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Open Journal of Ecology, 2021, 11, 163-182
https://www.scirp.org/journal/oje
ISSN Online: 2162-1993
ISSN Print: 2162-1985
DOI:
10.4236/oje.2021.112014 Feb. 22, 2021 163 Open Journal of Ecology
A Review of Zebra Mussel Biology, Distribution,
Aquatic Ecosystem Impacts, and Control with
Specific Emphasis on South Dakota, USA
Brandon Vanderbush1, Chris Longhenry1, David O. Lucchesi2, Michael E. Barnes3
1South Dakota Department of Game, Fish and Parks, Chamberlain, South Dakota, USA
2South Dakota Department of Game, Fish and Parks, Sioux Falls, South Dakota, USA
3South Dakota Department of Game, Fish and Parks, McNenny State Fish Hatchery, Spearfish, South Dakota, USA
Abstract
Zebra mussels
Dreissena
polymorpha
are a native bivalve from eastern Eu-
rope. They were first detected in North America in Lake St. Clair in 1988 and
were presumably introduced via infested ballast
water. Zebra mussels have
spread rapidly across the United States, with 31 states reporting infestations
as of 2019. Zebra mussels were first detected in South Dakota, USA, in 2015
in Lewis and Clark Lake and McCook Lake, with subsequent infestations oc-
curring in Lake Yankton in 2017, Lakes Francis Case and Sharpe in 2019, and
Pickerel Lake, Kampeska Lake, and Lake Cochrane in 2020. This review paper
presents information on zebra mussel biology and control, with specific in-
formation on the waters of South Dakota, USA.
Keywords
Zebra Mussel,
Dreissena
polymorpha
, South Dakota, North America
1. Introduction
The zebra mussel
Dreissena
polymorpha
is a bivalve native to eastern Europe [1]
[2]. It is a small, brown, freshwater mussel with a cream-colored zebra stripe
pattern that varies among individuals [2]. It inhabits large freshwater lakes and
rivers [3] but has also been found in a wide variety of aquatic habitats, including
flooded quarries, cooling ponds, and golf course ponds [4]. Zebra mussels exhi-
bit high fecundity [1] [5] [6] and an ability to attach to a variety of surfaces [7]
[8] [9] [10] that has allowed them to spread quickly and colonize new locations.
Sphaeriidae, Margaritiferidae and Unionidae are the only families of freshwa-
How to cite this paper:
Vanderbush, B
.,
Longhenry
, C., Lucchesi, D.O. and Barnes,
M
.E. (2021)
A Review of Zebra Mussel
Biology, Distribution, Aquatic Ecosystem
Impacts, and Control with Specific
Empha-
sis on South Dakota, USA
.
Open Journal of
Ecology
,
11
, 163-182.
https://doi.org/10.4236/oje.2021.112014
Received:
January 14, 2021
Accepted:
February 19, 2021
Published:
February 22, 2021
Copyright © 20
21 by author(s) and
Scientific
Research Publishing Inc.
This work is licensed under the Creative
Commons Attribution International
License (CC BY
4.0).
http://creativecommons.org/licenses/by/4.0/
Open Access
B. Vanderbush et al.
DOI:
10.4236/oje.2021.112014 164 Open Journal of Ecology
ter mussels native to North America, with Unionidae being the most common
[11]. Zebra mussels belong to the Dreissenidae [11], a mussel family possessing
characteristics not found in native mussels. Dreissenid mussels have planktonic
larvae that do not require a host to develop. In contrast, native mussels must rely
on host species to complete development. In addition, zebra mussels are epi-
faunal, using byssal threads to attach to hard surfaces and substrates not availa-
ble to native mussels, which are infaunal and typically bury themselves in sedi-
ments [11]. Zebra mussels can attach directly to native North American mussels,
which frequently leads to native mussel mortality [11].
Infestation of zebra mussels into new waterbodies is generally believed to oc-
cur during early life stages [12] [13] because of external fertilization of eggs in
the water column [14] [15] and free-swimming larvae [12] [16]. Both eggs and
larvae are capable of movement by either natural or anthropogenic means [17]
[18] [19].
Spawning of sexually mature zebra mussels begins when water temperatures
reach 12˚C [5] [6] [12] [20] with optimal spawning temperatures near 18˚C [20].
