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REPRODUCTIVE BIOLOGY OF ELLIPTOIDEUS SLOATIANUS, LAMPSILIS
SUBANGULATA, MEDIONIDUS PENICILLATUS, AND PLEUROBEMA
PYRIFORME
(BIVALVIA: UNIONIDAE)
By
Christine A. O'Brien
A THESIS PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
MASTER OF SCIENCE
UNIVERSITY OF FLORIDA
1997
I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality, as
a thesis for the degree of Master of science.
/Georg/ Tanner, Chair
Associate Professor of
Wildlife Ecology and
Conservation
I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality, as
a thesis for the degree of Master of Science.
Oi--
/J es Williams, Cochair
Adunct Professor of
ldlife Ecology and
Conservation
I certify that I have read this study and that in my
opinion it conforms to acceptable standards of scholarly
presentation and is fully adequate, in scope and quality, as
a thesis for the degree of Master of Science.
Loukas Arvanitis
Professor of Forest
Resources and Conservation
This thesis was submitted to the Graduate Faculty of
the College of Agriculture and to the Graduate School and
was accepted as partial fulfillment of the requirements for
the degree of Master of Science.
May, 1997 ____
Dea College of
Agriculture
Dean, Graduate School
Copyright 1997
by
Christine A. O'Brien
ACKNOWLEDGMENTS
The funding for this project was provided by the U. S.
Fish and Wildlife Service in Jacksonville, Florida. I would
like to thank Jayne Brim Box for introducing me to the
fascinating world of freshwater mussels. Jayne also
provided me with much needed guidance throughout my thesis
work, both in the field and laboratory. Jayne was always
willing to answer any questions I had about my work. I
would like to thank Shane Ruessler for his enthusiastic
assistance in both the field and laboratory. A special
thanks to Noel Burkhead and Howard Jelks for providing me
with information about fish biology and editorial comments.
I would also like to thank my committee members for
supporting my efforts during my work towards my Master of
Science degree.
Finally, I would like to thank my family for providing
me with love and support throughout my studies.
iii
TABLE OF CONTENTS
ACKNOWLEDGMENTS . .
LIST OF TABLES . .
LIST OF FIGURES . .
iii
. . vi
. . vii
ABSTRACT
viii
1 INTRODUCTION . . . .
Historical Background . .
Freshwater Mussel Biology . .
2 METHODS AND MATERIALS . . .
Study Site . . . .
Target Mussel Species . . .
Reproductive Biology . . .
Development of Immunity . .
Glochidia Reaction to Nonindigenous Fish
Glochidia Morphology . . .
3 Results . . . . .
Reproductive Biology . . .
Development of Immunity . .
Glochidia Reaction to Nonindigenous Fish
Glochidia morphology . . .
3
. . 3
. . 12
. . 25
S 25
S 38
S 41
S 41
4 Discussion
. 50
Reproductive Biology . . .
Development of Immunity . .
Glochidia Reaction to Nonindigenous Fish
Glochidia Morphology . . .
Conservation Issues . . .
5 Conclusion . . . .
APPENDICES
A-1 SITE RECORDS FOR MUSSEL COLLECTION SITES
B-l SITE RECORDS FOR FISH COLLECTION SITES
. . 65
LIST OF REFERENCES
BIOGRAPHICAL SKETCH
. 72
LIST OF TABLES
Tables page
2-1. List of fish names . . .. .. 19
3-1. Months when the mussels were found gravid . 26
3-2. Host fish and non-host fish for E. sloatianus 27
3-3. Percent fish producing E. sloatianus juveniles .29
3-4. Dates when superconglutinantes are released .30
3-5. Host fish and non-host fish for L. subangulata .32
3-6. Percent fish producing L. subangulata juveniles .33
3-7. Host fish and non-host fish for M. penicillatus .35
3-8. Percent fish producing M. penicillatus juveniles .37
3-9. Host fish and non-host fish for P. pyriforme .39
3-10. Percent fish producing P. pyriforme juveniles 40
3-11. Number of L. subangulata after two infestations .42
3-12. Nonindigenous fish reaction to glochidia . 43
LIST OF FIGURES
Figures page
1-1. Freshwater mussel life cycle . . 5
1-2. Superconglutinate . . . . 7
3-1. Elliptoideus sloatianus glochidia morphology 44
3-2. Lampsilis subangulata glochidia morphology .46
3-3. Medionidus penicillatus glochidia morphology .47
3-4. Pleurobema pyriforme glochidia morphology . 48
vii
Abstract of Thesis Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Master of Science
REPRODUCTIVE BIOLOGY OF ELLIPTOIDEUS SLOATIANUS, LAMPSILIS
SUBANGULATA, MEDIONIDUS PENICILLATUS, AND PLEUROBEMA
PYRIFORME
(BIVALVIA: UNIONIDAE)
By
Christine A. O'Brien
May 1997
Chairperson: Dr. George Tanner
Major Department: Wildlife Ecology and Conservation
A study on the reproductive biology of Elliptoideus
sloatianus, Lampsilis subangulata, Medionidus penicillatus,
and Pleurobama pyriforme was conducted from May 1995 to
January 1997. The mussels used in the study were collected
in the Apalachicola, Chattahoochee, Flint, and Ochlockonee
river drainages in Alabama, Georgia, and Florida. Periods of
gravidity were determined by inspecting female mussels
monthly; host fish were determined by laboratory infections.
A test was conducted to determine if host fish developed an
immunity to glochidia after multiple infestations occurred.
An experiment was also conducted to determine if unionid
glochidia will transform on a nonindigenous fish. Finally,
the glochidia from each mussel species were photographed
viii
using a scanning electron microscope. Primary host fish
were not identified for Elliptoideus sloatianus.
Elliptoideus sloatianus is a tachytictic breeder. Lampsilis
subangulata is a bradytictic breeder. Primary host fish
were identified as Micropterus punctulatus and M. salmoides.
Medionidus penicillatus is a bradytictic breeder. Primary
host fish were identified as Etheostoma edwini and Percina
nigrofasciata. Pleurobama pyriforme is a tachytictic
breeder. The primary host fish was identified as
Pteronotropis hypselopterus. After infesting M. salmoides
twice with L. subangulata glochidia, a t-test indicated that
there was a significant reduction in the number of juveniles
produced by M. salmoides after the second infection.
Poecilia reticulata, a nonindigenous fish, successfully
transformed glochidia from all four mussel species.
However, the number of Poecilia retuculata producing
juvenile mussels varied for each species of mussel.
CHAPTER 1
INTRODUCTION
Historical Background
Historically, North America was known for its rich
mussel fauna with about 300 species recognized (Turgeon et
al. 1988). Since the early 1900s, 6% of the mussel fauna
has become extinct and 21% are federally listed as
endangered or threatened (Neves 1992; Williams et al. 1992).
The reasons for this decline are not well understood.
However, loss of suitable habitat (caused by increased
siltation and dredging), introductions of nonindigenous
species, pollution, and commercial exploitation are thought
to have a negative impact on mussel populations (Ortmann
1909; Fuller 1974; Williams et al. 1992). In addition,
mussels are obligate parasites on fish, and recent declines
in the North American fish fauna may also have negative
effects on mussel populations (Allen and Flecker 1993). In
fact, aquatic species of North America have an imperilment
rate three to eight times greater than the imperilment rate
of avian and mammalian fauna (Master 1990).
In 1994, seven species of mussels from the eastern Gulf
of Mexico drainage were proposed for federal listing as an
endangered or threatened species under the Endangered
CHAPTER 1
INTRODUCTION
Historical Background
Historically, North America was known for its rich
mussel fauna with about 300 species recognized (Turgeon et
al. 1988). Since the early 1900s, 6% of the mussel fauna
has become extinct and 21% are federally listed as
endangered or threatened (Neves 1992; Williams et al. 1992).
The reasons for this decline are not well understood.
However, loss of suitable habitat (caused by increased
siltation and dredging), introductions of nonindigenous
species, pollution, and commercial exploitation are thought
to have a negative impact on mussel populations (Ortmann
1909; Fuller 1974; Williams et al. 1992). In addition,
mussels are obligate parasites on fish, and recent declines
in the North American fish fauna may also have negative
effects on mussel populations (Allen and Flecker 1993). In
fact, aquatic species of North America have an imperilment
rate three to eight times greater than the imperilment rate
of avian and mammalian fauna (Master 1990).
