Volume 7, Number 6 • Winter - Spring 1997
Natural Enemies of Zebra
Mussels: Predators, Parasites and Ecological Competitors
Investigators: Daniel P. Molloy, Alexander Y. Karatayev, Lyubov E.
Burlakova, Dina P. Kurandina, and Franck Laruelle
The following article is
based on Natural Enemies of Zebra Mussels: Predators. Parasites and Ecological
Competitors to be published in Reviews in Fisheries Science this
year. Research is headquartered at the New York State Museum and was the result
of an international collaboration supported primarily by grants from the Hudson
River Foundation and the National Academy of Sciences [Ed.].
I. Introduction
This paper represents an
extensive review of the literature on the zebra mussel and its predators,
parasites and ecological competitors that interact to restrict its spread and
control its population density. It is especially valuable in containing extensive
international research, particularly that published in Cyrillic. Since most of
the literature discussed here relates to research done on Dreissena
polymorpha, the term zebra mussel or Dreissena refers to that
species unless otherwise stated.
Zebra mussels originated in
Eurasia and a great deal of the research on predation and naturally occurring
parasites has been done there. Since the immigration to the Great Lakes region
of both the zebra mussel (D. polymorpha) and the related quagga mussel (Dreissena
bugensis) in the ballast water of transoceanic vessels, an explosive
expansion of these animals within littoral hardwater habitats throughout North
America has been observed. Besides significant economic impact as a
macrofouling nuisance, they have become key players in the ecology of lakes and
rivers in North America. Competition with native bivalves, declines in
phytoplankton productivity, and restructuring of benthic communities have all
been attributed to zebra mussel colonization.
Once introduced into a suitable
habitat, their high fecundity and growth rate, coupled with a tolerance of a
wide variety of environmental conditions, generally result in a rapid increase
in numbers. A lack of a natural enemy complex in North America doubtless contributed
to their rapid establishment and range expansion, but to what extent is subject
to debate. This paper attempts to address the issue of natural controls through
a review of the international literature on natural enemies of Dreissena and
the impact these enemies have on mussel populations.
II. Predators
A variety of predators exist for
attached Dreissena, but relatively little research exists for the
planktonic stages. Field observations of 10 European and 5 North American fish
species (Cyprinidae (7 species), Clupeidae (3 species), Osmeridae (2 species),
Percidae (2 species), Percichthyidae (1 species) have shown planktonic
dreissenid larvae in the alimentary tracts of the fry. Predatory copepods such
as Mesocyclops and calanoid copepods are reported to take veligers, with
the stages before the first "0"
(90 - 100 pm) stage being particularly vulnerable. Coelenterate predation on
veligers has also been reported in Europe and North America. Cannibalism of
pelagic larvae by adult zebra mussels has also been documented in Europe and
North America, and this may be a density dependent population control.
Attached mussel predation is
more extensively documented. Records from Europe and North America indicate
that at least 38 species of fish consume attached mussels. For many of these
species, however, zebra mussels may comprise a relatively small portion of
their diet. In North America, some 13 additional species are considered
potential predators based on their natural consumption of other bivalves. In North
America, freshwater drum (Aplodinotus grunniens) is the best documented
fish predator. This is in contrast to Europe where cyprinids comprise the
largest class of consumers. Predatory species capable of taking adult mussels
typically have either molariform pharyngeal teeth or strong crushing jaws and
even then, predation is limited by the size class of both the mussel and the
fish.
Zebra mussels can quickly become
a significant food resource for molluscivorous fish when introduced into new
habitat. Additionally, they can be a high quality food supplement for a
plant-dominated diet. Biomass of black carp (Mylopharyngodon piceus) in
the Tsimlyanskoe Reservoir and roach in the Rubyinsk Reservoir increased
following the invasion of D. polymorpha with concomitant increase
on the yields of the fisheries. Predation on zebra mussels can also result in
increased exposure of fish to parasites as well as toxins such as heavy metals
which bioaccumulate in mussel tissue.
At least 36 species of birds are
recorded as consumers of attached Dreissena, although they are not a
major dietary component for all these species. The best documented of the avian
predators are all diving birds, including the tufted duck (Aythya fuligula),
greater scaup (Aythya marila), lesser scaup (Aythya
afinis), goldeneye (Bucephala clangula) and a diving
rail, the coot (Fulica atra). The greater scaup (A. marila), goldeneye
(B. clangula), old squaw (Clangula hyemalis), herring gull (Larus
argentatus), and white-winged scoter (Melanitta fusca) are all known
to consume mussels in both Europe and North America.
