Parasites of pine marten, Martes americana in northeastern Alaska
by Christopher Rowe Scranton
A thesis submitted in partial fulfillment of the requirements for the degree of Master of Science in
Veterinary Science
Montana State University
© Copyright by Christopher Rowe Scranton (1986)
Abstract:
No systematic survey has ever been done on internal parasites of pine marten, Martes americana, in
Alaska. The purpose of this study was to determine the prevalence and intensity of internal parasites,
including Trichinella spiralis, in marten inhabiting the boreal forest ecosystem in northeastern Alaska.
One hundred and forty-one marten carcasses were collected in the Yukon Flats and Fairbanks areas.
The carcasses, which had been frozen from one to twenty-nine months, were thawed at room
temperature and examined using standard necropsy techniques. Muscle tissue was examined for
encysted forms using a standard peptic digest method. All parasites were collected, counted, examined,
and identified to species when possible. Live Trichinella spiralis larvae were fed to laboratory mice to
determine post freezing infectivity. Marten stomach contents were also examined to obtain information
on feeding habits in relation to parasite fauna.
12.7% of the marten examined were infected with Trichinella spiralis, with intensities of infection
ranging from .04 to 1,856 larvae per gram of muscle tissue. This is a new locality record for Trichinella
infection in marten. Viable Trichinella spiralis larvae were obtained from carcasses that had been
frozen up to 16 months. The presence of a cold resistant strain of Trichinella spiralis in Alaskdn pine
marten would have adaptive advantages for maintenance of this strain in an arctic ecosystem. Four
other internal parasites were identified in this study: Soboliphyme baturini, Molineus patens (a new
host record), Alaria mustelae and Taenia martis (a new locality record). Three other parasites were
found but not identified to species because of inadequate material. These include a Taenia sp.,
unidentified tissue nematodes, and an ascaroid nematode. PARASITES OF PINE MARTEN, MARTES AMERICANA
IN NORTHEASTERN ALASKA,
by
Christopher Rowe Scranton
A thesis submitted in partial, fulfillment
of the requirements for the degree
of
Master of Science
in
Veterinary Science
MONTANA STATE UNIVERSITY
Bozeman, Montana
June 1986
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ccT 2
ii
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of a thesis submitted by
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for
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degree
at
Montana
State
University, I agree that the Library shall make it available
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iv
ACKNOWLEDGEMENTS
I wish, to thank 'personnel of the Alas ka D e p a r t m e n t of
Fish and Game for their help in obtaining marten carcasses,.
I w o u l d also like to extend m y thanks to the m a n y trappers
in Venetie and Chalkyitsik for providing the majority of the
carcasses used in this study.
Finally,
a special note of appreciation to the Montana
State Unive rsi ty V et eri na ry Res ea rc h Lab staff including
Gayle Callis for her histological preparation of TrichinelIa
infected m u s c l e tissue, M e rr ie Menden hal l for all p h o t o ­
graphic w o r k and Dr. David W o r l e y for his support in ma n y
aspects of the study.
•
TABLE OF CONTENTS
1
Page
ACKNOWLEDGEMENTS............................................. iv
LIST OF TABLES . :.................................... '........vi
LIST OF FIGURES............................................. vii
ABSTRACT...........................
viii
INTRODUCTION................................................... T
MATERIALS AND METHODS......................................... 5
RESULTS........................................................ 9
DISCUSSION.................................................... 15
I
SUMMARY...... '................................... ■
........... 3 4
REFERENCES CITED
36
vi
LIST OF TABLES
TABLE
PAGE
1.
Prevalence and intensity of internal parasites
of 141 marten from northeastern Alaska(1984-85)...... 10
2.
Infectiyity of Trichinella larvae from Alaskan
marten in Swiss Webster mice........................... 1 1 ,
3.
Food items collected from 36 marten stomachs
.14
vii
LIST OF FIGURES
FIGURE
PAGE
I.
Study area in northeastern Alaska where, marten
parasit es w e r e collect ed October 19 8 4 - M a r c h
1985
............................................. .... 6
II .
Unidentified intramuscular nematode from Alaskan
mar te n.................................. ..............13
Ill.
Copulatorv bursa and spicules of Molineus patens
from the small intestine of Alaskan marten...... 16
IV.
Molineus patens showing enlargement of copulatory
bur sa ................................................. 17
V. .
Cross section of Trichinella spiralis-infected
....................... 20
muscle from Alaskan marten
VI .