In 1994, seven species of mussels from the eastern Gulf
of Mexico drainage were proposed for federal listing as an
endangered or threatened species under the Endangered
2
Species Act of 1973. The seven species included the fat
threeridge (Amblema neislerii), Chipola slabshell (Elliptio
chipolaensis), purple bankclimber (Elliptoideus sloatianus),
shinyrayed pocketbook (Lampsilis subangulata), Gulf
moccasinshell (Medionidus penicillatus), Ochlockonee
moccasinshell (Medionidus simpsonianus), and oval pigtoe
(Pleurobema pyriforme)(Federal Register 1994).
Historically, mussel shell was used to manufacture
buttons. In 1898 over 50 companies were in production along
the Mississippi River, producing over 30 million buttons in
only a few years. The high demand for shell products in the
late 1800s reduced mussel populations and prompted
conservation efforts to be implemented (Jones 1950). In
1894, the United States Bureau of Fisheries encouraged
studies in the artificial propagation of mussels to help
alleviate the high demand on natural mussel beds (Coker
1919). Despite these early efforts to conserve mussel
populations, their numbers continued to decline.
After the decline of the button industry, mussel
harvesting was greatly reduced for many years. However, in
the 1950s mussel harvesting increased as the pearl industry
began to grow. Today, mussel shell is used to seed pearl
oysters in China and Japan. In 1991, the pearl industry
encouraged the collection of 9,000 tons of mussel shell in
North America. In 1992 the harvest dropped to only 4,500
tons (Williams et al. 1992).
3
Freshwater Mussel Biology
Freshwater mussels are an important component of the
aquatic ecosystem. Freshwater mussels remove toxins, silt,
and other organic material from the water column, and
provide food for wildlife (Stansbery and Stein 1971;
Williams et al. 1992). Freshwater mussels are also good
indicators of water quality because they are long lived,
widely distributed, sessile organisms which are sensitive to
pollution (Stansbery and Stein 1971).
Freshwater mussels are unique among bivalves in that
most require a host fish to complete their life cycle.
Unlike male and female marine bivalves which release sperm
and eggs into the water column, fertilization of freshwater
mussels takes place within broodchambers in the gills of the
female (Jirka and Neves 1992). A broodchamber filled with
eggs and or mature glochidia is usually identified by its
swollen appearance (Coker 1919). The female mussel
carries the fertilized eggs in the gills until they develop
into a parasitic stage the called glochidia stage.
Mussels have been categorized into two groups based on
their embryo incubation period (Lefevre and Curtis 1912;
Waller and Holland-Bartels 1988). The first group,
tachytictic (short-term) breeders, fertilize eggs in the
spring and release glochidia in the fall. The second group,
bradytictic (long-term) breeders, fertilize eggs in late
4
summer and release glochidia in the following spring or
early summer. When fully developed, the female mussels
release the glochidia into the water column where they must
come into contact with the proper host fish (Figure 1-1)
Once attached to the host fish, the glochidia metamorphose
and drop to the substrate to become free living juveniles.
The mussel/fish relationship is often species-specific
(Lefevre and Curtis 1912). Only certain species of fish can
serve as suitable hosts for a particular mussel species. In
some mussels (i.e., Strophitus sp. and Uterbackia sp.)
glochidia do not require a host fish for transformation
(Lefevre and Curtis 1912).
The attachment of glochidia to a proper host fish is
often difficult. Female mussels increase the probability of
successful glochidia/host fish interactions by producing
thousands of glochidia (Jansen 1990). Female mussels can
(depending on size and species) produce anywhere from 2,000
(Kondo 1984) to as many as 3,000,000 glochidia (Coker et al.
1921). Some mussel species attempt to increase the chance
of glochidia contacting a proper host fish by releasing
glochidia into the water column when light sensitive spots
on the mantle are stimulated by the shadow of a passing fish
(Kraemer 1970; Jansen 1990). Other mussels lure host fish
by extending brightly colored portions of their mantles to
mimic prey (Coker et al. 1921; Kraemer 1970).
Glochidia attach to
gill filaments or fins
Sperm
- Juvenile mussel
Glochidia
Female Male
Figure 1-1. Freshwater mussel life cycle.
6
The use of lures to increase a mussel's chance of
infesting a host fish is not uncommon. In fact, several
mussel species in the subfamily Lampsiline have developed
lures, mainly in the form of modified mantle flaps in the
shape of prey (Kraemer 1970). The lures displayed by the
female mussels disillusions the host fish by mimicing a
consumable meal. When the host fish attempts to consume a
mimic lure, the female mussel releases glochidia into the
water column where attachment to the host fish can occur.
Perhaps one of the most amazing forms of a fish mimic is
that of a superconglutinate (Haag et al. 1995). A
superconglutinate holds the entire reproductive efforts for
the year in a package that mimics a small fish. The
superconglutinate consists of a mucus strand attached to a
modified conglutinate (Figure 1-2).
A conglutinate is a packet of glochidia, or eggs, that
takes the shape of water tubes of the gills in female
mussels. The size and shape of a conglutinate depends on
the species of mussel. The modified conglutinate is
comprised of single conglutinates that have been fused
together by the mucus strand. Most mussel species release
single conglutinates rather than fusing the conglutinates
(Coker et al. 1921). The length of the modified
conglutinate segment of the superconglutinate ranges from
three to five centimeters. The modified conglutinate not
only resembles a small fish in size and shape but in
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coloration as well. The modified conglutinate has
pigmentation in the form of a lateral band and eye spot.
During the production of the superconglutinate the water
currents move the fish mimic in motions that are similar to
a small fish.
The mimic fish structure (modified conglutinate) is
attached to a mucus thread which can be produced to lengths
up to one meter. After the complete production of a
superconglutinate, which can take about four hours, the
female mussel discontinues the production of mucus and the
superconglutinate breaks free from her excurrent siphon.
After detaching from the female, the superconglutinate
drifts passively in the stream current. The fate of the
superconglutinate now depends on the chance that the current
will wrap the superconglutinate around a rock, branch, or
any structure in the stream where it will continue to mimic
prey for a piscivorous host fish. When a fish attempts to
consume the superconglutinate thousands of the glochidia
within the modified conglutinate are released and may attach
to the fish and later fall off as juvenile mussels.
Glochidia failing to come into contact with a suitable
host will drift through the water column, surviving for only
a few days (Jansen 1990). When the glochidia come in
contact with a suitable host, attachment to the gill and/or
fin region will occur and the glochidium will become fully
encysted within 24 to 36 hours (Coker et al. 1921). The
9
encysting stage of the glochidia on the fish is a fish's
response to the puncture caused by the clamping of a
glochidium. Glochidia attaching to a non-host fish will
slough off soon after attachment occurs. Properly encysted
glochidia will metamorphose, with little change in size
(Coker et al. 1921), into free-living juveniles, displaying
abductor muscles, gill buds, and a ciliated foot with
protractor and retractor muscles (Karna and Millemann 1978).
The time required for complete metamorphosis of
glochidia is dependent in part on temperature and mussel
species (Jones 1950). One species of mussel, Quadrula
intermedia, takes 24 to 29 days to metamorphose in water at
190 C (Yeager and Saylor 1989), while Lampsilis radiata
takes up to 98 days at 150 C for metamorphosis to occur
(Tedla and Fernando 1969). Another mussel, Simpsoniconcha
ambigua, produces glochidia that metamorphose over the cold
winter months and requires up to seven months to complete
transformation (Howard 1951).
The reproductive biology of many freshwater mussels
remains incomplete (Jansen 1990). For example, host fish
for only 25% of the 300 mussel species in North America have
been identified (Watters 1992). Unfortunately, fewer than
25% of the host fish have been identified for the mussels of
the Gulf of Mexico drainages.
To enhance conservation efforts, fish hosts must be
identified for all mussel species with an emphasis on those
10
species proposed for endangered and threatened status.
There are two methods used to identify host fish for
freshwater mussels. The first method identifies host fish
via laboratory infestations. In the laboratory, known
species of glochidia are infected on known fish species.