Spawning continues as long as temperatures are adequate, even into early fall
[21]. A single female zebra mussel releases 30,000 to 40,000 eggs per spawning
event [1] [5] [6]. Within a year, one female can produce and release over a mil-
lion eggs [1] [5]. Several days after fertilization, free swimming larvae emerge
and disperse throughout a waterbody [16].
Larval zebra mussels undergo multiple stages of development, with corres-
ponding shifts in behavior. Shortly after hatching, larvae, called veligers, develop
velum, an organ used for feeding and movement [15]. Within the first seven
days post-hatching, veligers also develop an unornate D-shaped shell followed
by a more ornate shell a few days later [15]. After shell formation, organs, in-
cluding a foot and gill filaments, develop in the mantle cavity [15]. While gill fi-
laments will not become fully developed until later life stages, the foot is fully
developed at the veliger stage and can be used either for swimming near or
crawling along the bottom [15]. At 16 to 88 days post-hatch, veligers begin to
swim or crawl along the bottom in order to find suitable surfaces upon which to
settle [15].
Although veligers can settle upon a variety of surfaces, survival is influenced
by surface selection. Suitable surfaces are generally hard structures [7] [8] [9]
[10], including both natural surfaces such as rocks [7] [8] [9] and artificial sur-
faces such as cement, steel, or rope [7] [9] [22]. Veligers will also settle upon
macrophytes [8] [15] [23] [24], as well as on other invertebrates [8] [25]. Velig-
ers often have difficulty locating suitable substrate for settling, with mortality
rates as high as 98% [26]. After initial settlement, zebra mussels can relocate to
more suitable locations [10].
Once initial settlement has occurred, veligers secrete byssal threads to attach
to the selected substrate [27] and undergo further development. The velum is
replaced by fully functioning gill filaments and a mouth, and the foot moves to a
new position and increases in size [15]. These developments facilitate the excre-
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of Ecology
tion and formation of the adult shell [15]. However, even after the development
of the adult shell, zebra mussel juveniles are not classified as adults until sexually
maturity [15] [28]. In North America, sexually maturity typically occurs at a
length of approximately 8 mm, which frequently happens after just one year of
growth [6] [21] [25]. Mature mussels commonly congregate into colonies called
druses, which are often located in shaded areas [29]. All sizes of zebra mussels
exhibit negative phototaxis and prefer darker locations [10] [29] such as crevices,
corners and edges [30] [31]. The zebra mussel lifespan is typically between two
and nine years [6] [21] [25] [32].
Although generally considered nonmobile, if conditions become unfavorable,
zebra mussels can detach their byssal threads and use their feet to seek more
suitable habitat [33], particularly rough-textured structures [10]. Juvenile zebra
mussels also have special floating byssal threads allowing them to resuspend into
the water column and drift to new locations [34]. Toomey
et al.
[29] found that
smaller mussels (5 - 10 mm) tend to move a greater distance (e.g. 284 mm) than
larger mussels. Specifically, over a two-hour period, mussels at a length of 5 to 10
mm mussels move 284 mm, compared to mussels at a length of 10 to 20 mm that
moved 115 mm, and those longer than 20 mm that moved 47 mm [29]. While
hypoxic conditions will stimulate movement [10], unfavorable calcium levels
and water temperature will not [29].
The presence of conspecifics reduces zebra mussel movement [35], leading to
their aggregation druses [10]. The formation of druses likely is influenced by the
availability of preferred substrates and a predator-avoidance mechanism [10].
However, druses have the potential to reduce mussel growth and condition due
to the accumulation of wastes and the depletion of dissolved oxygen and food
supplies [36] [37]. If deteriorating conditions in the druse do occur, smaller
mussels exit the druse upward, while larger mussels frequently remain stationary
and die [36] [37] [38].
Zebra mussel survival and growth is greatly influenced by water temperature.
McMahon [20], Cohen [39], and Pollux
et al.
[13] indicate zebra mussel survival
in temperatures ranging from 1˚C to 30˚C, while Spidle
et al.