Soboliphyme baturini collected from the
stomach of an Alaskan mar ten ........................ 22
VII.
Whole mount of Alaria mustelae from the
small intestine of Alaskan marten.................. 24
VIII .
Alaria mustelae from the small intestine
of Alaskan mart en.................................... 25
IX.
Hooks of Taenia martis from Alaskan m a rte n.........27
X.
Mature proglottid of Taenia martis from Alaskan
mart en ................................................ 28
XI.
Taenia martis from Alaskan marten.................. 29
XII.
Frequency distribution of helminths from 141
32
Alaskan mart en....................................... 32
viii
ABSTRACT .
No s y s t e m a t i c survey has ever been done on internal
parasites of pine marten, Martes americana, in Alaska.
The
pur pose of this study was to d e t e r m i n e the pre va len ce and
intensity of internal parasites, includi ng Tri chine Ila
spiralis, in marten inhabiting the boreal forest ecosystem
in northeastern Alaska.
One h u n d r e d and fort y - o n e m a r t e n carc a s s e s were
colle cted in the Yukon Flats and Fairbanks areas.
The
carcasses, wh i c h had been frozen fr om one to t w e n t y-n in e
months, were thawed at room temperature and examined using
standard nec rop sy techniques.
M u s c l e tiss ue was e xam in ed
for encys ted forms using a sta ndard peptic digest method.
Al I parasites we r e collected,
counted,
examined,
and
identifi ed to species when possible.
Live T r i c h i n e l la
spiralis larvae w e r e fed to laboratory m i c e to det e r m i n e
post freezing infectivity.
M a r t e n s t o m a c h contents we r e
also e x a m i n e d to obta in i n f o r m a t i o n on feeding habits in
relation to parasite fauna.
12.7% of th e m a r t e n e x a m i n e d w e r e i n f e c t e d w i t h
Trichinella spiralis, with intensities of infection ranging
from .04 to 1,856 larvae per gram of muscle tissue.
This is
a new locality record for Trichinella infection in marten.
Viable T r i c h i n e l la spiralis larvae wer e obt ai ne d from
carcasses that had been frozen up to 16 months. The presence
of a cold r e s i s t a n t ' strain of T r i c h i n e l la spiralis in
Alaskd n pine m a r t e n w o u l d have adaptive advanta ges for
m a i n t e n a n c e of this strain in an arctic ecosystem.
Four
other internal par asi tes were identified in this s t u d y :
Soboliphyme baturini, M olineus patens (a new host record),
Alar ia m uste lae and Taenia m artis (a n e w loc ali ty record).
Three other parasites wer e found but not identif ied to
species bec aus e of inadequ ate material.
These include a
Taenia sp., u n i d e n t i f i e d tissue nematodes, and an ascaroid
nematode.
I
INTRODUCTION
The
purpose
of
th i s
study
was
to
determine
the
prevalence and intensity of internal parasites of marten in
nor t h e a s t e r n Alaska.
D e t e r m i n a t i o n of the pre sen ce
and
frequency of tissue infections with Trichinella spiralis was
of
special
implications.
study
and
area.
the
interest
due
to
possible
human
health
Marten are sometimes eaten by people in the
Freezing
i n f e c ti vit y
resistance,
range
of
post-freezing
larvae
of
the
viability,
TrichinOl la
strain in marten from Alaska was also of major interest in
this study.
Food items from m a r t e n sto ma ch contents also
we re noted wh en possible.
Alt ho ug h this was not a maj o r
em p h a s i s of the study, i n f o r m a t i o n on diet w a s considered
relevant to an understanding of parasite transmission cycles
in a predatory species such as the marten.
Fe w
parasites
sy ste m a t i c
surveys
of pine marten,
have
Martes
been
done on internal
americana.
Holmes
(1963)
examined twenty-four marten carcasses from the District of
Mackenzie and reported Alaria taxideae Swanson and Erickson,
1946 in
six. Tae ni a m artis (Z e d e r , 1803) Freeman, 1956 in
seven and Taenra m ust ela e G m e l i n , 1790 in three animals.
Poole et al.
one
hundred
(1983) recovered five species of helminths from
thirty-nine
taxideae in seventy-five;
marten
Taenia sp.