The fish are then held until transformed gi chidia drop from
the fish. The second method identifies host fish via
identifying encysted glochidia, to the species level, on
fish collected from streams. A fish species that produced
juvenile mussels in the laboratory and was also found with
encysted glochidia, from the same mussel species, in a
stream is a confirmed primary host fish (Trdan and Hoeh
1982; Neves et al. 1989).
The identification of glochidia to the species level
can be difficult. In some cases streams have few species of
mussels, and the size and shape of the glochidia are
diagnostic (Neves et al. 1989). However, streams that
support a diversity of mussel species, such as those in the
southeastern United States, can make glochidia
identification to the species level almost impossible
without the aid of scanning electron microscopy (Burch 1975;
Hoggarth 1988; Waller et al. 1988).
Once the host fish have been identified for a mussel
species, more information can be focused on the status of
the host fish population. For example, a mussel species may
be forced to utilize the same host fish repeatedly in
11
streams where there are low numbers of host fish available.
Researchers have discovered that some fish develop an
immunity to glochidia when infected repeatedly (Coker et al.
1921; Karna and Millemann 1978; Luo 1993). Since most
mussels are obligate parasites on fish, it is important that
conservation efforts are focused on both mussel and fish
populations, so that all phases of the life cycle are
protected.
The five main objectives of this study are as follows:
1) determine when Elliptoideus sloatianus, Lampsilis
subangulata, Medionidus penicillatus, and Pleurobema
pyriforme produce mature glochidia, 2) identify the primary
host fish for the four target mussel species, 3) test for
the development of an immune response when a fish is
infected twice with the same species of glochidia, 4) test
whether a nonindigenous fish has an immunity to glochidia of
the target mussel species, and 5) describe the glochidia of
each of the target mussel species using the scanning
electron microscopy (SEM).
CHAPTER 2
MATERIALS AND METHODS
Study Site
The Apalachicola, Chattahoochee, Flint, and Ochlockonee
river drainages cover approximately 41,979 km2 of the
southeastern United States, making it one of the largest
river drainage systems in the eastern Gulf Coastal Plain
(Leitman et al. 1983). The majority of mussel species occur
in the low gradient streams of the Coastal Plain and
Piedmont regions. Most streams in the Coastal Plain region
typically have substrate of coarse sand, silty sand, and
gravel. However, the substrata of the Apalachicola and
Ochlockonee rivers consists of a coarser substrate of
cobble, boulders, and bedrock. The Apalachicola,
Chattahoochee, Flint, and Ochlockonee River basin has a rich
aquatic fauna consisting of 30 crayfish species, 20 species
of aquatic snails, 122 fish species, and 32 endemic mussel
species (Butler 1989; Couch et al. 1996).
Target Mussel Species
Elliptoideus sloatianus is a large mussel with a
maximum length of 203 mm and is usually found in sand, muddy
12
CHAPTER 2
MATERIALS AND METHODS
Study Site
The Apalachicola, Chattahoochee, Flint, and Ochlockonee
river drainages cover approximately 41,979 km2 of the
southeastern United States, making it one of the largest
river drainage systems in the eastern Gulf Coastal Plain
(Leitman et al. 1983). The majority of mussel species occur
in the low gradient streams of the Coastal Plain and
Piedmont regions. Most streams in the Coastal Plain region
typically have substrate of coarse sand, silty sand, and
gravel. However, the substrata of the Apalachicola and
Ochlockonee rivers consists of a coarser substrate of
cobble, boulders, and bedrock. The Apalachicola,
Chattahoochee, Flint, and Ochlockonee River basin has a rich
aquatic fauna consisting of 30 crayfish species, 20 species
of aquatic snails, 122 fish species, and 32 endemic mussel
species (Butler 1989; Couch et al. 1996).
Target Mussel Species
Elliptoideus sloatianus is a large mussel with a
maximum length of 203 mm and is usually found in sand, muddy
12
13
sand, and cobble in moderate current (Heard 1975).
Elliptoideus sloatianus is most commonly found in deeper
sections of flowing streams and does not tolerate impounded
waters (Williams and Butler 1994).
Elliptoideus sloatianus was historically found in the
mainstem of the Apalachicola, Chattahoochee, Chipola, Flint,
and Ochlockonee rivers. Currently, E. sloatianus exist only
in the lower unimpounded mainstem of the Flint River and
several areas along the Ochlockonee River (Williams and
Butler 1994).
Lampsilis subangulata, the shinyrayed pocketbook, is a
medium-sized mussel with a maximum length of 85 mm and is
found in sandy or silty sand substrates in moderate to slow
currents. The shell is smooth and yellow in color with dark
green rays (Clench and Turner 1956). Lampsilis subangulata
is not tolerant of stream impoundments.
Historically, Lampsilis subangulata was found in the
Flint River, the mainstem of the Chattahoochee River
(including six of its tributaries), throughout the
Apalachicola River tributaries, Chipola River, and several
sites in the Ochlockonee River system (Williams and Butler
1994).
Today, the distribution of Lampsilis subangulata has
declined to one-third of its original range. Currently,
populations occur in Uchee Creek (tributary of Chattahoochee
River), a few sites in the Flint River system, Chipola
14
River, and a few sites in the upper part of the Ochlockonee
River (Williams and Butler 1994).
Medionidus penicillatus, the Gulf moccasinshell, is a
small mussel with a maximum length of approximately 53 mm.
M. penicillatus is found in sand and gravel areas with slow
to moderate currents (Heard 1975). Medionidus penicillatus
has not been found to survive in impounded river sections.
Historically, Medionidus penicillatus was found in
tributaries and main channel of the Chattachoochee and Flint
rivers, and tributaries of the Apalachicola River (Clench
and Turner 1956). The overall distribution of M.
penicillatus has declined by 75% of its original range
(Williams and Butler 1994).
Pleurobema pyriforme, the oval pigtoe, is a medium-
sized mussel with maximum lengths of 56 mm (Clench and
Turner 1956). Pleurobema pyriforme is usually found in
substrate ranging from sand to sand/gravel usually in the
center of stream channels. Pleurobema pyriforme does not
tolerate impoundments (Williams and Butler 1994).
Pleurobema pyriforme was once found in the mainstems of
the Flint, Chattachoochee, and Apalachicola River systems
(Clench and Turner 1956). Recent surveys indicate the
current distribution of P. pyriforme encompasses only two-
thirds of its historical distribution with no current
populations documented in Alabama (Williams and Butler
1994).
15
Reproductive Biology
Mussels were collected monthly and inspected for mature
glochidia starting in May 1995 and ending in April 1997.
Female mussels found with fully developed glochidia were
considered gravid. Female mussels found with eggs or
developing eggs will be mentioned.
Some monthly collections were not conducted due to
adverse field conditions. Mussels were collected from four
streams that were known to have existing populations of
Elliptoideus sloatianus, Lampsilis subangulata, Medionidus
penicillatus, and Pleurobema pyriforme. All of the streams
from which the mussels were collected occurred in the
Apalachicola, Chattachoochee, Flint, and Ochlockonee river
drainages. The mussels were collected by hand, using
snorkeling and scuba gear.
Elliptoideus sloatianus were collected at two sites
located on the Ochlockonee River and one site on the
Apalachicola River. Elliptoideus sloatianus were collected
from September 1995 to April 1997. Lampsilis subangulata
were collected from the following three creeks in southwest
Georgia: Chickasawhatchee, Cooleewahee, and Kinchafoonee.
L. subangulata were inspected for glochidia from May 1995 to
July 1996. Medionidus penicillatus and Pleurobema pyriforme
were collected from two streams, Chickasawhatchee and
Kinchafoonee, in southwest Georgia from February 1996 to
January 1997 (Appendix A-i).
16
Mussels were opened about 0.5 cm gills were and
inspected gills for the presence of glochidia. When gravid
mussels were found, they were carefully put into plastic
bags and placed into coolers with enough ice to maintain the
stream temperature during the transport to the U. S.
Geological Surveyy (USGS) laboratory. Mussels were
separated by species into separate four-liter jars and
aerated until the glochidia were collected.
