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A Survey of Helminths of Ondatra Zibethicus inEight States and Four Foreign CountriesMike P. Lyons

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Recommended CitationLyons, Mike P., "A Survey of Helminths of Ondatra Zibethicus in Eight States and Four Foreign Countries" (1993). McCabe ThesisCollection. Paper 11.

The Edwin P. McCabe Honors Program

Senior Thesis

"A Survey of Helminths of Ondatra Zibethicus in Eight States and Four Foreign Countries"

Mike P. Lyons

May 1993

Langston University Langston, Oklahoma

A SURVEY OF HELMINTHS

OF ONDATRA ZIBETHICUS IN EIGHT STATES

AND FOUR FOREIGN COUNTRIES

By

Mike Lyons

Department of Biology

Division of Arts and Sciences

Langston University

Langston, Oklahoma

Submitted in partial fulfillment of the requirements of the E. P. McCabe Honors Program

July 1994

M. B. Tolson Black Heritage Center Langston University Langston, Oklahoma

A SURVEY OF HELMINTHS

OF ONDATRA ZIBETHICUS IN EIGHT STATES

AND FOUR FOREIGN COUNTRIES

ii

ACKNOWLEDGMENTS

I would like to thank the faculty in the Department of

Biology at Langston University for their assistance and

support throughout this project. Dr. James Abram, Dr.

Reuben Manning, and Dr. Sarah Thomas have all given of

themselves to see this project to completion. I would also

like to thank Dr. Joy Flasch for her indefatigable efforts

(too numerous to list) toward seeing this thesis properly

completed.

Finally, a sincere thank you to my family (mom, dad,

sister, and both brothers) whose love, support, and guidance

have helped me through life's ups and downs.

iii

TABLE OF CONTENTS

Chapter Page

I. INTRODUCTION 1

Purpose of Parasite Surveys 1 Approach to the Project 1 Limitations of the Study 2 Background of the Study 2

E. REVIEW OF THE LITERATURE 3

Beckett and Gallicchio's Ohio Survey 3 Maryland Studies 3

Abram's Work 4 Dozier's Study on Salinity 4 Harris' Finding of External Parasites 4 Penn's Louisiana Survey 4

Chandler's Texas Survey 4 Wootten and Murrell's Michigan Study 5 Illinois Studies 5 Dyer and Klimstra's Work 5 Jilek's Study 5 Eastman and Worley's Montana Survey 6 Forrester's Florida Study 6 Foreign Survey 6

Gibson and McKiel's Ontario Study 6 Rigley and Threlfall's Newfoundland Study 7 Shiryaev's USSR Study 7 Murai, Tenora, and Stanek's Hungary Study 7 Ewald's German Study 8

m. DESCRIPTION OF STUDY AREA AND NECROPSY EXAMINATION 9

Description of Marshes 9 Classification of Habitat 9

iv

Types of Muskrat Dwellings 10 Sites for Muskrat Traps 10 Environmental Factors 10 Necropsy Examination Protocol 11

IV. RESULTS AND DISCUSSION 13

Nematodes Found 14 Trematode Table 15 Trematode Figures 16 Cestode Table 18 Cestode Figures 19 Nematode Table 20 Nematode Figures 21

V. SUMMARY AND CONCLUSION 22

Current Trends in Survey Sites 22 Summaries of Studies 22 Chapter Summaries 26 Final Comments 26

BIBLIOGRAPHY 27

v

CHAPTER I

INTRODUCTION

The muskrat, Ondatra zibethicus. is a large member of

the Order Rodentia and regarded as the United States' most

important fur bearing mammal (Abram, 19 69) . Helminths, or

parasitic worms, include amongst its members: trematodes

(flukes), cestodes (tape worms) and nematodes (round worms).

Parasite surveys based on geography and subspecies of the

host, Ondatra zibethicus. have pieced together information

gaps based on these criteria and enabled investigators to

construct an overall picture of helminth parasites in the

United States and elsewhere.

The question of helminths in representative host

species can be addressed either through necropsy

examinations or through literature surveys. Literature

surveys can provide adequate insight into parasite

distribution and is applicable in this investigation. Thus,

the approach here is a literature review of helminths of

muskrats. The notable criteria in formulating this study

are an exhaustive literature search, description of muskrat

habitats, and revelation of parasite burden in eight states

and four foreign countries.