/
from
Manitoba:
Alaria
(cf. martis martis)
in
2
sixteen;
T aenia
m ustelae
in nine;
B a y l isa sc ari s
devosi
Spren t , 1952 in one; and Trichinel la sp. Rai I I i e t , 1895 in
one.
four
Trichinel la spiralis was reported in t w o of twe nt ymarten
fro m
twenty-two
of
M o nt ana
thi rt y- si x
(W o rle y
et
marten
al.,
from
1974)
Brit ish
and
in
Col u m b i a
(Schmitt et al., 1976).
So m e
studies
have
touched
on
several
parasitism
in co nju nct ion w i t h broader based
research.
Morgan
(1943)
rep or te d
first
rep orted
from
Alask a
by
Swartz
of
biological
Sob o l i p h y m e
Petrow, 1930 in one marten from North America.
was
aspects
baturini
£h baturini
(1968),
who
collected two specimens from the stomach of a marten trapped
near Fairbanks.
Eighteen of sixty-two marten from Colorado
e x a m i n e d by Olsen (1952) w e r e infected wi t h the l u n g w o r m
C r e n o s o ma co lo ra doe ns is Olsen,
1952.
Taenia m a r t is was
first reported in marten from Ontario by Freeman (1956).
this report,
he compiled descriptions of taenioid cestodes
fro m M u s t e l i d a e .
marten
from
In
Ala ri a taxidea e was
Oritario
by
Pearson
first rep orted
(1956).
Joh ns on
in
(1979)
outlined the morphology and life history of Alaria mustelae.
Based upon his research,
he c ons id ere d A. tax id ea e and A.
canadensis to be synonyms of A. mustelae.
As a result of the co rrela ti on b e t w e e n pr e y items and
parasitism,
the food habits of m a r t e n were of interest in
the pres ent study.
The feeding habits of m a r t e n are well
documented in many parts of North America, including Alaska.
3
C o w a n and M a c K a y (1950) e x a m i n e d one 'hundred and ninetyseven marten scats from British Columbia and Alberta.
They
reported that sixty-six percent of the food items consisted
of mice and voles.
we r e
the
Red-backed voles, Clethrionomys gapperi,
pr ef e r r e d
food
ite.m.
R ed- ba cke d
voles
were
reported in forty percent of two hundred fifty marten from
Britis h
Columbia
(Quick,1955).
Douglass
et
al.
(1983)
reported that seventy-five percent of the marten scats from
the Northwest Territories contained Microtus species.
Red-
backed voles made up thirteen percent of the diet.
Studies fr om W y o m i n g (M u r i e , 1961), Idaho (Marshall,
1951) and M o n t a n a
similar
food
(W e c k w e r t h and
habit
data.
Hawley,
Microtines
1962)
reported
occurred
most
frequently in the marten diet in those states.
Zielinski
et
al.
(1983)
and
Hargis
and
McC ul l o u g h
(1984) repor te d s i m i l a r data on food habits of m a r t e n from
California.
M i crotus species o c c u r r e d m o s t fre qu entl y as
food items in their study.
Douglas squirrels, Tamiasciurus
douglasii, were also important prey of California marten.
Two studies of food habits of Alaskan marten have been
reported.
Microtine rodents occurred in fifty-eight percent
of four hundred sixty-six scats collected in interior Alaska
(L e n s i n k
et
al.,
1955).
h u d s o n i c u s , sn o w s h o e
grouse,
hare,
Red
squirrels,
Lepus
Tamiasciurus
a m ericanus
and
spruce
Canachites canadensis made up the remainder of the
anima l food items.
Buskirk and M a c D o n a l d (1984) reported
4
m i c r o t i n e s in s eventy percent of four hund red sixty- sev en
scats
collected
in south-central
Alaska.
Red-backed voles
we r e the mo s t c o m m o n food taken by mar te n in their study.
5
MATERIALS AND METHODS
The
survey area
in the nor th eas te rn
part
of Alaska
inc luded the Yukon Flats and Fai rba nks vic in itie s (Figure
I). The study area consist ed of boreal spfu ce / a s p e n forest
with
some
willow
species
and
streams and low lying a r e a s .
c o t t o nwo od s
common
along
Other species of w i l l o w and
birch were found throughout the study area.
One hundred and forty-one frozen marten carcasses were
collected
during
th e p e r i o d
October
1984-March
1985.
Thirty-five were obtained from the Alaska Department of Fish
and Game.
They w e r e supplied by trappers located on the
road syst em in the v i ci nit y of Fairbanks.
The other one
hundred and six were obtained from trappers in Venetie (76),
and Chalkytsik
(30).