The mussel species used in this experiment are proposed
for protection under the Endangered Species Act. Procedures
for removing the glochidia did not result in sacrificing the
mussel. When glochidia were collected from the mussels,
three subsamples were set aside. The first subsample was
used to test for viability by observing a snapping response
when salt crystals were added to the glochidia (Zale and
Neves 1982). The second subsample of glochidia was used to
determine the longevity of the glochidia once they had been
released. The third subsample of glochidia was preserved in
70% ethanol and later used for scanning electron microscopy.
The remain glochidia were used to preform laboratory
infestations.
The mechanisms for releasing glochidia vary slightly
from species to species, therefore, the techniques used to
collect the glochidia from each mussel species was slightly
different. For example, the gills of Elliptoideus
sloatianus are characterized by reduced swelling that is
17
typically observed in most freshwater mussels with
developing eggs or mature glochidia. As a result, it was
difficult to determine which individuals were gravid under
field conditions, therefore, 10 to 15 individuals were
brought to the laboratory for closer inspection.
Once at the laboratory Elliptoideus sloatianus were
held in plastic tubs on the bottom of large holding tanks
(diameter 3 m; depth 1 m). The mussels were then observed
daily until glochidia were released. When conglutinates
were found on the bottom of the tubs, a subsample was taken
and inspected under the microscope. When fully developed
glochidia were found a viability test was performed as
outlined in Zale and Neves (1982).
Gravid female Lampsilis subangulata were identified by
swollen outer gills with dark pigmentation. When gravid
females were found they were brought back to the laboratory
and placed into a current tank. The current tank contained
substrate, water temperature, and photoperiod similar to the
stream from which the mussels were collected. Lampsilis
subangulata expel glochidia via superconglutinate which made
collecting glochidia easy. Once the females were placed in
the tank, superconglutinates were released within a month.
The search for superconglutinates was conducted in the
stream while collecting female Lampsilis subangulata. The
temperature and number of superconglutinates found were
recorded for each trip.
18
Gravid Medionidus penicillatus were identified in the
field by swollen outer gills. Unlike the other mussels, M.
penicillatus did not abort their glochidia in the laboratory
setting. Glochidia were successfully collected from an
individual mussel by making a small incision in the gill and
washing the glochidia with a squirt bottle into a small
petri dish. Each mussel that underwent this glochidial
removal technique was observed for two to four weeks after
the procedure was performed to determine mussel
survivorship.
Pleurobema pyriforme were the most difficult of the
four mussel species to collect viable glochidia from.
Female P. pyriforme were highly sensitive to handling, and
as a result expelled their glochidia prematurely. In order
to maximize the collection of viable glochidia, female
mussels were not inspected in the field. A collection of 12
to 18 individuals were transported to the laboratory and
placed into three different four-liter holding containers.
The bottoms of the containers were siphoned through a 105 im
mesh sieve and inspected for viable glochidia daily.
Fifteen species of fish representing six families were
used in the host fish identification experiment (Table 2-1).
Fish used in the experiment were purchased from fish
hatcheries or collected in streams located in the
Apalachicola, Chattahoochee, Flint, and Ochlockonee river
drainages. Fish collections were conducted as needed from
Table 2-1. The scientific and common names of the
fish used in the host fish identification experiment.
Scientific Name
CYPRINIDAE
Notropis harper
Notropis petersoni
Notropis texanus
Opsopoeodus emiliae
Pteronotropis hypselopterus
CATOSTOMIDAE
Moxostoma robustum
ICTALURIDAE
Noturus leptacanthus
POECILIIDAE
Gambusia holbrooki
Poecilia reticulata
CENTRARCHIDAE
Lepomis auritus
Lepomis macrochirus
Micropterus punctulatus
Micropterus salmoides
PERCIDAE
Etheostoma edwini
Percina nigrofasciata
Common Name
redeye chub
coastal shiner
weed shiner
pugnose minnow
sailfin shiner
smallfin redhorse
speckled madtom
eastern mosquitofish
guppy
redbreast sunfish
bluegill
spotted bass
largemouth bass
brown darter
blackbanded darter
Scientific nomenclature follows that of Robins
et.al. 1991.
20
April 1995 to July 1996 in Tired Creek, Gad'sden County,
Florida; Jones Creek, Worth County, Georgia; and Bear Creek,
Grady County, Florida (Appendix B-1). Fish were collected
via electroshocking and dip netting from streams with known
low densities of mussels in order to avoid using fish with
prior or existing glochidial attachments (Yeager and Neves
1986). Aerated coolers were used to hold the fish during
transportation to the laboratory. Fish purchased from the
fish farms and collected in the streams were separated by
species and placed into 12 40.0-liter flow through holding
tanks at the USGS laboratory. The fish were held in the
tanks for one to two weeks before the experiments were
conducted allowing the fish to acclimate and any previously
attached glochidia to drop from the fish (Zale and Neves
1982; Luo 1993).
After collecting viable glochidia from a single mussel
species, one to two thousand glochidia were placed into a
500-ml beaker. Larger fish species (Lepomis macrochirus and
Micropterus salmoides) were placed into a 1.0-liter beaker
with 750 ml of water with three to four thousand glochidia.
To avoid overcrowding and reduce stress, no more than six
fish of the same species were placed into the beaker with
the glochidia mixture. The glochidia were suspended by two
to three aeration hoses. Each fish was exposed to the
glochidia mixture for 30 minutes. During this time it was
assumed that each fish had equal opportunity for glochidia
attachment.
21
After 30 minutes the fish were taken from the glochidia
mixture and placed in separate 4.0-liter containers.
Replicates were achieved by holding each fish in a separate
4.0-liter container. Each container held equal volumes of
water, an aeration hose, lid, and a screen on the bottom of
the jar. The screen was used to discourage the fish from
consuming the juvenile mussels after they transformed. The
4.0-liter containers were then placed into a large flow-
through bath to maintain an equal temperature range (20.50 C
to 23.50 C) for all of the fish in the experiment.
Each container was then siphoned through a 6.35-mm tube
and into a 105-um nylon mesh sieve every third day starting
the third day after infestations. When juvenile mussels
were found, the tanks were siphoned daily until no juveniles
were collected for three consecutive days. If no juveniles
were collected one month after the fish were infected with
glochidia, they were inspected under a microscope for
encysted glochidia. If no encysted glochidia were found,
the fish species was deemed a non-host for that mussel
species. If encysted glochidia were found on a live fish,
the fish was returned to the jar and reinspected each week
until no encysted glochidia were found. Fish that died
before the experiment was finished were inspected for
encysted glochidia under a microscope. When encysted
glochidia were found on a dead fish and more than half of
the fish in the experiment died the experiment was run
again.
22
Water temperature, number of sloughed glochidia,
number of transformed glochidia, and dates of glochidia
transformation were recorded for each fish. Transformed
glochidia (juveniles) were defined as free-living glochidia
possessing gill buds, a ciliated foot complete with
protractor and retractor muscles, and a pair of abductor
muscles (Karna and Millemann 1978).
Past experiments (Coker et al. 1921; Zale and Neves
1982; Neves et al. 1991) held fish of the same species in a
single container. This experiment was designed to identify
the number of juvenile mussels produced by each fish
individually. Variations in the number of fish that produce
juvenile mussels and the number of juveniles produced by
each fish can give an indication of the effectiveness of
each fish species in successfully transforming juvenile
mussels for that particular mussel species. A strong host
fish species will have produced juvenile mussels from each
fish used in the experiment.
A primary host fish was determined by the following
criteria: 1) more than 30% of the fish must produce juvenile
mussels, 2) the fish must also have a native distribution
similar to the mussel, 3) and the fish must have similar
microhabitat requirements as the mussel. A fish species
producing juvenile mussel(s) but failing to meet all four
criteria was identified as a satellite host fish. Satellite
host fish are fish that produce juvenile mussels but are not
considered a reliable host fish for the mussel species.
23
Development of Immunity
Development of immunity was tested by infesting the
same fish twice with the same species of glochidia and
recording the number of juveniles produced after each
infestation. The immunity experiment was conducted by
infesting Micropterus salmoides with Lampsilis subangulata
glochidia. M. salmoides were infected with L. subangulata
glochidia because the glochidia were easily obtained and the
glochidia transformed in a short enough time to allow for a
second infestation.