The approach to this project essentially is evaluating

the variation in helminth kind and burden. The supporting

1

2

literature suggests a fairly wide variation in the kinds of

species given the ecological factors that would impact on

this study.

The study area includes Ohio, Maryland, Louisiana,

Texas, Michigan, Illinois, Montana, and Florida. Also

included are four foreign countries: Canada, the former

Soviet Union, Hungary, and Germany. The choice of these

particular states and countries was due to the availability

of relevant literature. This represents one of the

limitations on this study.

Another limitation was not being able to perform

necropsy examinations on muskrats in order to reveal

helminths. Due to stringent regulations regarding humans

laws and protection of fur-bearing mammals, trapping seasons

have been greatly reduced and regulations for scientific

investigation are now lengthy and cumbersome. However, a

description of a necropsy examination that most researchers

follow is given in Chapter IV.

Parasitic invasion of the muskrat was first chronicled

in 1858 by Joseph Leidy. However, the first in-depth study

of helminths in muskrats was made by Barker and his co­

workers (1915). In 42 muskrats, 881 helminth parasites

(mostly trematodes) were found, including eight previously

unknown species, three new nematodes, and two new cestodes.

CHAPTER II

REVIEW OF THE LITERATURE

Since Barker's monumental work Parasites of the

American Muskrat in 1915, perhaps the most comprehensive

helminthological study on muskrats has been done by Beckett

and Gallicchio (1967). From research based in Portage

County, Ohio, they derived an extensive chart listing the

various species of helminths found in Ondatra zibethicus.

In 130 muskrats examined, ten species of trematodes, two

species of cestodes, five species of nematodes, and one

genus of acanthocephalans were found.

Studies in Maryland clearly demonstrate ecological

variation as well as helminth diversity impacting muskrats.

One of the pioneering spirits in parasite surveys was E. W.

Price (1931). J. B. Abram's works thirty-five years later

revealed findings similar to those of Price as well as a

broad diversity of parasite differences existing in the

marshland of the Eastern Shore and the mountains of

Maryland's piedmont. Abram's survey revealed the following

trematodes: Echinostoma revolutum. Ouinqueserialis

3

4

ouincrueserialis. Wardius zibethidUS, EdhihbCfrasmus

schwartzii. Nudacotvle nQyiga; cestode, Taenia taeniaformis:

and nematode, Trichiuris trichiura (1969).

Extensive Maryland studies were also conducted by

Dozier and Harris. Dozier's study (1947) of the Dorchester

County marshes presented the various aspects of salinity on

tidal marshes and their influence on muskrat production.

Harris (1952) studied the biology of the Dorchester County

muskrat and observed various external parasites.

In 1942, Penn wrote of the helminths in Louisiana

muskrats in the bayous and marshes of that region. During

the 1939 - 1940 trapping season, he found 9.06% incidence of

Porceohalus crotali in Louisiana muskrats. His study of

their life cycle found that the adults of Porcephalus

crotali live in the lung cavities of the reptilian host.

The eggs, which are located in the reptilian sputum, are

ingested by the muskrat and eventually migrate to the lungs

to mature. Penn also found trematodes in Louisiana

muskrats, including Nudacotvle novica and Echinochasmus

schwartzii.

In southeastern Texas, A. C. Chandler conducted a

helminth survey of thirty-six muskrats. Sixteen of the

animals were collected near Port Arthur in Jefferson County,

while the other twenty were collected a few miles northeast

of High Island in Chambers County. Necropsy examinations

yielded three species of trematodes (two of which include

Nudacotvle novica and Echinochasmus schwartzii), four

5

species of nematodes, and no cestodes.

In Michigan, the fluke Ptyalincola ondatrae was found

in the salivary glands and other oral organs of Ondatra

zibethicus (Wootten and Murrell, 1967). Prior to this

study, these organs had never been cited as locations for

fluke infestation in muskrats. Anodonta qrandis, a fresh

water mussel, serves as the molluscan host for the encysted

metacercarial stages of the fluke. Although Errington

(1963) did not mention bivalves as a part of the muskrat

diet, experimental muskrats were shown to consume three to

six bivalves daily. It has been concluded that when the

Douglas and Carp lakes are frozen, bivalves constitute a

substantial portion of the diet of muskrats.