These two Indian villages are located
in the Yukon Flats, about thirty mil es north of the Arctic
Circle and about two hundred miles north of Fairbanks.
Carc ass es whi ch we re frozen fro m one to tw e n t y - n i n e
mont hs were t h aw ed at r o o m temperature.
fecal
A sat ur at ed NaCl
flotation was performed to determine the presence of
cestode and n e m a t o d e eggs or larvae and coc ci dian oocysts.
Skinned weight was recorded for each carcass, and the sex of
each specimen was noted.
examined
nematodes.
Nasal cavities were dissected and
macroscopically
for
the
presence
of
nasal
6
/ Study Area
Figure I .
Study area in northeastern Alaska where marten
parasites
were collected.
October 1984March 1985.
V, Venetie; C,
Chalkyitsik; F,
Fairbanks; YR , Yukon River; T R , Tanana River.
7
The
gas tro in te sti na l
tract>
removed intact for examination.
heart
and
lungs
were
The tract was divided into
three major sections: the esophagus-stomach, small intestine
and large intestine.
section.
An e n t e r o t o m e was used to open e a c h ’
The contents were scraped and w a s h e d through a
s i x t y - m e s h screen.
Material col lected on the screen was
b a c k w a s h e d into an i l l u m i n a t e d glass o b s e r vat io n tray and
searched for parasites under low power magnification.
Intestinal parasites were isolated from the collecting
tray w i t h eye dropper s and d iss ec tin g needles.
were
then
stored
in
glycerin
alcohol
(nematodes
trematodes), or 10% phosphate buffered formalin
Spleen,
urinary
bladder,
heart
Spe ci me ns
an d
an d
(cestodes).
kidneys
were
dissected and examined using a dissecting microscope.
The
re sp ir a t o r y tree was opened, the liver was slic ed and both
organs
were placed in jars with 0.86% physiological
solutio n
and
Lockard, 1973).
screen,
agi tat ed
for
twenty
minu tes
saline
(Barber
and
The contents we r e poured onto a 100 -m es h
rinsed and backwashed into an illuminated tray for
observation.
Standard procedures
were used to prepare whole mounts
of representative helminths.
stained
carmine,
in Delafield's
Cestodes and trematodes were
hematoxylin
destained in acid alcohol,
or S e m i c h o n "s acetocleared with xylene or
cedarwood oil, and mounted whole for microscopic examination
a n d 'identification.
Nematodes
were
cleared in glycerin or
8
lactophenol and examined.
A few nem a t o d e spe c i m e n s wer e
permanently mounted in glycerin jelly.
T w e n t y - f i v e gra ms of m u s c l e tissue w e r e r e m o v e d from
the biceps femoris and semitendinosus
carcass.
region
of the thawed
This was refrozen for five to ten months and then
rethawed, chopped into small pieces and h o m o g e n i z e d in an
O m n i m i x e r wi t h a 0.7% HCl and 0.8% pepsin solution.
This
suspension was then incubated on a shaker at 37 degrees C
for five hours.
mesh
screen
The solution was then washed through a 60-
and
collected
on a 1 0 0 - m e s h
s c ree n.
The
retai ned m a te ria l was b a c k w a s h e d into a c o u n t i n g dish and
examined
for
microscope.
host tissue
Viable
T r d^chi. ne J A a
larvae
with
a
dissecting
Res ul ts we r e rec ord ed as larvae per gram of
(l.p.g.).
Trichinella
larvae were administered orally to
Swiss Webster mice, Cox strain.
Each animal received fifty-
five
The
to
one
examined
hund red
sixty
to
larvae.
ninety
days
mice
later
were
to
killed
determine
and
if
infection had occurred from the larvae obtained from marten
carcasses.
9
RESULTS
The major results of this study are summarized in Table
I.
Parasitic helminths were recovered from 88 of 141 marten
examined.
one
Soboliphyme baturini was found in the stomach of
marten.
AlI
spe cim ens
of
M olineus
p a t e n s , Alaria
m u s t e l a e , Taenia sp., and the u n i d e nti fi ed asc ar id species
were
located
in
th e
small
intestine
of
the
host.
Tr ich i n e l l a spiralis and the u n i d e nti fi ed tissu e n ema to de
w e r e found in dig est ed biceps fe m o r i s and s e m i tendinosus
muscle tissue.