Micropterus salmoides were infested by pipetting
several hundred glochidia into both branchial chambers.
Each M. salmoides was placed into separate containers and
the number of juveniles produced were recorded for each
fish.
Glochidia Reaction to Nonindigenous Fish
Poecilia retuclata were exposed to glochidia from each
of the four target mussel species to test whether
nonindigenous fish have a natural immunity to freshwater
mussels. Poecilia retuclata were infected using the same
methods utilized for the native fishes described in the
primary host identification section.
23
Development of Immunity
Development of immunity was tested by infesting the
same fish twice with the same species of glochidia and
recording the number of juveniles produced after each
infestation. The immunity experiment was conducted by
infesting Micropterus salmoides with Lampsilis subangulata
glochidia. M. salmoides were infected with L. subangulata
glochidia because the glochidia were easily obtained and the
glochidia transformed in a short enough time to allow for a
second infestation.
Micropterus salmoides were infested by pipetting
several hundred glochidia into both branchial chambers.
Each M. salmoides was placed into separate containers and
the number of juveniles produced were recorded for each
fish.
Glochidia Reaction to Nonindigenous Fish
Poecilia retuclata were exposed to glochidia from each
of the four target mussel species to test whether
nonindigenous fish have a natural immunity to freshwater
mussels. Poecilia retuclata were infected using the same
methods utilized for the native fishes described in the
primary host identification section.
24
Glochidia Morphology
Glochidia used for SEM were preserved in 70% ethanol
(Waller et al. 1988b). The preserved specimens were placed
on double-sided carbon adhesive tabs that were positioned
onto mounting pegs. After the specimens were dry (about 15
minutes), three small smudges of graphite cement were placed
at the edge of the carbon tape and the mounting peg. The
mounted glochidia were then coated with 200 angstroms of
gold-pallatium and examined under an ETEC Autoscan scanning
electron microscope. These methods were described by
Hoggarth (1988) and Kennedy et al. (1991). Glochidia shell
surface, lateral side, and micropoints were photographed for
each of the mussel species. Measurements of the glochidia
were made by measuring ten glochidia under a light
microscope.
CHAPTER 3
RESULTS
Reproductive Biology
Mature glochidia were collected from Elliptoideus
sloatianus late February through mid April (1996 and 1997).
This species is a confirmed tachytictic breeder (Table 3-1).
Gravid individuals were collected from the stream with water
temperatures ranging from 8.00 C to 15.0' C. Mature
glochidia were collected from E. sloatianus individuals as
small as 120 mm (anterior edge to posterior edge). Eggs
were released in January 1996 as rigid white conglutinates.
The conglutinates were 10 to 15 mm long and 1.5 mm wide.
Viable glochidia were released in late February 1996 in
the form of white conglutinates that easily disintegrated
when disturbed. Elliptoideus sloatianus glochidia remained
viable for three days after they were released by the female
mussel.
Three potential host fish were identified from nine
species of fish infested with Elliptoideus sloatianus
glochidia: Gambusia holbrooki, Poecilia reticulata, and
Percina nigrofasciata (Table 3-2). Transformation of the
glochidia required 17 to 21 days on Gambusia holbrooki, 16
25
CHAPTER 3
RESULTS
Reproductive Biology
Mature glochidia were collected from Elliptoideus
sloatianus late February through mid April (1996 and 1997).
This species is a confirmed tachytictic breeder (Table 3-1).
Gravid individuals were collected from the stream with water
temperatures ranging from 8.00 C to 15.0' C. Mature
glochidia were collected from E. sloatianus individuals as
small as 120 mm (anterior edge to posterior edge). Eggs
were released in January 1996 as rigid white conglutinates.
The conglutinates were 10 to 15 mm long and 1.5 mm wide.
Viable glochidia were released in late February 1996 in
the form of white conglutinates that easily disintegrated
when disturbed. Elliptoideus sloatianus glochidia remained
viable for three days after they were released by the female
mussel.
Three potential host fish were identified from nine
species of fish infested with Elliptoideus sloatianus
glochidia: Gambusia holbrooki, Poecilia reticulata, and
Percina nigrofasciata (Table 3-2). Transformation of the
glochidia required 17 to 21 days on Gambusia holbrooki, 16
25
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28
to 21 days on P. reticulata, and 20 days when encysted on
P. nigrofasciata in an average water temperature of 20.5 C
30 C.
Even though Percina nigrofasciata occur in the same
microhabitat as Elliptoideus sloatianus, P. nigrofasciata
were not considered a primary host fish because only two
glochidia transformed from one P. nigrofasciata (Table 3-3).
A glochidia transformation rate of 16% may not be sufficient
enough to support a wild population of E. sloatianus.
Gravid Lampsilis subangulata were found throughout the
year and are a confirmed bradytictic breeder (Table 3-1).
On 19 May 1995, an individual L. subangulata was discovered
producing a superconglutinate in Cooleewahee Creek, Baker
County, Georgia. This was the first time L. subangulata had
been documented producing a superconglutinate. Lampsilis
subangulata were observed releasing superconglutinates when
water temperatures warmed to about 22.50 C.
Superconglutinates were collected from late May (1995 and
1996) to early July (1995 and 1996) when water temperatures
were between 22.00 C and 23.5 C (Table 3-4). The glochidia
remained viable for about four days after the
superconglutinate was released.
Host fish were identified by infecting 10 species of
fish with Lampsilis subangulata glochidia. Potential host
fish were identified as Gambusia holbrooki, Poecilia
reticulata, Lepomis macrochirus, Micropterus punctulatus,
O3 T -3 -O
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Table 3-4. Dates and temperatures when Lampsilis
subangulata were found releasing superconglutinates
in Cooleewahee Creek, GA.
Number of
Date Superconglutinates Temperature
Found
19 May 1995 4 23.0C
1 June 1995 2 23.0C
22 June 1995* 1 23.0C
23 June 1995* 2 23.0C
16 May 1996 0 20.0C
29 May 1996 5 20.0C
31 May 1996 24 20.0C
6 June 1996 5 23.5C
15 July 1996 1 23.0C
16 July 1996* 1 23.0C
17 July 1996* 1 23.0C
* indicates superconglutinates released in the
laboratory.
and M. salmoides (Table 3-5). Transformation occurred in 13
to 14 days for G. holbrooki, 15 to 17 days for P.
reticulata, 13 days for L. macrochirus, 11 to 15 days for M.
punctulatus, and 12 to 16 days for M. salmoides. The
average water temperature during this transformation period
was 22.50 C 2.5' C.
Only one Lepomis macrochirus out of ten L. macrochirus
tested in the experiment was able to produce one juvenile
Lampsilis subangulata (Table 3-6). The production of a
juvenile mussel from only 10% of the fish is not sufficient
to support the existence of a mussel population. When M.
punctulatus and M. salmoides were exposed to L. subangulata
glochidia 100% of the fish produced juvenile mussel (Table
3-6). Micropterus punctulatus and Micropterus salmoides are
both considered effective host fish for Lampsilis
subangulata. However, the results of a t-test indicated the
M. salmoides was significantly more effective at
transforming L. subangulata glochidia when compared to the
M. punctulatus (df=30; t=-2.49; P=0.019). During the
treatment it was assumed that each fish has equal
opportunity of attaching glochidia and that a point of
saturation was reached.
Gravid Medionidus penicillatus were found at
Chickasawhatchee and Kinchafoonee creeks during the months
of March (1996), April (1996), September (1995), and
November (1996) and is therefore considered a bradytictic
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34
breeder (Table 3-1). Gravid M. penicillatus were found when
water temperatures were between 11.0' C and 13.0 C.
Medionidus penicillatus were observed at Chickasawhatchee
Creek in March (1996) and April (1996) completely out of the
substrate, laying on their umbos with their white glochidia-
filled gills pushed to the edge of the shell, flapping their
thickened dark mantles (Brim Box, personal communication)
The mantle-flapping behavior could possibly be a mechanism
to attract the proper host fish. This behavior was also
observed on subsequent trips to collect gravid individuals.