In 1978, two separate studies were done in southern

Illinois. Dyer and Klimstra found that of 209 muskrats

studied, 139 were infected with one or more of the following

species: Echinostoma revolutum. Qujpqueserialia

cruincrueserialis. Ascaris sp., Capillafia sp. , NematOSPiPPide

lonaispiculata. and Rodentolepis evaginata. In those same

three counties, Jilek collected eighty-one muskrats,

seventy-five of which were infected with one or more of the

following species of trematodes: Echinostoma revolutum.

Ouinoueserialis ouincrueseralis. and Echinopatyphiwn

recurvatum. The finding of £. recurvatum represented a new

state record.

In a Montana study, Eastman and Worley (1979) examined

360 rodents and insectivores (representing five species) to

6

determine the intermediate host of the alveolar hydatid

tapeworm Echinococcus multilocularis. Two muskrats were

found to have E. multilocularis liver cysts. This was the

first confirmed natural infection with this larval cestode

to be reported in the muskrat in North America.

In 1987, Forrester and his co-workers studied the

helminths of 114 round-tailed muskrats from sugarcane fields

in southern Florida. There were eight species of

helminths found: seven nematodes and one cestode. Results

showed 113 of 114 muskrats studied were infected with one to

five species, with intensities varying from one to 2,443.

In this sample of round-tailed muskrats, the helminth

community was dominated by satellite species, apparently

derived from cotton rats (Siomodon hisoidus) .

Surveys in Foreign Countries

Apart from the United States, the vast majority of

contemporary muskrat parasite surveys have been done in

Canada and the former Soviet Union. Hungary, Germany, and

other European countries constitute the few remaining sites

of surveys.

A muskrat in north central Ontario was found to harbor

the nematode Dracunculus insianis subcutaneously (Gibson

and McKiel, 1972) . The occurrence of Eustroncrvlides sp.

larvae intramuscularly in this muskrat is the first reported

natural infection of mammal by nematodes of this genus.

7

In a 1981 Newfoundland study, Rigley and Threlfall

reported that of 114 muskrats examined, eleven species of

helminths were found: seven Digenea, two Cestoda, and two

Nematoda. Most of the helminths recovered in this study

preferred the proximal sixty percent of the small intestine.

Also, Diolostomum merai was found in a mammal for the first

time.

A study done along the Ilir river delta in the Balkash

territory (USSR) showed a change in hydatid and

macracanthorhynchosis infection of the muskrat attributable

to irrigation (Shiryaev, 1983). In dry years, the

prevalence of helminthoses increased. However, a reduction

was noticed when water conditions improved. Shiryaev found

that irrigation changes the extent of muskrat contact with

difinitive hosts of the helminths.

In an experimental stock of Ondatra zibethicus in

Hungary, all individuals died at the age of thirteen to

sixteen months (Murai, Tenora, and Stanek, 1989). During

necropsy examinations, various members of strobilocerci were

always found in the liver parenchyma. In liver lobes and

tissue, six to thirty-two metacestodes of Hydatiaera

taeniaeformis were recovered.

In Germany, 492 foxes and fifty-three cats (definitive

hosts)and 1,101 muskrats (intermediate hosts) were examined

for the tapeworm Echinococcus multilocularis (Ewald, 1990).

Results showed 16.1% of the adult foxes, 6.5% of fox

cubs, 0% of cats, and 5% of the muskrats were infected with

8

the tapeworm. In the Black Forest, extremely high rates of

infestation were found in the foxes and muskrats, while

much lower rates were seen in the southern Upper Rhine.

Previous studies showed significantly higher rates of

infestation. An increase in parasites and differences in

the degree of postmortem autolysis of the study material

can be pointed to as reason for the increase. A proposed

reason for the increase in parasites may be the greater

density in the fox population.

CHAPTER III

DESCRIPTION OF THE STUDY AREA AND NECROPSY EXAMINATION

Throughout the United States and abroad, preferred

habitats for muskrats are marshes. Marshes are wet areas

where such non-woody plants as cattails, grasses, rushes,

and sedges grow. Also marshes are found in places where the

soil is permanently moist ground.