Factors influencing selection of
D. polymorpha as prey include seasonal availability and migratory
patterns, depth and density of mussel populations, and prey size. Fall, winter,
and spring are times of peak mussel predation by birds. Flocking for seasonal
migration results in high bird densities and plants are often not available
during the winter. Migratory or overwintering populations can consume large
quantities of zebra mussels. Shallow water areas with a high mussel density are
generally preferred for foraging. Medium length mussels (ca. 5-20 mm) are
preferred.
Waterfowl predation can substantially
decrease zebra mussel densities in a limited area over the short term. It can
also result in the removal of a size class, but the change is often short-lived
as space available is generally recolonized within a year. Lasting reductions
in zebra mussel numbers are seen only when recruitment is low and predation is
intense.
Zebra mussels can be a
significant food source for waterfowl. Increases in flock size as Dreissena colonized
a water body have been observed in Lake Erie, and lakes in Germany and
Switzerland. In Europe, both distribution and timing of migration routes are
influenced by availability of zebra mussels. Large standing populations of
mussels have caused thousands of waterfowl to overwinter on Swiss lakes rather
than continue their migration south.
Detrimental effects can be seen
with narrow reliance on zebra mussels as a food source. In Europe, a decline in
mussel populations in the bitterly cold winter of 1986 was a contributing
factor in the population crash due to starvation of pochard and tufted duck.
Zebra mussels tissues also harbor contaminants and intermediate stages of
parasites, both of which can have adverse affects on their avian predators.
Crustaceans and reptiles may
also be predators in North America. Both laboratory and field data suggest that
blue crabs (Callinectes sapidus) can be aggressive consumers of large
mussels. Crayfish (Orconectes) are documented predators in European
waterbodies and are suspected to be consuming dreissenids in North America
also. Astacus leptodactylus and Cambarus affinis are also
predatory species in European waters. Predation was generally higher among
female crayfish. Intensity of predation was related to temperature and prey
size. Predation increased with increasing water temperature and smaller (8 mm)
mussels were preferred. Laboratory studies suggest turtles may also feed on Dreissena,
although not as preferred prey.
III. Parasites
The relationship between many of
the microscopic organisms found in and on D. polymorpha is
unclear. Therefore, some symbionts are discussed that have an obligate
association with zebra mussels but whose precise relationship may actually
prove to be mutualistic or commensal.
Over 30 species of parasites are
described that have been reported within attached zebra mussels. There is no
reported research on parasites of planktonic mussels, although such parasites
may exist. Parasites are commonly thought to enter the adult mussel via the
inhalant siphon. They then migrate to the specific tissue within the mussel. In
some cases, the mussel may be the sole host, while others such as digenetic
trematodes spend only a portion of their life cycles within the mussel before
being passed ultimately to the definitive host, often a fish or waterfowl.
To date, 5 species of host
specific ciliates (Conchophthirus acuminatus, Conchophthirus klimentinus,
Sphenophrya dreissenae, Sphenophrya naumiana, and Hypocomagalma
dreissenae (Figure 1 A-E) have been reported within the mantle of D.
polymorpha. In addition, ophryoglenine species have been reported in the
digestive gland (Figure 1F-G). In a low stress environment, a healthy mollusc
is generally in equilibrium with the ciliates that inhabit it; only when
conditions alter to permit uncontrolled growth will significant damage to the
mollusc occur.
Throughout the world Conchophthirus
spp. are found on gills, viscera, and within the mantle cavities of both
freshwater and marine bivalve species. Based on vacuole contents analysis, they
are generally thought to be a commensal since only one species, Conchophthirus
magna, has been reported consuming epithelial cells as a parasite. No
detrimental effects have been reported even with extremely heavy infestation.
To date, only two species have been reported in Dreissena, C. acuminatus (Figure
1A, 2A) and C. klimentinus (Figure 1B). In the absence of vacuole
analysis for Conchophthirus spp. in Dreissena, it is assumed that
the more general commensal pattern is followed.
Hypocomagalma dreissenae (Figure 1C) is the only ancistrocomid ciliate
reported in Dreissena. It is widely distributed throughout Europe. The
entire family exhibits morphological characteristics typical of the parasitic
form. Ciliation is reduced and the mouth has been replaced with a suctorial
tentacle which is inserted into the epithelial cell of the host. In Dreissena,
as well as other bivalves, this group is clearly parasitic; however, the
infections seem to be of low intensity and produce few pathological effects.
Sphenophrya spp. are also considered parasitic. The adults of
this genus have lost their mouth, apparently feed osmotically, and lack cilia -
all traits consistent with parasitism. Two species are reported in D. polymorpha
(Figure 1D-E). Infection records are few in number and limited geographically,
with S. naumiana reported only in Macedonia and S. dreissenae
in Macedonia and Poland.