Host fish for Medionidus penicillatus were determined by
infesting seven species of fish with thier glochidia.
Glochidia attached to every fish with which they were
exposed. However, Gambusia holbrooki, Poecilia reticulata,
Etheostoma edwini, and Percina nigrofasciata were the only
fish species to produce juvenile mussels (Table 3-7).
Transformation occurred on G. holbrooki in 19 to 21 days, on
P. reticulata in 30 to 32 days, on E. edwini in 30 to 37
days, and on P. nigrofasciata in 29 to 33 days in water held
to an average temperature of 21.50 C. The glochidia
remained viable for only two days after they were released
by the female mussels.
When Etheostoma edwini and Percina nigrofasciata were
exposed to M. penicillatus glochidia, 100% of the E. edwini
and P. nigrofasciata tested transformed M. penicillatus
0
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36
glochidia (Table 3-8). Etheostoma edwini and P.
nigrofasciata also occur in the same microhabitat as the
mussel.
Etheostoma edwini and Percina nigrofasciata are both
considered effective host fish for M. penicillatus.
However, the results of a t-test indicate that E. edwini is
significantly more effective at transforming juvenile M.
penicillatus glochidia when compared to P. nigrofasciata
(df=12; t=-6.40; P=0.00003). During thetreatment it was
assumed that each fish had an equal opportunity of attaching
glochidia and that a point of saturation was reached.
Gravid Pleurobema pyriforme were collected at
Chickasawhatchee and Kinchafoonee creeks during the months
of March, April, May, June, and July (1995 and 1996) and are
therefore considered to be tachytictic breeders (Appendix A-
1; Table 3-1). Viable glochidia were collected from P.
pyriforme in water temperatures ranging from 13.0' C in the
spring, to 25.00 C in late summer. The glochidia were found
to remain viable for three days after being released by the
female.
Female Pleurobema pyriforme usually aborted
conglutinates after several days in captivity.
Conglutinates contained glochidia in several stages of
development; eggs, developing eggs, and glochidia. Low
numbers of viable glochidia made the fish infestation
process difficult.
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38
Yokley (1972) also observed the development of glochidia
in multi-stage conglutinates by Pleurobema cordatum. The
production of conglutinates with glochidia in different
developmental stages is thought to be an indication that the
mussel releases a few glochidia at a time instead of the
entire conglutinate (Yokley 1972).
Host fish for Pleurobema pyriforme were identified by
infesting 10 species of fish with P. pyriforme glochidia.
Only the Pteronotropis hypselopterus, Gambusia holbrooki,
and Poecilia reticulata transformed glochidia into juvenile
mussels (Table 3-9). Transformation occurred in 20 to 25
days when attached to the P. hypselopterus, 18 to 21 days
when the glochidia attached to the G. holbrooki, and 19 days
when attached to P. reticulata. The average water
temperature during the transformation period was 23.00 C
3.00 C.
Even though 46% of the Pteronotropis hypselopterus
tested produced juveniles and the number of juveniles
produced by each fish varied, P. hypselopterus are
considered primary host fish for Plerobema pyriforme (Table
3-10).
Development of Immunity
Lampsilis subangulata juveniles were collected from each
Micropterus salmoides after the first and secondinfestations
with glochidia. Only one of the four Micropterus salmoides
rU
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41
produced more juvenile L. subangulata after the second
infestation (Table 3-11). A t-test indicated that there was
a significant reduction in the number of juvenile mussels
after the first infestation when compared to the number of
juveniles produced after the second infestation (df=6;
t=2.01; P=0.04).
Glochidia Reaction to Nonindigenous Fish
Poecilia reticulata successfully transformed glochidia
from Elliptoideus sloatianus, Lampsilis subangulata,
Medionidus penicillatus, and Pleurobema pyriforme. However,
the number of fish producing juveniles and the number of
juveniles produced by each P. reticulata was highly variable
(Table 3-12). None of the four mussel species had glochidia
transform on every P. reticulata infected in the experiment.
Glochidia Morphology
The shape of Elliptoideus sloatianus glochidia is sub-
elliptical (Figure 3-la). The height (dorsal to ventral) is
153 5 pm and the length (anterior to posterior) is 173 6
im. Hooks are lacking and pitting, small holes on the
surface of the shell, is minimal (Figure 3-1b). Shell
sculpturing is loose-looped and increases near the umbo
region. Micropoints, small extensions along the flange,
41
produced more juvenile L. subangulata after the second
infestation (Table 3-11). A t-test indicated that there was
a significant reduction in the number of juvenile mussels
after the first infestation when compared to the number of
juveniles produced after the second infestation (df=6;
t=2.01; P=0.04).
Glochidia Reaction to Nonindigenous Fish
Poecilia reticulata successfully transformed glochidia
from Elliptoideus sloatianus, Lampsilis subangulata,
Medionidus penicillatus, and Pleurobema pyriforme. However,
the number of fish producing juveniles and the number of
juveniles produced by each P. reticulata was highly variable
(Table 3-12). None of the four mussel species had glochidia
transform on every P. reticulata infected in the experiment.
Glochidia Morphology
The shape of Elliptoideus sloatianus glochidia is sub-
elliptical (Figure 3-la). The height (dorsal to ventral) is
153 5 pm and the length (anterior to posterior) is 173 6
im. Hooks are lacking and pitting, small holes on the
surface of the shell, is minimal (Figure 3-1b). Shell
sculpturing is loose-looped and increases near the umbo
region. Micropoints, small extensions along the flange,
Table 3-11. Number of juvenile Lampsilis subangulata
produced from each Micropterus salmoides after two
consecutive infestations.
M. salmoides Number of transformed
size mm juveniles
recovered after
1"' infestation 2nd infestation
45 35 19
51 43 14
58 22 33
64 30 5
-H
.. -
0
-Iz- *-1.
l 0 C)
U0 0
CO
0 0) 0
-H -I f
-4
Q4 '-1Y
d 1 -
aWQ
300
CnTi 0-J
* co
o T) 0
0 CU
S.-i
OH r
a4 > -Q
C14 -
-40 '-1
-'-1 -1J0
1 41 O
1 0 )
--1 U C
Cn a 'Ol
1 rQ
U *'- tl~
,iwQ 0
cr0 3
E-i C ^
-I O
0
4r -,-rI
0U +1
UO
= 4-4 (
OC
.-4
H CO)
(l)
04
U) C
0
60
C-)
C l
3o
M C
SO
m K3 ) ri
N~ ^r N^ 1
r- i
Figure 3-1. Glochidium of Elliptoideus sloatianus; a. shell
shape and surface; b. lateral view of valve; c. flange with
micropoints.
cover 15 percent of the flange, a flattened region at the
edge of the shell, region in complete vertical rows (Figure
3-ic).
The glochidia shape of Lampsilis subangulata is sub-
spatulate (Figure 3-2a). The height (dorsal to ventral) is
267 8 pm and the length (anterior to posterior) is 212 7
pm. Hooks are lacking and pitting is present, but few in
number (Figure 3-2b). Shell sculpturing is tight-looped;
and greatest near the umbo region. The micropoints cover
half of the flange region in complete vertical rows (Figure
3-2c).
Medionidus penicillatus glochidia is sub-spatulate
shaped (Figure 3-3a). The height (dorsal to ventral) of the
glochidia is 298 6 pm and the length (anterior to
posterior) is 239 7 pm. Hooks are lacking and pitting is
not apparent (Figure 3-3b). The valve surface is smooth.
Micropoints are blunt lanceolate in shape and decrease in
size from the proximal to distal on the flange (Figure 3-
3c). The micropoints are organized in complete vertical
rows and cover about 75 percent of the flange.
The shape of Pleurobema pyriforme glochidia is sub-
elliptical (Figure 3-4a). The height (dorsal to ventral) of
the glochidia is 172 3 pm and the width (anterior to
posterior) is 164 5 pm. Hooks are lacking and pitting is
apparent on the valve (Figure 3-4b). The surface of the
valve has a slight loose-looped texture near the umbo
46
A
Figure 3-2. Glochidium of Lampsilis subangulata; a. shell
shape and surface; b. lateral view of valve; c. flange with
micropoints.