The Eastern Shore of Maryland is, at this time, the

most abundantly populated area of Ondatra zibethicus. and

it is an estuarine marsh (Abram, 1969). An estuarine marsh

is one which is washed by salt water tides part of the time

and by fresh water the rest of the time. The "mix" of salt

and fresh water provides a supply of food that supports the

flora and fauna of the area.

Marshes are usually classified according to the

dominant plant life present. On the Eastern Shore of

Maryland, the most abundant marsh species are three-square

sedge, needlerush, saltmarsh three-square, salt grass,

saltmeadow cordgrass, tall cordgrass, saltmarsh cordgrass,

and cattail. The three-square sedge and cattail make up 75%

of the muskrat diet in Maryland (Harris, 1952).

9

10

Those muskrats not situated in the marshlands of the

eastern and southern states live in burrows or tunnels and

dig in the banks of streams. They make houses by plastering

water plants such as cattails and reeds together with mud.

These muskrat houses are dome-shaped structures located in

open marshes. The second type of muskrat home in marshes is

the den. These dens are burrows into the banks of either

marshes, streams, or ponds and usually go undetected in the

marshes unless the tides have fallen (Dozier, 1947). Those

that tunnel in banks usually have more than one underwater

entrance or the entrances may be above water.

In determining potential sites for muskrat traps, there

are several indicators to look for. These include droppings

on nearby partially submerged rocks, den entrances in the

banks of marshes, ponds, or streams that seem active, plant

cuttings in the water or on the edge of the bank, feed

beds, and diggings along the banks.

Just as favorable environmental factors are directly

proportional to the muskrat's survival and well being, so

too is the ecology of the helminth parasite. In the case of

parasitic organisms, the requirements for survival and

development in the environment outside of the host include

sufficient oxygen, favorable temperature, and adequate

moisture. In addition, there must be ample protection from

the hazardous effects of heat from direct sunlight,

desiccation, and freezing. For some species, the physical

environment provides stimuli for 1) hatching the eggs of

11

many nematodes and trematodes, 2) direction of movement,

such as cercarie swimming to or away from light, 3)

periodic activity, shown by trichostrongyles that migrate up

and down grass blades in response to light intensity,

diurnal periodicity of microfilariae, and time of day when

cercariae leave their snail hosts, and finally 4) molting

of the first and second stage strongyles and

trichostrongyles (Olsen, 1974).

Due to the stringent regulations regarding humane laws

and protection of fur-bearing mammals, trapping seasons

have been greatly reduced and regulations for scientific

investigation are now lengthy and cumbersome. Therefore,

actual necropsy examination of muskrats were unable to be

performed for this study. An explanation of such an

examinations follows.

Necropsy Examination

Almost all of the aforementioned researchers followed

routine necropsy protocol when examining the muskrats for

helminth infection. A ventral midline incision is made

running from below the xiphoid process of the sternum to the

hind legs of the muskrat. Most major organs are removed,

including the heart, lungs, liver, stomach, small intestine,

caecum, bladder, and kidneys, and are initially examined

grossly for helminths.

The stomach, small intestine, and caecum (the blind

12

pouch forming the beginning of the large intestine) are

separated, tied off, and placed in their own containers of

physiological saline. In each organ, a continuous

lengthwise slit is made to expose the lumen and dislodge any

helminths that may adhere to the stomach or intestinal wall

or mucous membrane. Stripping the organ by running it

between the fingers is performed twice to insure recovery of

all helminths.

The visceral organs, including the heart, kidney,

bladder, liver, and lungs, are removed, minced, placed into

physiological saline and incubated at 37 degrees Celsius.

Existing parasites within the tissue usually migrate out

following this procedure.

CHAPTER IV

RESULTS AND DISCUSSION

This survey chronicles the invasion of Ondatra

zibethicus by helminths in eight states and four foreign

countries. The states include Ohio, Maryland, Louisiana,

Texas, Michigan, Illinois, Montana, and Florida. The

foreign countries are Canada, the former Soviet Union,

Hungary, and Germany.

Seven different species of trematodes (flukes) were

found in the eight states. Maryland muskrats alone harbored

five of the seven species found. Only one species, however,

was found in the other four countries studied. Diplostomum

merai. the only trematode discovered outside of the states

in the study, represented a significant find. Recovered

from a muskrat in Newfoundland, it represented the first

time this species of trematode has been found in a mammal.