The Trichinella spiralis strain
recovered from marten
in the study area demonstrated resistance to freezing at -15
degrees C.
had
been
r ec ove re d
Live larvae were recovered from one carcass that
frozen
from
for
one
16
months.
carcass
Live
that
had
larvae
been
also
frozen
were
for
7
months, two carcasses frozen for 6 months, and two carcasses
frozen
for
3 months.
carcasses examined,
from
two
of these
Of
th e
18 Tr i^h_i neJL JLa p o s i t i v e
six had live larvae present.
samples
whi c h
Larvae
were fed to whi te mi c e
induced Trichinella infections in five of twelve mice (Table
2) .
I
An unidentified tissue nematode
of 141 m a r t e n mu sc l e digests.
larva was
found in 34
Thes e were p r ese nt in low
numbers ranging from I to 12 larvae per 25 grams of
muscle
10
I
Table I.
Prevalence and intensity of internal parasites
141 marten from northeastern Alaska (1984-85)
Parasite
Prevalence of Infection
Mean Intensity
%
(Ran g e )
Trichinella spiralis
Railliet, 1895
12.7%
Soboliphyme baturini
Petrow, 1930
.7%
Molineus patens
(Dujardin, 1845)
147.2 LPG*
(0.4-1,856)
8
7.8%
5.6 (1-30)
Alaria mustelae
IBosma, 1931
11.1%
29 (1-225)
Taenia martis
(Zeder , 1803)
3.6%
Taenia sp.
(probably T . martis)
Unidentified muscle
tissue nematode
Unidentified ascaroid
nematode.
38.2%
2.8 (2-5)
2.9 (1-17)
24.1%
.09 LPG
.7%
I
*E x p r e s sed as larvae per g r a m of skeletal m u s c l e
(.04-.48)
11
Table 2. Infectivity of Trichinella larvae from
Alaskan marten in Swiss Webster white mice.
Source
Results
No. positive for /No. Inoculated
Trichinella /
LPG
I
Marten
0 / I
------
Marten
2 / 4
3.I,6.9
Marten
0 / 2
------
Marten
0 / I
------
'Marten
3 / 4
LPG = larvae per gram
2.9,9.6,16.9
12
tiss ue .
The
larvae
were
roughly
twice
the
length
of
Trichinella spiralis larvae and were noticeably thicker and
not so tightly coiled.
to freezing.
They showed considerable resistance
Live larvae of the unidentified nematode were
found in 9 of 34 positive carcasses.
obtai ned
from
months.
These
one
carcass
that
Viable specimens were
had
been
frozen
for
29
larvae were still alive and m o t i l e after
being placed in physiological saline solution for 28 days at
3 degrees C (Figure II).
One specimen
of an ascaroid
nematode
measuring 9 m m
in length was found in the small intestine of one marten.
The specimen was in poor.condition which prevented positive
identification.
AlI marten in this study were examined for
the nasal n e m a t o d e Skr jab ingy lus
sp.
No nasal n ema to des
were found.
No
parasites
kidneys,
nasal
were
passages,
found
in
hear t,
uri na ry
lungs,
bladder
locations other than those mentioned above.
or
liver,
any
other
All NaCl fecal
flotation tests were negative for helminth eggs and larvae.
Blood
was
no t
examined
for
parasites
because
of
the
inability to obtain fresh material.
Identifiable animal food items were found in 36 of 141
m a r t e n examined.
141
marten
Table 3 out lin es these findings.
examined,
78
wer e
male
and
63
were
Of the
female.
W e ig hts for the 61 mal es ranged f r o m 443 to 1,400 grams,
wi t h an aver age w e ig ht of 877.5 grams.
W e i g h t s for the 45
.4mm
I
Figure II.
I
I
Un ide nt ifi ed int ram usc ula r n e m a t o d e from
A l as kan marten. Mag ni f i c a t i o n 100 X.
14
Table 3.
Food items collected from 36 marten stomachs.
Number of marten
Food Item
containing the food item
I
Bird Parts (mostly gray jayPeriosoreus canadensis)
11
Red-backed Vole
Clethrionomys rutilus
26
Red Squirrel
Tamiasciurus hudsonicus
2
Snowshoe Hare
Lepus americanus
I
females ranged from 402 to 760 ^ra m s , with an average weight
of
614
grams.
skinning.
These
weights
are
for c a r c a s s e s
after
It was not possible to obtain w h o l e uns kin ned
carcasses in this study.