Figure 3-3. Glochidium of Medionidus penicillatus; a. shell
shape and surface; b. lateral view of valve; c. flange with
micropoints.
48
Z -._. -
Figure 3-4. Glochidium of Pleurobema pyriforme; a. shell
shape and surface; b. lateral view of valve; c. flange with
micropoints.
49
region. The blunt lanceolate-shaped micropoints are
arranged in an unorganized fashion covering only a quarter
of the flange (Figure 3-4c).
CHAPTER 4
DISCUSSION
Reproductive Biology
A primary host fish for a freshwater mussel is a fish
species that can meet the reproductive requirements and
ensure the existence for a particular mussel species. The
first step of a primary host fish is the need to have
contact with the mussel species. The next requirement for a
primary host fish to meet the reproductive requirements of a
freshwater mussel is the ability to successively transform
glochidia. Freshwater mussels are virtually sessile
organisms. Therefore, the fish species must also frequent
areas with the freshwater mussel in order for the
mussel/fish interaction to occur.
Glochidia from Elliptoideus sloatianus, Lampsilis
subangulata, Medionidus penicillatus, and Pleurobema
pyriforme successfully transformed on Gambusia holbrooki and
Poecilia reticulata. However, G. holbrooki and P.
reticulata are not considered a primary host fish for any of
the target mussel species. Neither G. holbrooki nor the
nonindigenous P. reticulata occupies the same microhabitat
as any of the target mussels species. Gambusia holbrooki
CHAPTER 4
DISCUSSION
Reproductive Biology
A primary host fish for a freshwater mussel is a fish
species that can meet the reproductive requirements and
ensure the existence for a particular mussel species. The
first step of a primary host fish is the need to have
contact with the mussel species. The next requirement for a
primary host fish to meet the reproductive requirements of a
freshwater mussel is the ability to successively transform
glochidia. Freshwater mussels are virtually sessile
organisms. Therefore, the fish species must also frequent
areas with the freshwater mussel in order for the
mussel/fish interaction to occur.
Glochidia from Elliptoideus sloatianus, Lampsilis
subangulata, Medionidus penicillatus, and Pleurobema
pyriforme successfully transformed on Gambusia holbrooki and
Poecilia reticulata. However, G. holbrooki and P.
reticulata are not considered a primary host fish for any of
the target mussel species. Neither G. holbrooki nor the
nonindigenous P. reticulata occupies the same microhabitat
as any of the target mussels species. Gambusia holbrooki
51
and P. reticulata are therefore considered satellite host
fish.
The primary host fish for Elliptoideus sloatianus
remains unknown. Aside from Gambusia holbrooki and Poecilia
reticulata, Percina nigrofasciata was the only other fish
species to transform E. sloatianus glochidia.
The use of only 6 Percina nigrofasciata in the
experiment could have resulted in the low number of
transformed juvenile mussels. Future host fish studies for
Elliptoideus sloatianus should re-examine the potential of
P. nigrofasciata as a primary host fish. The transformation
of two glochidia by P. nigrofasciata may indicate that the
host fish belongs to the Percidae family. Future host fish
experiments should also test other darter species, for
example Etheostoma beani, E. edwini, E. swaini, and E.
parvipinne.
Lampsilis subangulata glochidia transformed on Gambusia
holbrooki, Poecilia reticulata, Lepomis macrochirus,
Micropterus punctulatus, and Micropterus salmoides.
However, only the M. punctulatus and the M. salmoides are
primary host fish. Even though L. macrochirus are found in
the same microhabitat as L. subangulata and were observed
consuming superconglutinates, L. macrochirus are not
considered a primary host fish. Lepomis macrochirus are
considered satellite host fish because they failed to
effectively transform L. subangulata glochidia.
52
The results of the t-test indicated that Micropterus
salmoides are more effective at transforming juvenile L.
subangulata than M. punctulatus. These results may be
misleading because the M. salmoides used in the experiment
were about twice the size as M. punctulatus (Table 3-5).
Lampsilis subangulata glochidia mainly attach to the gill
filaments of Micropterus sp.. Micropterus salmoides have
larger gill chambers compared to M. punctulatus, providing a
larger area for more glochidia to encyst. However, both are
effective at transforming L. subangulata glochidia to
support a population.
The identification of Micropterus punctulatus as a
primary host fish is of special interest because M.
punctulatus is not a native fish to the Apalachicola,
Chattahoochee, Flint, and Ochlockonee river drainages.
Micropterus punctulatus was introduced and is now well
established in the drainage. The ability for M. punctulatus
to act as a primary host fish for Lampsilis subangulata is
reassurance that the introduction of M. punctulatus will not
disrupt the reproductive cycle of L. subangulata.
Medionidus penicillatus glochidia transformed on
Gambusia holbrooki, Poecilia reticulata, Etheostoma edwini,
and Percina nigrofasciata. However, the results of the t-
test indicated that E. edwini are significantly more
effective at transforming M. penicillatus glochidia than P.
nigrofasciata (p=0.0003). These results were unusual since
53
E. edwini used in the experiment were smaller than P.
nigrofasciata (Table 3-7). One reason for these results
could be the glochidia's ability to transform on the gills
and fins of E.edwini. Unlike E. edwini, P. nigrofasciata
appeared to only transform glochidia on its gills. The
transformation of glochidia belonging to the subfamily
Lampsiline on fins is not a common event. However, in some
cases hookless glochidia have been observed encysting on
soft fish fins (Coker et al. 1921).
Under laboratory conditions Etheostoma edwini is the
superior primary host fish but these conclusions may not
hold true in the wild. Other parameters must be considered
before E. edwini can be considered a more effective primary
host fish than P. nigrofasciata. For example, E. edwini may
not be as common as P. nigrofasciata in the wild. If E.
edwini is not common in the field, then it may not be a very
reliable primary host for M. penicillatus.
Etheostoma edwini and Percina nigrofasciata transformed
Medionidus penicillatus glochidia effectively. Even though
the number of juvenile mussels produced varied, 100% of E.
edwini and P. nigrofasciata tested in the experiment
produced juvenile mussels (Table 3-8). The production of
juvenile M. penicillatus by E. edwini and P. nigrofasciata
could support a M. penicillatus population. Under
laboratory conditions E. edwini and P. nigrofasciata are
considered primary host fish for M. penicillatus.
54
Under laboratory conditions Pteronotrcpis hypselopterus
was identified as a primary host fish for Pleurobema
pyriforme. The transformation of glochidia on only 46% of
the Pteronotropis hypselopterus tested in this experiment
may be a common occurrence in the field. Pteronotropis
hypselopterus are common fish that travel in large schools.
A mussel species relying on a fish species that is small in
size and occurs in schools such as P. hypselopterus may not
require a 100% glochidia transformation rate to support the
reproduction of a mussel population. For example, a mussel
species that relies on a host fish species that tends to be
less common and does not occur in schools, like Micropterus
salmoides, must attempt to encyst a large number of
glochidia on as many fish it comes in contact with. These
explanations are only assumptions and require further
studies.
Development of Immunity
The development of immunity was observed when five
Micropterus salmoides were infected with Lampsilis
subangulata glochidia twice. The development of an immune
response has been studied since Coker et al. (1921). Myers
and Millemann (1977) reported a decrease in the ability of
salmonids to produce juvenile Margaritifera margaritifera
after they were infected three times with glochidia. Luo
55
(1993) also reported similar results after darters were
infected three times with glochidia from Medionidus
conradicus. The development of an immunity against
glochidia could be of concern in streams with endangered
mussels and low fish densities. Mussels, such as L.
subangulata that rely on a small number of host fish species
to complete their life cycle, may be at risk of lowered
reproductive capabilities in areas with low numbers of
available host fish. When a species of mussel relies on the
same fish repeatedly for glochidia transformation, the fish
could become more resistant to glochidial attachment. The
length of time that the immune response is effective remains
unknown.
Glochidia Reaction to Nonindigenous Fish
There is a growing concern regarding the introduction of
nonindigenous fish species and how they may affect the
reproductive cycle of North American mussels (Unionids).
The preliminary results of this study indicate that Poecilia
reticulata, a nonindigenous species, could act as a
satellite host fish for the four mussel species tested.