The former Soviet Union, Hungary, and Germany, as well as

Montana and Florida, constitute the sites where there was no

evidence of trematode invasion of muskrats.

Cestodes (tapeworms), the class of helminths least in

13

14

number in this study, were discovered in four of the eight

states. Three different species were found in Ohio,

Maryland, Montana, and Florida. As for the foreign

countries, cestodes represented the only class of helminths

found in more than one country. Cestode infection was

documented in both Hungary and Germany. Hvdatiaera

taeniaformis. also known as Taenia taeniaformis. was found

in Ohio and Maryland, but also in Hungary. Echinococcus

multilocularis was found in Montana and also in Germany.

Nematodes (round worms) of seven different species were

found in the eight states. However, the seven species were

concentrated in only four states: Ohio, Maryland, Illinois,

and Florida. Illinois muskrats were found to carry three

different species of nematodes. Canada was the only

foreign country in the study where nematodes were found.

Two nematodes, Dracunculus insianis and Eustronovlides sp.,

were recovered from a north central Ontario muskrat.

The tables on the following pages show the helminths

found infecting muskrats in the eight states studied. Each

table represents one of the three major classifications of

helminths: trematodes (flukes), cestodes (tapeworms), and

nematodes (roundworms).

Following each table is a figure of one or more of the

helminths represented in the table.

M. a Tolson BlacK her.taga c*„iar X Langston University

Langston, Oklahoma

TABLE I

TREMATODE INFECTION OF MUSKRATS IN SELECTED SITES

OH MD LA TX MI IL MT FL

Echinostoma revolutum OXOOOXOO

Echinochasmas schwartzi OXXXOOOO

Ouinqueserialis quinqueserialis OXOOOXOO

Wardius zibethicus XXOOOOOO

Nudacotvle novica OXXXOOOO

Ptvalincola ondatrae OOOOXOOO

Echinoparvphium recurvatum OOOOOXOO

X Denotes Presence of Parasite

O Denotes Parasite Not Found

FIGURE I

TREMATODES LEFT: OUINOUESERIALIS OUINOUESERIALIS

RIGHT: ECHINOSTOMA REVOLUTUM

FIGURE II

TREMATODES CONTINUED LEFT: WARDIUS ZIBETfflCUS

RIGHT: NUDACOTYLE NOVICA

18

TABLE B

CESTODE INFECTION OF MUSKRATS IN SELECTED STATES

OH MD LA TX MI IL MT EL

Taenia taeniaformis XXOOOOOO

Echinococcus multilocularis OOOOOOX O

Raillietina sigmodontis OOOOOOOX

X Denotes Presence of Parasite

O Denotes Parasite Not Found

19

FIGURE HI

CESTODE SCOLEX OF TAENIA TAENIAEFORMIS

TABLE m

NEMATODE INFECTION OF MUSKRATS IN SELECTED STATES

OH MD LA TX MI IL MT FL

Trichuris opaca XXOOOOOO

Trichiuris trichiura OXOOOOOO

Ascaris sp. OOOOOXOO

Capillaria sp. OOOOOXOO

Nematospiroides longispiculata OOOOOXOO

Strongyloides sigmodontis OOOOOOOX

Trichostrongvlus spp. OOOOOOOX

X Denotes Presence of Parasite

O Denotes Parasite Not Found

FIGURE IV

NEMATODES ABOVE: TRICHURIS TRICHIURA

A. ADULT FEMALE B. ADULT MALE C. EGG BELOW: ASCARIS LUMBRICOEDES

REFERENCE NOT TO BE TAKEN FROM THIS ROOM

CHAPTER V

SUMMARY AND CONCLUSION

In summary, parasite surveys, which were the popular

discipline in parasitology in early twentieth century, have

drastically fallen off. The majority of helminth studies

in muskrats are now being conducted in Canada and Europe.

Research before the 1970's, however, shows that the most

comprehensive studies on helminths in muskrats up to that

time were done in the United States.

Barker's work (1915), the first in-depth study of

helminths in muskrats, chronicled the extraction of 881

helminths, mostly trematodes. Since Barker's study, perhaps

r.he most important work on the subject was done by Beckett

and Gallicchio in Portage County, Ohio (1967). From 130

muskrats examined, they derived an extensive chart listing

the various species of helminths found in Ondatra

zibethicus.