15
DISCUSSION
This
internal
research
is
par as it es
the
first
of m a r t e n
systematic
in Alaska.
survey
on
The finding of
M olineus patens (D u j a r d i n , 1845) is a ne w host record for
this species.
M o l ineus patens wa s rep orted in m i n k fr o m
Mississippi (Skinker, 1933), weasels and stoats from England
(B a I i s i n g a m , 1963) and in fisher fr om M a n i t o b a
Leonard,
1979).
It has also been reported in least weasels
(Morgan,
1943).
reported
M . p a te n s^ f r o m
including
wolverine,
skunks.
(Dick and
Balasingam
(1963)
a wide
and
variety
otter, badger,
Schmidt
of
(1965)
m u s t e I ids
and several
species of
None of these authors list pine m a r t e n as a host
for M. p a t e n s , and an ex ten siv e literature search rev ealed
no records of this nematode in marten.
The
average
approximately
spicules
length
7 mm.
ran ge d
in
Male s
of
M . patens^
a v era ge d
length
fro m
6 mm
females
in
149 m m
length.
to
was
The
17 2 mm.
Al I characteristics matched the description in Schmidt's key
to the species of M olineus
(Schmidt,
1965) for M. patens
(Figures III and IV).
Trichinella spiralis has been reported
Montana, Idaho, and W y o m i n g
Columbia
in marten from
(Worley et a I., 1974), British
(Schmitt et a I., 1976) and M a n i t o b a
Dick, 19 8 2).
(Chadee and
It has also been rep ort ed fro m a pine m a r t e n
I
Figure
III.
.2mm
Co pul a t o r y bursa and spicules of M olineus
patens from the
small intestine of Alaskan
marten.
Magnification 250 X.
17
Figure
IV.
M o l ineus
patens
showing enlargement
of
copulatory bur sa.
Each spicule has three
spikes. G , gubernaculum;
S, spicules.
18
in D e n m a r k (Clausen and Henriksen,
1976).
The finding of
Trichinella spiralis in marten is a new locality record for
Al a s k a .
Rausch
Tr jch in ell a
Alaska.
et
a I.
spiralis
They
(19 5 5 ) r e p o r t e d
survey
examined
18
of
ma n y
pine
mammal
marten
and
evi dence of infecti on wit h T. s p i r a l i s .
many
other
species
of
A l as ka n
spiralis including grizzly,
an
extensive
species
in
reported
no
This study found
mammals
pos i t i v e
black and polar bears,
for
T.
domestic
dogs, coyotes, wolves, red fox, arctic fox, least weasel,
sh ort -t ail ed w e a s e l , wolverine, lynx, s n o w s h o e h a r e , m a n y
rodent species, and several marine mammals.
Trichinel la s p i r a l is has also been rep or ted in fisher
fro m
Manitoba
Albert a
(Dies,
(Rogers,
1975)
(Dick and
1980),
and
Leonard,
1979),
in black bears
in black
and
from
et a I. (1974)
wolverines,
mountain
from
the
(Zim me rman n, 1977).
lions,
striped skunks,
from
Superior
reporte d T r i c h i n e l Ia spiralis
grizzly and black bears,
fishers,
Lake
grizzly bears
western and north central United States
Worley
in w o l v e s
bobcats,
red foxes,
fro m
martens,
and coyotes
in Montana.
The
findings
of
Trichinella spiralis
the
pres ent
from marten
is
study
which
that
resistant to freezing
for long periods of time are of considerable
would be an adaptive
show
interest.
advantage for Trichinella
spiralis
It
in
arctic regions to withstand freezing prior to ingestion by a
preda tor or scavenger.
W i nte r t e m p e r a t u r e s in the study
19
area often reach -45 degrees C. and r e mai n b e l o w freezing
for long periods.
natural
Resistance to freezing would help insure
transmission in an arctic ecosystem where infected
carcasses may not be eaten immediately.
cov er ed
by
snow
and
are not
expo sed
Carcasses are often
until
spring.
The
tendency of marten to feed on carcasses of other carnivore’s
presumably accounts for the presence of Trichinella spiralis
in Martes americana (Strickland et a l ., 1982).
There have been several studies which examined the time
of survival by Trichinella spiralis in frozen muscle.
Dies
(1980) found viable larvae in wolf mus cle w h i c h had been
frozen
at
-10 d e g r e e s
C for
18
months.
These
larvae
p ro duc ed T r i c h i n e l la infections in white laborat ory mice.
