et al. 1992), and
therefore must rely on an upstream source of larvae for recruitment (Mackie 1995). Geomorphically, both Christiana Creek and Turkey Creek lack
large pools or backwater areas, which Macke
(1995) mentions as areas where larvae could be
retained to sustain stream populations. In streams
with areas for larval retention, instream production of veligers could seed populations further
downstream, resulting in zebra mussel distributions similar to a downstream march (Fig. 3C).
However, this distribution is still dependent on a
primary source population that is self-sustaining,
such as a headwater lake.
Our study mostly concerned small streams to
moderate-sized rivers. In large navigable rivers,
zebra mussels may colonize and be sustained
from 2 sources: upstream lentic sources (including upstream lakes, impoundments, and large
backwaters) and boating traffic. For example,
the introduction of zebra mussels into the Mississippi River drainage likely was the result of
veligers drifting from Lake Michigan into the
Illinois River. The Detroit, Niagara, and St. Lawrence rivers likely were invaded by veligers produced in upstream lakes St. Clair, Erie, and Ontario, respectively (Griffiths et al. 1991). Impoundments (e.g., locks and dams) also can provide habitats where zebra mussels can establish
dense populations and produce veligers to further seed downstream sites (Mackie 1995).
These upstream habitats may be important
sources of new recruits for sustaining downstream populations. In contrast, the Upper Mississippi, Ohio, Tennessee, and Arkansas rivers
likely were colonized by barges incidentally carrying adult or larval mussels. Barges likely continue to transport mussels that could maintain
upstream populations.
[Volume 15
Streamsize and zebra mussels
Stream size has been used to predict the distribution and abundance of lotic macroinvertebrates because it can affect many attributes of
the lotic environment, such as water temperature, current velocity, substrate composition,
and food resources, that in turn affect invertebrate populations (Minshall et al. 1983). For example, stream size was a useful predictor of
unionid distributions in New York and Pennsylvania (Strayer 1993) and in southeastern Michigan (Strayer 1983). A general paradigm in
stream ecology, the river continuum concept
(Vannote et al. 1980), explains the distribution
of invertebrate functional feeding groups based
partly on stream size (i.e., stream order).
Small streams in general have been viewed as
unsuitable habitat for zebra mussels (e.g., Martel
1996), based largely on Strayer's (1991) literature
analysis. The colonized streams in the St. Joseph
River basin had average widths of 7 m and 20
m (Table 3), suggesting that zebra mussels can
colonize streams with average widths well under 30 m. However, stream zebra mussel densities in the St. Joseph River basin are much lower than those reported from lakes and large rivers. For example, a density of 400,000 mussels/
m2 was reported in Lake Erie (MacIsaac et al.
1991), and 60,000 mussels/m2 were found near
the headwaters of the Rhine River (100 m wide)
in Europe (Cleven and Frenzel 1993). In contrast, a short distance (<1000 m) downstream
of the lake source in Christiana Creek and Turkey Creek, mussel densities rarely exceed 100/
m2. Ecological effects by zebra mussels in
streams have not yet been reported, perhaps because zebra mussel densities in small streams
are too low to have a detectable ecological impact. Zebra mussels had to exceed densities of
1000/m2 to significantly affect unionid clams in
the St. Lawrence River (Ricciardi et al. 1995).
The presence of zebra mussels in streams appears to be dependent more on an upstream
source of larvae than on stream size per se. Our
reanalysis of the European literature reviewed
by Strayer (1991) coupled with our own survey
of the St. Joseph River basin shows that the presence of zebra mussels in upstream lakes is a
critical factor in zebra mussel invasions of
streams and rivers. For example, recruitment in
the Rhine River is dependent on larvae produced in Lake Constance and in areas of long-
ZEBRA MUSSELS IN LAKE-STREAM SYSTEMS
1996]
term water retention(e.g.,behind dams) (Borcherding and De Ruyter van Steveninck 1992,
Kern et al. 1994). Other river systems not included in our analysis also demonstrate the
lake-stream linkage in zebra mussel distributions. Forexample,Statzner(1987)attributedthe
presence of zebra mussels in the Schierenseebrook (Germany)to the upstream lake population. Two other Michigan streams with colonized upstream lakes also have been invaded
recently by zebra mussels: the Huron River (P.
Marangelo, University of Michigan, personal
communication)and the Clinton River (R. D.
Hunter, Oakland University,personal communication).Thus, upstreamsource populationsin
lakes appear to donate mussels, as larval drift,
to downstreamriverinehabitats.
Concludingremarks
Freshwaterecosystems in North Americaare
continuingto be invadedby zebramussels. Our
study suggests that stream populationsare not
self-sustaining,but ratherrely on an upstream
source population. As a result, mussel distributions in small to medium-sized streamsmay
be limited to low-densitysink populationswithin a few km of their lake sources. Previousbeliefs that small streams will not support zebra
mussel populationsrequirereexamination.Given suitable physicochemical conditions, the
presenceof upstreamdonorpopulationsmay be
the criticalfactordeterminingzebramussel distribution in any size of stream. The potential
colonizationof small streamsand the dynamics
of source and sink populations in rivers of all
size should be consideredwhen evaluatingcurrent or projecteddistributionsof zebra mussels
and possibly other exotic organisms.
Acknowledgements
Thisresearchwas fundedthrougha cooperative
agreement(CR820290-01and CR820290-02)with
the US EnvironmentalProtectionAgency (EnvironmentalResearchLaboratory,Duluth, Minnesota) as part of the EPAIntroducedSpeciesResearchProgram.We particularlythankDr.J. David Yountfor his assistanceas EPAprojectmanager.David Strayerkindlyprovidedthe European
literaturecitationsused as part of this analysis,
greatlyimprovedan earlierversionof this manuscript, and clarifiedour thinking about source-
573
sink dynamics. Lydia Skrynnikovareviewed much
of the European literature,Torben Lauridsen provided information on one of the Danish zebramussel-invaded lake-stream systems, and Steven
Beaty, Anna Hill, Kristin Lewis, and James Myers
assisted in collecting and processing samples. Drs.
Robert Bailey, Gerald Mackie, and Rosemary
Mackay, along with an anonymous reviewer, also
provided helpful comments on an earlier version
of this paper.
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