[40] determined
that they could survive at somewhat higher temperatures in North America. Al-
though zebra mussels can survive, and grow, for short periods at temperatures
greater than 30˚C [20] [40] [41], they cannot survive at temperatures less than
0˚C [13] [20] [39] [40] [41]. Growth generally occurs between 6˚C and 30˚C
[42], with optimal temperatures for growth ranging from 10˚C to 15˚C [43]. Ze-
bra mussels located in relatively deep water tend to grow slower, most likely due
to lower water temperature and reduced food availability [44].
In addition to temperature requirements, adequate calcium levels are also
critical for zebra mussel survival and growth. Minimum calcium concentrations
in the range of 12 to 15 mg/L are required for proper shell development and
growth [20] [39] [45] [46] [47]. Low calcium levels can hinder egg development,
as well as interfere with muscular contraction, nerve function, cellular cohesion,
pH balance, and other aspects of mussel physiology [13] [47] [48]. Mussel cal-
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cium uptake is influenced by pH [47] with a desirable range from 6.5 to 9.5 [42].
Zebra mussels are considered intolerant of low dissolved oxygen [49], requir-
ing minimum values of 4 to 6 mg/L depending on other environmental condi-
tions [42]. As such, the hypolimnion of lakes, impoundments, river floodplains,
or other areas with water containing low dissolved oxygen may not be suitable
habitat for zebra mussels [44] [50]. Other environmental factors that impact ze-
bra mussel growth and mortality include suspended solids, turbidity, and salini-
ty. High suspended solid concentrations and turbidity can hinder zebra mussel
growth by negatively affecting ingestion and clearance rates [51]. Zebra mussels
can tolerate salinity ranging from 0.6 to 12 mg/L [37] [52] [53] with upper lethal
limits dependent on temperature [42] [53]. Environmental factors can affect ze-
bra mussel growth and mortality both by acting independently and in combina-
tion with each other [44] [46] [47] [50].
Zebra mussels feed primarily on algae, but also consume micro-invertebrates,
bacteria, detritus and other organic matter [12]. Food items are obtained by
clearing (filter feeding) particles ranging in size from 0.5 to 1200 µm into the
mantle of the mussel [54] [55]. The preferred size for food items ranges from 15
- 40 µm [56]. Clearance rates are affected by mussel size [57] and temperature,
with the most advantageous rates occurring at temperatures between 14˚C and
26˚C [54]. Clearance rates and food ingestion are also negatively affected by high
levels of suspended solids and turbidity, with clearance rates most notably af-
fected when concentrations of suspended solids are greater than 1 mg/L [51]. In
addition to the effects on clearance rates, increased suspended solids can also in-
crease the production of pseudofeces, which are mucous-coated particles ex-
pelled from the siphon or mantle [51] [57] [58]. Pseudofeces production does
result in increased respiration and energy costs however [51].
2. Distribution and Spread
Zebra mussels are native to eastern Europe, originally occupying areas around
the Volga River and the Aral, Black, and Caspian Seas [2]. Canal construction
during the 1800s facilitated their spread throughout western Europe [1] [2] [19].
Zebra mussels were first reported in North America in 1988 from Lake St. Clair,
Michigan [59], likely having been introduced via ballast water [17] [59] [60].
Within a month they were detected in the western basin of Lake Erie [61] and
have subsequently spread across much of North America. In 1991, zebra mussels
were detected at several locations along the Mississippi River [19] [62] and later
were found in the river all the way from Minnesota to Louisiana [19]. Zebra
mussels are now found in 31 states [63].
The Missouri River, the longest tributary of the Mississippi, bisects the state of
South Dakota and also forms part of the border between South Dakota and Ne-
braska. Zebra mussels were first detected in the Missouri River near Sioux City,
Iowa in 1999 [19] [63]. Zebra mussels were first observed in South Dakota wa-
ters in 2015 in Lewis and Clark Lake, which is the furthest downstream Missouri
River mainstem reservoir [63]. In the same year, adult zebra mussels were also
B. Vanderbush et al.
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of Ecology
found in McCook Lake, a small lake near North Sioux City, South Dakota main-
tained by pumping water from the Missouri River [63]. In 2017, zebra mussels
were detected in Lake Yankton, South Dakota, a manmade lake located adjacent
to the Missouri River, just below Lewis and Clark Lake [64]. Further zebra mus-
sel infestations were not detected again in South Dakota waters until 2019 when
adult mussels were found in Lake Francis Case and Lake Sharpe, two Missouri
River reservoirs immediately upriver from Lewis and Clark Lake [63]. In 2020,
zebra mussel infestations were observed in Pickerel Lake, Lake Kampeska, and
Cochrane Lake, all of which are located in Eastern South Dakota at distances in
excess of 250 km from the Missouri River and its reservoirs. Most of the waters
in South Dakota have the water chemistry and other environmental characteris-
tics suitable for zebra mussels.