Chadee and Dick (1982)
found viable
larvae in arctic fox
muscle frozen for 14 mon th s, in polar bear muscle frozen for
12 m o n t h s , and in m a rt en m u sc le frozen for 5 months.
In
the p r es ent s t u d y , the r e co ve ry of viable larvae in m a rte n
tissue w h i c h had been frozen for 16 m o n t h s is the longest
survival time reported for Trichinella spiralis in this host'
(Figure V).
The abil ity of s y I vatic strains of T. spiralis
to survive freezing contrasts with the lethal effects of low
t e m p e r a t u r e exposure in d o m e s t i c isolates of the par asite
(Chadee and Dick, 1982).
S o b o l i p h y me b a t u r i n i
Petrow, 1930 has been reported
twic e in m a r t e n fro m Alaska (Bezdek, 1942; Swartz,
1968).
It was first reported in marten from the lower 48 states
by
Figure
V.
C r o s s s e c t i o n of T r i c h i n a I l a s p i r al!
infected muscle from Alaskan marten. Magnif
cation IOO X.
H-Im
20
21
Morgan (1943) and again in marten from Minnesota by Erickson
(1946).
S. baturini has.also been reported in wol ve rine s
from M o n t a n a
(Price,
1930),
in m i n k from Alaska
(Swartz,
1968), in least weasel, w o l v e r i n e and fisher in Min n e s o t a
(Erickson,
Chitwood,
1946)
1951).
and
in f i s h e r
The
from
Maine
(Meyer
and
baturini specimens from marten are
illustrated in Figure VI.
A l ar ia
m ustelae Bosma,
1934
was des c r i b e d in mink,
Mustela vison from South Dakota (Bosma, 1934).
the
He outlined
life cycle of this strigeid tre m a t o d e in a nor thern
prairie ecosystem.
According to B o s m a , A. mustelae requires
four hosts:
a planorbid snail is infected by free swimming
miracidia,
wh i c h hatch from eggs in the w a t e r via anima l
feces.
Cercariae develop within the snail and then emerge
to infect tadpoles.
Mesocercariae develop in the tadpoles.
A rodent or other m a m m a l be c o m e s infected by ingestion of
tadpoles
or
frogs
containing
th e
mesocercariae.
m e t a c e r c a r i a I stage develop s w i t h i n the third host.
A
The
cycle is c o m p l e t e d wh en a m a m m a l con sumes i nfe ct ed third
stage hosts con ta in in g the metacercariae.
develops
in the small
intesti ne
The adult then
of the def in i t i v e
host.
Eggs are released into the intestine and passed through the
feces.
Joh nso n
(1979) reporte d adult A. m ustelae in two
cats and a raccoon infected with mesocercariae from leopard
frogs.
He s h ow ed that four stages are.not o b l i g a t o r y for
development in the definitive host.
22
B
IOmm
I
Figure VI.
Soboliphyme baturini collected from the stomach
of an Alaskan marten.
BC, buccal capsule;
E,
esophagus;
I , intestine;
V D , vas deferens; B,
bursa ; V, vulva;
U, uterus; 0, ovary.
23
In the present study area planorbid snails were common
in most of the nu m e r o u s ponds and lak e s .
The wood frog,
Rana s y I v a t i c a , was also c o m m o n there. Several species of
voles and lemmings were also present.
with
adult
infected
A.
by
m ustelae
direct
predation on
in this
ingesti on
The marten infected
study p r e s u m a b l y bec am e
of
infected
frogs,
or
via
paratenic hosts such as voles and/or lemmings.
This is the second report of A. mustelae in Alaska.
Sekerak
(1969) first reported Alaria taxidae from marten in central
Alaska.
A. taxideae and A.canaden sis are syn o n y m s for A.
mustelae
(Johnson, 1979).
A l ar ia tax id ea e wa s
rep or te d
the District of MacKenzie
(Poole and Dick, 1983).
m u s telids
in
(Holmes,
in
pine
m a r t e n fro m
1963) and from
Manitoba
It w as also rep orted f r o m various
M i n n e s o t a , incl uding
badger,
sho rt -tai le d
weasel, and spotted and striped skunk (Swanson and Erickson,
1946).
A. canade nsi s was reporte d in striped skunk fr om
Quebec
(Webster
repor ted
in
and
Wolfgang,
wolverine
(Addison and Boles,
from
1978).
1 95 6 ).
the
AJL ar i^a sp.
Northwest
was
Ter ritor ies
Figures VII and VIII illustrate
specimens from the present study.