However, P. reticulata is an unreliable satellite host fish.
The number of P. reticulata producing juveniles and the
number of juvenile mussels produced by each P. reticulata
varied for each of the mussel species (Table 3-12). There
56
is speculation that P. reticulata could act as a universal
host fish because this fish species evolved where Unionids
were absent. However, more research is nedded with more
mussel species to confirm these results.
Another nonindigenous fish species that was introduced
into the Apalachicola, Chattahoochee, Flint, and Ochlockonee
river drainages is Micropterus punctulatus. Fortunately, M.
punctulatus was identified as a primary host fish for
Lampsilis subangulata. Micropterus punctulatus appears to
be a comparable primary host fish to M. salmoides, a native
fish in the Apalachicola, Chattahoochee, Flint, and
Ochlockonee river drainages.
These results may indicate that the introduction of
nonindigenous fish into areas where there are native mussels
may not interfere with the freshwater mussel reproductive
cycle. However, more studies must be conducted to confirm
these preliminary results.
Glochidia Morphology
The photos taken of the glochidia from each of the four
mussel species did provide enough information to distinguish
each species. Elliptoideus sloatianus glochidia and
Pleurobema pyriforme glochidia are sub-elliptical in shape
(Figures 3-la and 3-4a, respectively However, E.
sloatianus glochidia have sculpting near the umbo and the
57
shell is more compressed than P. pyriforme glochidia.
Lampsilis subangulata and Medionidus penicillatus glochidia
have similar sub-spatulate shell shapes (Figure 3-2a and 3-
3a). However, one feature that can distinguish the two
species is the highly sculptured umbo region of L.
subangulata glochidia. The umbo region of M. penicillatus
glochidia lacks sculpturing.
Unfortunately, there is not enough information to
distinguish the glochidia of the target mussel species from
any of the other mussel species that occur in the
Apalachicola, Chattahoochee, Flint, and Ochlockonee river
drainages. Elliptoideus sloatianus and Pleurobema pyriforme
have glochidia shapes that might be confused with glochidia
from the genus Elliptio. The glochidia shapes of Lampsilis
subangulata and Medionidus penicillatus are similar to most
of the Lampsiline glochidia in the Apalachicola,
Chattahoochee, Flint, and Ochlockonee river drainages. More
research is needed before the mussel species from the
Apalachicola, Chattahoochee, Flint, and Ochlockonee river
drainages can be identified to the glochidia level.
Conservation Issues
Based on these results, Elliptoideus sloatianus,
Lampsilis subangulata, Medionidus penicillatus, and
Pleurobema pyriforme rely on reproductive mechanisms (lures,
58
i.e., a superconglutinate or mantle flapping) or host fish
that are sensitive to habitat degradation. Lampsilis
subangulata and M. penicillatus rely on lures to visually
attract a host fish. Increased suspended sediments in the
water column reduce visibility thereby rendering host fish-
attracting lures ineffective (Haag et al. 1995). If host
fish are unable to see the lure the interaction between the
mussel and host fish is reduced. As a result, the
reproduction capabilities of these freshwater mussels could
be inhibited.
Mussel species that rely on water currents as a
mechanism to complete their reproductive cycle could be
negatively affected by the construction of a reservoir.
Elliptoideus sloatianus have small, light glochidia that
easily move in the water current. Production of glochidia
easily distributed by water currents could be a mechanism to
carry glochidia to a host fish. Lampsilis subangulata also
relies on water current to effectively display a
superconglutinate to lure the primary host fish.
Reproduction for E. sloatianus and L. subangulata would be
greatly reduced in areas where water currents have been
drastically slowed or damned.
The most important part of the freshwater mussel's
reproductive cycle is the presence of a primary host fish
population. If the host fish population is absent or in low
densities, reproduction for that particular mussel species
59
will be impossible (Weiss and Layzer 1995). Angermeier
(1995) found that fish species belonging to the darter or
minnow groups are more vulnerable to extinction based on
their physiographic range. Mussel species like Medionidus
penicillatus and Pleurobema pyriforme, that rely on fishes
from groups which are more vulnerable to extinction, could
share the increased risk of extinction.
CHAPTER 5
Conclusion
Elliptoideus sloatianus is a tachytictic breeder and is
gravid from late February to April. The primary host fish
for E. sloatianus remains unknown. Satellite host fish were
identified in the laboratory as Gambusia holbrooki and
Poecilia reticulata.
Lampsilis subangulata is a bradytictic breeder and is
gravid throughout the year. Lampsilis subangulata releases
superconglutinates from late May to early July when water
temperatures are between 20.00 C and 23.5 C. The primary
host fish for L. subangulata were identified in the
laboratory as Micropterus punctulatus and Micropterus
salmoides. Satellite host fish were identified in the
laboratory as Gambusia holbrooki, Poecilia reticulata, and
Lepomis macrochirus.
Medionidus penicillatus is a bradytictic breeder and is
gravid September to May. The primary host fish for M.
penicillatus were identified in the laboratory as Etheostoma
edwini and Percina nigrofasciata. Satellite host fish were
identified in the laboratory as Gambusia holbrooki and
Poecilia reticulata.
Pleurobema pyriforme is a tachytictic breeder and is
gravid March to July. The primary host fish was identified
in the laboratory as Pteronotropis hypselopterus. The
61
satellite host fish were identified as Gambusia holbrcoki
and Poecilia reticulata.
Host fish identification for endangered and threatened
mussels is an important part of a recovery plan. By
understanding the specific reproductive requirements of
freshwater mussels (required host fish and mechanisms for
the attachment of glochidia to a host fish), streams with
low densities of host fish or alterations which interfere
with the mussel's ability to attract a host fish can be
identified as streams at risk of losing the mussel
populations. When disturbed streams have been identified
conservation efforts can then be implemented in order to
save the mussel populations as well as the fish populations.
The close association between mussels and fish is just
another example of how ecosystems are interconnected;
conservation efforts should focus on protecting the entire
ecosystem and avoid focusing on a single species.
Many questions surrounding the biology of freshwater
mussels, especially the four proposed mussels in this
experiment, remain unanswered. The host fish for
Elliptoideus sloatianus remains unknown. However, there is
speculation that a fish belonging to the Percidae family may
be a host fish.
The primary host fish for Lampsilis subangulata,
Medionidus penicillatus, and Pleurobema pyriforme need to be
verified in the wild. For example, the host fish identified
62
in this experiment were determined in the laboratory. The
bodies and gills of fish collected, during periods of
glochidia release from streams where the target mussels
occur, must be inspected for encysted glochidia. The
identification of the mussel species to the glochidia level
may be difficult with standard microscopes, but SEM pictures
as used this research, could provide vital information in
identifying the glochidia to the species level. If a
primary host fish were identified in the laboratory and
found to have encysted glochidia belonging to the same
mussel species, that fish would be a confirmed primary host
fish for that mussel species.
The identification of host fish is an important part of
a recovery plan. However, there is also a need to determine
whether existing populations of Elliptoideus sloatianus,
Lampsilis subangulata, Medionidus penicillatus, and
Pleurobema pyriforme are viable. There has been recent
controversy surrounding the sampling techniques for
recruitment of a mussel population. Designing a technique
or method for sampling freshwater mussel recruitment could
be used to test whether conservation efforts or recovery
plans are working for a target mussel species.
APPENDIX A
SITE RECORDS FOR MUSSEL COLLECTIONS
The following is a list of sites where each mussel species
was collected for this project. The county, state, road
crossing, and drainage is presented for each location site.
4J 4-J
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tfl
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APPENDIX B
SITE RECORDS FOR FISH COLLECTIONS
The following is a list of sites where each fish
species was collected for this project. The county, state,
road crossing, and drainage is presented for each location
site.
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BIOGRAPHICAL SKETCH
I was born in Gainesville, Florida on April 15, 1968.
In 1986 I graduated from P.K. Yonge Laboratory School. In
May 1993 I received a B.S.F.R.C degree in natural resource
conservation from the School of Forest Resources and
Conservation at the University of Florida. After completing
an internship with the U.S. Forest Service Fisheries
Department in Washington state, I entered the University of
Florida once again in pursuit of a master's degree in
wildlife ecology and conservation.
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