Research in Maryland by Price (1931), Abram (1969),

and Dozier (1947) point to ecological factors influencing

22

23

helminth diversity in muskrats. Some thirty-five years

after Price's Maryland survey, Abram's research in the

Marshland of the Eastern shore and the mountains of

Maryland's piedmont revealed a broad diversity of parasites

that exist in muskrats. Dozier's study showed various

aspects of salinity on tidal marshes and their influence on

muskrat production in Dorchester County.

In 1942, Penn chronicled the helminths of Louisiana's

muskrats in the bayous and marshes of that region. His

findings included two species of trematodes: Nudacotyle

novica and Echinochasmus schwartzii. Penn also found an

annelid worm, Porceohalus crotali. in the lung tissue of

muskrats.

A.C. Chandler (1941) conducted a helminth study in

thirty-six muskrats in southeastern Texas. Necropsy

examinations yielded three species of trematodes (two of

which were Echinochasmus schwartzii and Nudacotvle novica),

four species of nematodes, and no cestodes.

In 1967, Wootten and Murrell found the trematode

Ptyalincola ondatrae in the salivary glands and other oral

organs of Michigan muskrats. Anodonta arandis. a freshwater

mussel, served as the molluscan host for the encysted

metacercarial stages of the fluke. Although bivalves were

not previously known to be part of the muskrat diet, it was

concluded that when the Douglas and Carp lakes froze,

muskrats consumed three to six bivalves daily.

In 197 8, two separate studies on helminths were done in

24

southern Illinois. In 209 muskrats studied, Dyer and

Klimstra found that 139 were infected with at least one of

the following species: Echinostoma revolutum.

Quincrueserialis quinqyeserialig, Agg^rig sp. , Caoillaria

sp. , Nematospiroides loncrispiculata, and Rodentolepis

evaainata. In those same three counties, Jilek concluded

that seventy-five of eighty-one muskrats studied carried one

or more of the following trematodes: Echinostoma revolutum.

Quincrueserialis quincrueserialis. and Echinooarvphium

recurvatum. The finding of E. recurvatum in muskrats

represented a new state record.

In 1979, Eastman and Worley examined Montana muskrats

to determine the intermediate host of the alveolar hydatid

tapeworm Echinococcus multilocularis. Two muskrats were

found to harbor £. multilocularis liver cysts. This was the

first confirmed natural infection with this larval cestode

to be found in a North American muskrat.

Forrester and his co-workers (1987) studied the

helminths of 114 round-tailed muskrats in southern Florida's

sugarcane fields. Results showed 113 of the 114 muskrats

were infected with at least one of the eight helminth

species found, which included seven nematodes and one

cestode. In this sample of muskrats, the helminth community

was dominated by satellite species apparently derived from

Sicrmodon hisoidus. the cotton rat.

Apart from the United States, most contemporary studies

are being done in Canada, the former Soviet Union, Hungary,

25

Germany, and a few other European countries. In 1972,

Gibson and McKiel found Dracunculus insianis subcutaneously

in a north central Ontario muskrat. They also found

Eustroncrvlides sp. larve intramuscularly in a muskrat. In

another Canadian survey, researchers found that of 114

Newfoundland muskrats studied, eleven species of helminths

were found: seven Digenea, two Cestoda, and two Nematoda

(Rigley and Threlfall, 1972). Most of the helminths

recovered in this study preferred the proximal 60% of the

small intestine.

A 1983 study in the former Soviet Union showed a change

in hydatid and macracanthorhynchosis infection of the

muskrat attributable to irrigation (Shiryaev). In dry

years, the prevalence of helminthoses increased. A

reduction was noticed, however, when water conditions

improved.

In a 1989 Hungary survey (Murai, Tenora, and Stanek),

all of the members of an experimental stock of muskrats died

between the ages of thirteen to sixteen months. Necropsy

examinations revealed six to thirty-two metacestodes of

Hvdatidera taeniaeformis in the liver lobes and tissues.

In Germany, 1,101 muskrats were examined for the tape

worm Echinococcus multilocularis (Ewald, 1990). Five

percent of the muskrats were found to be infected with the

tapeworm. Extremely high rates of infection were documented

in the Black Forest, while much lower rates were seen in the

southern Upper Rhine area.