Although barge traffic is believed to have facilitated the transportation of ze-
bra mussels upriver in many river systems [18] [19], it is likely not responsible
for mussel introductions into South Dakota waters. Only the lower 1,181 km of
river (Sioux City to the confluence with the Mississippi River), is maintained for
navigation and the Missouri River dams upstream from Sioux City lack locks for
watercraft passage. However, barges may have indirectly facilitated zebra mussel
introduction into South Dakota by transporting them upriver to Sioux City,
Iowa, where that population may have served as a source population for intro-
duction by overland transport to Lewis and Clark Lake or Lake Yankton. How-
ever, it is more likely that water vessels used for recreation, research, or industri-
al work such as construction or bridge maintenance, were responsible for intro-
duction [18] [65] [66]. Both zebra mussel adults and veligers have the potential
to be transported overland under the right conditions [17] [67] [68] [69]. Adult
mussels can attach to boat hulls, motors, and anchors [18] [65] [66], as well as
macrophytes attached to trailers or boats [66]. Under cool, moist conditions, at-
tached adult mussels can survive out of water for four days [17] [67] [68] [69].
Veligers can be transported via standing water in boat bilges, motors, and live
wells [18] [65] [66]. The most plausible explanation for the spread of zebra
mussels in South Dakota is via overland transport by fishing and recreational
boats [18] [66].
While wild animals such as ducks, turtles, fish, and other organisms have the
potential to transport zebra mussels, [18] [70], waterfowl are the most likely
animals to contribute to mussel spread [18] [70]. Although little research has
been conducted, it has been hypothesized that veligers and juvenile mussels
could become trapped within feathers or debris carried on the feathers or feet of
birds [18] [70] [71].
Even though zebra mussels can survive transportation, a single introduction may
not be adequate to establish a population [72]. Even in favorable environmental
conditions, multiple introductions may be needed to establish a self-sustaining pop-
ulation [13] [20] [39] [40] [42] [53] [65] [72] [73]. Thus, waterbodies that are the
closest to existing mussel populations and those most frequented by recreational
users are most susceptible to zebra mussel colonization [74]. In addition, fre-
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quently used waterbodies containing zebra mussels can act as reservoirs facili-
tating zebra mussel spread [65].
3. Impacts on Aquatic Ecosystems
The impact of zebra mussels on aquatic ecosystems in North America has varied
from a dramatic change in trophic state [75]-[81] to virtually no effect at all [76] [82]
[83] [84]. The ability of zebra mussels to increase water clarity is well-documented
[61] [76] [79] [85] [86], however some studies have found little to no change in
water clarity after introduction [83]. In two Ohio lakes, water clarity increased
by 2 m after zebra mussel introduction [79] [86], while an even greater water
clarity increase was observed in the eastern basin of Lake Erie [83]. However, the
western and central basins of Lake Erie did not experience a similar water clarity
increase [83]. Turbidity in the Detroit River decreased by about 33% after zebra
mussel introductions [76], while water clarity in the Hudson River only in-
creased by 7% [76]. In general, holomictic lakes and slow-flowing rivers with lit-
tle water mixing may likely experience a larger increase in water clarity after the
introduction of zebra mussels than meromictic lakes or fast-flowing, highly
mixed rivers [76].
Zebra mussel impacts on phytoplankton have also varied. The mussels have
reduced chlorophyll
a
in a wide variety of water bodies [81] [87] [88] [89] [90]
[91], with a 41% reduction observed in a small lake in Ireland [81]. However, not
all zebra mussel introductions have reduced phytoplankton abundance [84] [92]
[93]. Phytoplankton communities may change because of zebra mussels. De Sta-
sio
et al.