Ciliates of the order
Hymenostomatida, separated into small (Figure 1G) and large forms (Figure 1F)
and tentatively placed in the suborder Ophryoglenina, have been reported in the
digestive gland of D. polymorpha in Russia. Degeneration of the
digestive gland has been noted. In Lake Erie, Ophryoglena was observed
in the mantle cavity of living and dead mussels, but it is highly probable that
they were not the same ophryoglenine species as in European D. polymorpha and
may simply have been free-living histophagous species - not parasites at all.
Dreissena spp. have seven genera of trematodes capable of
infecting them as either intermediate hosts in a complex life cycle or as the
sole host. Most trematodes are digenetic species and require more than one host
to complete their life cycle. Bucephalus polymorphus is a digenetic
trematode that inhabits three hosts during its life cycle. Dreissena is
the first intermediate host parasitized by the miracidium after hatching.
Within the visceral mass of the mussel, the sporocyst develops into a knotted
white mass of tubules (Figure 2B). This mass is found primarily in the gonads
and typically renders the mussel sterile; however, these tubules can also
extend into surrounding tissues such as the gills, digestive gland, and mantle
epithelium. Cercariae released from infected mussels attach to fish, encyst,
and metamorphose into metacercariae. Cyprinids are most commonly infected, but
not the only fish hosts for B. polymorphus metacercariae. In France,
pathologies have been observed in cyprinids, although not on a consistent
basis. The definitive hosts for B. polymorphus are predatory fish that
consume infected forage fish. Northern pike (Esox lueius), Eurasian
perch (Perea fluviatilis), zander (Stizostedion lueioperea), and
brown bullhead (Ietalurus nebulosus) have all been documented as
harboring adult worms in their intestines. No pathologies associated with the
infection have been reported in these host species. A growing body of evidence
suggests B. polymorphus is host specific for Dreissena. Although
found throughout Europe, infected populations are not common. Prevalence varies
widely. Rates of infection peak during the warmest months resulting in
subsequent shedding of cercariae 1 - 2 months later. B. polymorphus has
not been reported in North America.
Phyllodistomum spp. require only one other host, a fish, to complete
their life cycle. After hatching, a miracidium enters the mantle cavity of a
dreissenid through the siphon and encysts in a gill demibranch where it forms a
mother sporocyst. Daughter sporocysts are produced, with 200 - 300 infecting
various locations within the gills (Figure 2C). Mature sporocysts containing
metacercariae are then shed to be eaten by a variety of fish genera where the
adult worms are ultimately develop in the urinary tract. Zebra mussels infected
by Phyllodistomum demonstrated reduced dry weight and higher
concentrations of toxic substances. No adverse effects were observed in the
fish host. Although widely distributed throughout Europe, prevalence of
infection is generally low. Increasing water temperatures generally increases
prevalence of infection. Both prevalence and intensity of infection increase
with mussel size.
FIGURE 1. Ciliates from Dreissena
(bar = 50 pm). A - Conehophthirus aeuminatus; B Conehophthirus
klimentinus; C Hypoeomagalma dreissenae; D Sphenophrya
dreissenae; E Sphenophrya naumiana; F - Large ophryoglenine
associated with digestive gland; G - Small ophryoglenine associated with
digestive gland. (Reprinted with permission of Rev. Fish. Sci. CRC Press.)
Dreissena acts as one of several possible intermediate hosts for
Echinoparyphium recurvatum. Freshwater snails and sometimes tadpoles act
as first intermediate hosts for the miracidium. Sporocysts develop within these
hosts with subsequent release of free swimming cercariae. The cercariae enter
the second intermediate host which can be a tadpole, snail or Dreissena and
encyst as metacercariae. Such infected hosts are ingested by waterfowl and
sometimes mammals. The adult parasite infests the small intestine sometimes
producing a fatal infection in waterfowl. The infection is thought to be
insignificant to the zebra mussel, but the increased availability of
intermediate host species may prove detrimental to waterfowl populations.
Aspidogaster limacoides has been reported in Russian zebra mussels. Aspidogaster
conchicola is native to both Europe and North America and is a documented
parasite of Dreissena as well as unionids and snails. These trematodes
require only one host to complete their life cycle. No known pathological
effects are evident with infection, but histological studies are lacking.
Additional species of trematode reported in Dreissena are Leucochloridiomorpha
spp. in the Ukraine and plagiorchiid metacercariae at Port Colbome (Lake
Erie).