26

Chapter III described the preferred habitats for

muskrats in the United States and abroad--the marshes. The

Eastern Shore of Maryland is, at this time, the most

abundantly populated area of muskrats in the United States,

and it is an estuarine marsh (Abram, 1969) . Marshes are

usually classified according to their dominant plant life.

Those muskrats not situated in the marshlands live in

burrows or tunnels and dig in the banks of streams.

Descriptions of helminth ecology and a necropsy protocol are

also given in Chapter III.

Chapter IV compiled the helminth surveys to give a

clearer picture of the worms found. Three charts are given,

showing the trematode, cestode and nematode infestation of

muskrats in the eight states studied. Sketches are also

given of some of the worms.

Stringent regulations by conservation groups, humane

zealots and environmentalists have made access to fur-

bearing animals difficult; therefore, necropsy examinations

of muskrats were unable to be performed for this study. A

detailed explanation of the necropsy examination is given in

Chapter IV, however.

Initially this study was intended to survey helminths

of the Oklahoma muskrat. This state, however, apparently

has not been the site of a helminth study of Ondatra

zibethicus. In the absence of the opportunity to survey

parasites of Oklahoma muskrats, this study focuses on

updating existing literature regarding helminth parasites of

muskrats.

BIBLIOGRAPHY

Abram, J. B. 1969. Some gastrointestinal helminths of Ondatra zibethica Linnaeus, the

muskrat in Maryland. Proc. Helm. Soc. Wash. 36:93-95.

Ameel, D. J. 1944. A life history of Nudacotvle novica Barker, 1916 (Trematoda,

Notocotylidae). J. Parasit. 30(4):257-263.

Anderson, D. R., and R. L. Beaudoin. 1966. Host habitat and age as factors in the

prevalence of intestinal parasites of the muskrat. Bull. Wildl. Dis. Assoc.

2:70-77.

Ball, L. 1952. Notes on the helminth parasites of muskrats from western Colorado. J.

Parasit. 38:83-84.

Barker, F. D. 1915. Parasites of the American muskrat (Fiber zibethicus). J. Parasit.

1:184-197.

Beckett, J. V., and V. Gallicchio. 1967. A survey of helminths of the muskrat Ondatra z.

zibethica Miller, 1912 in Portage county, Ohio. J. Parasit. 53:1169-1172.

Byrd, E. E., and R. J. Reiber. 1942. Mammalian trematodes n. Three flukes from small

mammals. J. Tenn. Acad. Sci. 17:143-148.

Chandler, A. C. 1941. Helminth Parasites of muskrats in southeast Texas. J. Parasit.

27:175-181.

Cheng, T. C. 1973. General parasitology. Academic Press, New York.

Dunagan, T. T. 1957. Helminth parasites of Alaskan muskrats. Trans. Amer. Micr. Soc.

27

28

76:318-320.

Dozier, H. L. 1947. Salinity as a factor in Atlantic Coast tide water muskrat production.

Trans. N. Amer. Wildl. Conf. 12:398-420.

Dyer, W. G., and W. D. Klimstra. 1978. Gastrointestinal helminths of the muskrat

Ondatra zibethicus in southern Illinois USA. Trans. Dl. State Acad.

Sci. 70:356-362.

Eastman, K. L., and D. E. Worley. 1979. The muskrat as an intermediate host of

Echinococcus multilocularis in Montana. J. Parasit. 65:34.

Edwards, R. L. 1949. Internal parasites of central New York muskrats (Ondatra

zibethica zibethica L.) J. Parasit. 35:547-548.

Errington, P. L. 1963. Muskrat populations. Iowa State University Press, Ames.

Ewald, D. 1990. Distribution of the tapeworm Echinococcus multilocularis in the fox

(Vulpes vulpes) and muskrat (Ondatra zibethicus) in the Freiburg administrative

district. Mitteilungen Des Badischen Landesvereins Fuer Naturkunde Und

Naturschutz E V Freiburg Im Breisgau. 15:81-100.

Forrester, D. J. 1987. Ecological analysis of the helminths of round-tailed muskrats

Neofiber alleni True in southern Florida USA. Can. J. of Zool. 65:2976-2979.