[84] reported a change in the phytoplankton community in Green Bay,
Lake Michigan, from chlorophytes to cyanobacteria and diatoms. Increased
cyanobacteria densities after zebra mussel introduction are not uncommon [76]
[89] [94] [95] [96] [97]. The presence of zebra mussels may be favorable for
blooms of the cyanobacteria
Microcystis
aeruginosa
[94] [95], which they find
unpalatable due to the presence of hepatotoxins or microcystins [93] [98]. Al-
though zebra mussels can alter the phytoplankton community, overall biomass
may stay the same [84].
Zebra mussels may affect zooplankton, both directly through consumption
and indirectly through competition for food [78]. Selective consumption appears
to be the primary mechanism contributing to changes in zooplankton species
composition [77] [78] [99] and abundance [100] [101] [102]. Pace
et al.
[77] re-
ported that after zebra mussel introduction, zooplankton biomass in the Hudson
River decreased over 70%. After mussel introduction into Lake St. Clair, clado-
ceran and copepod abundance decreased by 50%, while rotifers declined by over
80% [102]. However, in Oneida Lake, New York, there was no decrease in
Daphnia spp. biomass, but only a shift to larger bodied species [88]. The rela-
tively weaker swimming strength of smaller zooplankton may make them more
susceptible to zebra mussel predation [78] [88] [100]. It is also possible that any
impacts of zebra mussels on zooplankton may be isolated to only those areas of a
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of Ecology
lake suitable for zebra mussels. There is also a potential that with larger water-
bodies, impacts of zebra mussels on zooplankton can be patchy, isolated to areas
of a lake with suitable zebra mussel habitat [88] [103].
Most mussel families native to North America have been negatively affected
by the introduction of zebra mussels [3] [75]. These impacts can occur by zebra
mussels settling on native mussels or by the creation of toxic conditions because
of zebra mussel waste, but food competition is likely the primary mechanism
behind the decline of native mussels after zebra mussel introductions [3] [75].
The decline in native mussel populations with the expansion of zebra mussels
across North America is a major concern to natural resource managers [3] [11]
[75].
Zebra mussel introductions have a positive effect on many aquatic invertebrate
populations. The appearance of zebra mussel druses often coincides with an in-
crease in the abundance of most invertebrates, such as amphipods, chironomids,
oligochaetes, hydrozoans, and smaller mollusks [80] [104]-[110]. Large mollusks,
large net-spinning caddisfly, and those invertebrates that use soft substrates may
be negatively impacted by zebra mussels [105] [110]. Macro-invertebrates likely
benefit from zebra mussels by increasing the availability of food and hard struc-
ture. Improved water clarity makes food more accessible [61] [76] [79] [85] [86],
and macro-invertebrate food may increase due to increased organic matter re-
sulting from zebra mussel filter feeding [111] [112] [113]. However, most studies
attribute increased hard structure due to zebra mussels as the primary reason for
increased macro-invertebrate numbers [80] [104] [106] [109] [113] [114] [115].
Druses, with living mussels, dead shells, and bysaal threads, increase bottom
complexity, providing protection to invertebrates from predators [109] [110]. In
addition, a druse on soft sediment provides the hard surface required by many
invertebrates [106] [116].
Evidence of zebra mussel impacts on fish populations is limited. In Lake Erie,
walleye
Sander
vitreus
, white bass
Morone
chrysops
, yellow perch
Perca
flaves-
cens
, freshwater drum
Aplodinotus
grunniens
, emerald shiner
Notropis
hudso-
nius
, and trout-perch
Percopsis
omiscomaycus
populations did not change after
zebra mussel introduction [117] [118]. However, gizzard shad
Dorosoma
cepe-
dianum
abundance may have been affected [117]. A decrease in walleye of 50%
to 70% in Lake St. Clair was observed after the introduction of zebra mussels
[82], although this may or may not be a cause-and-effect relationship. The de-
crease may have been due to mussel-induced water quality decreasing the lower
light and higher turbidity conditions more conducive to walleye foraging success
[119] [120]. However, increased water clarity and the subsequent increase in
aquatic macrophytes [79] [121] benefits other fish species such as muskellunge
Esox
masquinongy
, yellow perch, smallmouth bass
Micropterus
dolomieu
, and
other centrarchids [82].