3ibson, G. G., and D. A. McKiel. 1972. Dracunculus insignis (Leidy, 1858) and larval

Eustrongylides sp. in a muskrat from Ontario, Canada. Can. J. Zool.

50:897-900.

Gilford, J. H. 1954. A survey of muskrat helminths in Illinois. J. Parasit. 35:547-548.

Harris, V. T. 1952. Muskrats on tidal marshes of Dorchester County. Chesapeake biol.

Lab., Dept. Res. and Ed., Solomons Island, MD. 36p.

Harwood, P. D. 1939. Notes on Tennessee helminths. IV. North American trematodes

of the subfamily Notocotylinae. J. Tenn. Acad. Sci. 14:332-340; 421-437.

Jilek, R. 1978. Trematode parasites of the muskrat Ondatra zibethicus in southern

Illinois USA. Trans. 111. State Acad. Sci. 70:105-107.

Leidy, J. 1888. Trematodes of the muskrat. Proc. Acad. Nat. Sci. Phil. 40:126.

Maggenti, A. 1981. General nematology. Springer-Verlag, New York.

Meyer, M. C., and J. R. Reilly. 1950. Parasites of muskrats in Maine. Amer. Midi.

Natural. 44:467-477.

Murai, E., et al. 1989. A typical strobilocercus (Cestoda: Taeniidae): a parasite

in experimental stocks of Ondatra zibethicus (Rodentia). Miscellanea Zoologica

Hungarica 5:21-27.

Olsen, O. W. 1974. Animal parasites. University Park Press, Baltimore.

Penn, G. H. 1942. Parasitological survey of Louisiana muskrats. J. Parasit. 28:348-349.

Price, E. W. 1931. Four new species of trematode worms from the muskrat, Ondatra

zibethica. with a key to the trematode parasites of the muskrat. Proc.

U.S. Natl. Mus. 79:1-13.

Rankin, J. S. 1946. Helminth parasites of birds and mammals in western Massachusetts.

Amer. Midi. Natural. 35:756-768.

Rausch, R. L. 1946. The parasites of Ohio muskrats. J. Wildl. Mgmt. 10:70.

Rider, C. L., and R. W. Macy. 1947. Preliminary survey of the helminth parasites of

muskrats in northwest Oregon, with description of Hvmenolepis ondatrae

n. sp. Trans. Amer. Micr. Soc. Wash. 24:141-142.

Rigley, M. D., and W. Threlfall. 1981. Helminth parasites of the muskrat (Ondatra

30

zibethicus (L.)) in Newfoundland. Can. J. Zool. 59:2172-2176.

Shiryaev, V. V. 1983. Dynamics of muskrat infection by helminths in the Balkash

territory (USSR) related to irrigation. Byulleten'-Moskovskogo-Obshchestva-

Ispytatelei-Prirody. 88:62-67.

Skijabin, K. I. 1964. Keys to the trematodes of animals and man. Univ. of Illinois Press,

Urbana.

Tiner, J. D. 1950. Two new species of Trichuris from North America, with

redescriptions of Trichuris opaca and Trichuris leporis (Nematoda: Aphasmidia).

J. Parasit. 36:350-355.

Wardle, R. A. 1974. Advances in the zoology of tapeworms 1950-1970. Univ. of

Minnesota Press, Minneapolis.

Wootton, D. M., and K. D. Murrell. 1967. Ptvalincola ondatrae. gen. et. sp. n.

(Trematoda: Brachylaimidae), a fluke inhibiting the salivary gland of muskrats.

J. Parasit. 53:739-742.

VITA

Mike Patrice Lyons

Bachelor of Science

and

Candidate for the Completion of

E. P. McCabe Honors Program

Thesis: A SURVEY OF HELMINTHS OF ONDATRA ZIBETHICUS IN EIGHT STATES AND FOUR FOREIGN COUNTRIES.

Major: Biology

Biographical Information:

Personal Data: Born in Oklahoma City, Oklahoma, November 5, 1971, the son of Mack Lyons Jr., and Lois Lyons.

Education: Graduated from Bishop McGuinness High School, Oklahoma City, Oklahoma, in May 1989. Received Bachelor of Science degree from Langston University in May 1993. Entered Meharry Medical College, Nashville, Tennessee, in the Fall of 1993.