Zebra mussel veligers and adults are consumed by a number of fish species
[122] [123]. Predation on veligers has been reported for alewife
Alosa
pseudo-
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harengus
, rainbow smelt
Osmerus
mordax
, gizzard shad, blueback herring
Alosa
aestivalis
, and white perch
Morone
americana
[122] [124]. Adult mussels are
commonly consumed by freshwater drum, blue catfish
Ictalurus
furcatus
, redear
sunfish
Lepomis
microlophus
, pumpkinseed
Lepomis
gibbosus
, round goby
Neogobius
melanostomus
, and several other fish species [122] [123] [125] [126]
[127] [128] [129].
Indirectly, zebra mussels appear to increase yellow perch growth by increasing
invertebrate abundance [130]. Although yellow perch and bluegill
Lepomis
ma-
crochirus
foraging success may decrease with the presence of druses [108] [131],
any such decrease is more than compensated by the large increase in inverte-
brate numbers.
Walleye spawning success in Lake Erie was not impacted by zebra mussels
[61] [132]. However, Marsden and Chotkowski [133] suggested that zebra mus-
sels decreased lake trout
Salvelinus
namaycush
natural reproduction in Lake
Michigan by altering reef spawning habitat and increasing the potential for egg
predation.
No impacts on fish populations due to zebra mussels have been identified in
South Dakota. However, zebra mussels do not have a long history in the state
and specific studies focused on potential zebra mussel impacts have not been
undertaken.
4. Control
Characteristics such as high fecundity [1] [5] [6], free swimming larvae [12]
[16], and the ability to attach to a variety of surfaces [7] [8] [9] [10] make zebra
mussel control extremely difficult. Once a zebra mussel population is estab-
lished, chemical control is possible on smaller water bodies in closed systems
[134]. However, chemical control is very expensive, limiting its use [135] [136].
A potassium solution was used to successfully eradicate zebra mussels from a
12-acre enclosed lake in Virginia [136]. Copper sulfate was used for zebra mussel
control at Offutt Air Force Base Lake, Nebraska in 2008, but two years later,
adult zebra mussels were again found in the lake (Tony Barada Nebraska Game
and Parks,
personal
communication
). Copper sulfate and other chemical mol-
luscicides have the potential to negatively impact native mussel species [136]
[137], as well as zooplankton, macroinvertebrates and fish species [136] [138].
Physical removal has also been used for zebra mussel control [139]. Repeated
zebra mussel removals by divers in Lake George, New York [140], reduced zebra
mussel populations to where reproduction and recruitment were encumbered,
and further recruitment prevented [141]. However, water chemistry in Lake
George was unfavorable for zebra mussel development which may have allowed
for scuba removals to be successful [141]. The placement of tarps over zebra
mussels to deprive them of oxygen, paired with chemical applications, has been
used for mussel control in California [139].
Drawdowns are another mechanical control method. A drawdown simply in-
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of Ecology
volves lowering the water level to expose zebra mussels to adverse environmental
conditions leading to desiccation or freezing. In Nebraska, zebra mussels were
eradicated from Zorinsky and Cunningham Reservoirs using drawdowns (Tony
Barada Nebraska Game and Parks,
personal
communication
). In Zorinsky Re-
servoir the drawdown was followed by a chemical fish treatment.
Biological control has also been used against zebra mussel populations. A
biopesticide (Zequanox, Marrone Bio Innovations, Davis, California, USA) con-
tains a killed strain of
Pseudomonas
flourescens
(
Pf
-CL145A), that when in-
gested damages the digestive tract of mussels causing death, with no impacts on
fish, native mollusks, birds, plants, algae, and numerous invertebrates [139]
[142] [143]. When used at Christmas Lake in Minnesota, zebra mussels were
completely removed within the treatment area [144]. However, such treatments
can be costly, at up to 11,000 USD per acre [145].
Because of the difficulty and expense of control after zebra mussel introduc-
tions, preventing the anthropogenic spread of zebra mussels has become a focus
of natural resource managers in North America [146]. Considerable attention
has focused on recreational watercraft inspections and disinfections [147] [148].
In addition, protocols to allow for the safe movement of fish and fish eggs be-
tween water bodies have also been developed [149] [150] [151] [152]. All of
these preventative measures have been used in South Dakota.
Acknowledgements
We thank Jill Voorhees and Amy Gebhard for their assistance with this manu-
script.
Conflicts of Interest
The authors declare no conflicts of interest regarding the publication of this pa-
per.
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