The finding
of Taenia martis
study was expected.
fr o m
(1979)
Manitoba
found
in
this
T. m artis has been found in pine marten
(Poole and Dick,
Taen ia
(Zeder, 1803),
sibirica
1983).
in
fisher
Dick
and Leonard
from
Manitoba,
A c c o r d i n g to Ver st er (1969 ), T. sibirica and T . int er medi a
24
.25mm
-t—
Figure VII.
------ 1
Whole mount of Alaria mustelae from the small
intestine of Alaskan marten. Magnification 50
25
l mm
I
_
_
_
_
Figure
VIII.
Alaria mustelae from the small intestine of
Alaskan marten.
PT,
posterior testes; AT,
anterior testes;
0,
ovary;
P, pseudo
sucker;
P h , pharynx;
OS, oral sucker;
V,
vitellaria; O v , ovum.
26
were reporte d in stoats and wea sel s from Eng la nd 1(L e i p e r ,
1936).
T. martis was also reported in pine marten from the
Dis tr ic t of M a c K e n z i e
(Holmes, 1963), in
w o l v e r i n e fr om
the Northwest Territories (Addison and Boles,
pine m a r t e n fr om Cz ech o s l o v a k i a (Prokopic,
1978),
1970).
and in
Taenia
martis appears to be a holarctic species.
Taeniid tapeworms are often difficult to identify even
with fresh specimens.
Freezing of these cestodes creates a
m a j o r p r o b l e m due to loss of hooks since the hooks are often
the m a j o r c rit eri on for ide nti fic ati on of T a eni a species.
Fortunately, in this study, enough hooks wer e recover ed to
assure identification of some of the specimens to T. m artis
(Figure IX).
M o s t of the u n i d e nti fi ed spe c i m e n s fit the
criteria
T.
for
m artis
as
(Figure X and Figure XI).
des cr ibed
by
V e rst er
(1969)
This is the first repo rt of this
cestode in pine marten from Alaska.
The apparent absence of Taenia mustelae
in m a r t e n fro m this study is of interest.
Gmelin (1790)
It is pos sible
that some of the unidentified specimens in this study are T.
m u s t e l a e , but no hooks were rec ov ered that m a t c h e d those
d es cr ib ed for the species.
from Ontario (Freeman,
Dick, 1983).
Lockard,
T. m ustelae has been reported
19 5 6 ) and from M a n i t o b a
It has also been r epo rt ed in m i n k (Barber and
1973) and in sh ort -ta il ed weasels
from Montana.
(Poole and
(Locker,
1955)
T a en iid t a p e w o r m s we r e the mo s t c o m m o n l y
found helminth in marten in the present study.
27
I
Figure
IX.
.4mm
t
I
Hooks of Taenia m artis from A l ask an marten.
Magnification 100 X.
28
I
.4 mm
Figure X. M a tu re proglot tid of Taenia m artis from Alaskan
marten. Magnification 100 X.
29
U
-Li
Figure XI.
Taenia martis from Alaskan marten.
T, testes;
G,
genital atrium;
0, ovary;
V, vitellarium;
U, uterus;
R, rostellum;
S, suckers; Y, yolk
gland.
The single as carid s p e c i m e n reco vered fr om the small
intestine of one marten in this study may be Baylisascaris
devosi
whe n
Sprent 1952.
collected.
(Poole
and
B.
The s p e c i m e n was in poor condition
devosi
D i c k f 1983)
has
and
been
rep or te d
in fisher
1979) fr om M a ni tob a and in w o l v e r i n e
Territories
(Addison and Boles,
in
marten
(Dick and Leonard
from the N o r t h w e s t
1978).
The u n i d e nt ifi ed i n t r a m u s c u l a r n e m a t o d e s whi c h we re
found in 24.1% of the m a r t e n e x a m i n e d in this study m a y be
third
stage
larvae
of
Bayl isa scari s
devosi.
S p r e n t 's
e x p e r i m e n t s w i t h w h i t e mi c e and his des cr ipt io ns of third
stage
larvae
closely
fit
th e
observations
of
the
u n i d e n t i f i e d tissue ne ma t o d e s found in the p r ese nt study.
Sprent
(1953) reported experiments
with
third
stored at -20 degrees C for several weeks.
m o t i l i t y after thawing.
Several
stage
larvae
He noted active
larvae rec ov ered
in the
present study were vigorously motile after being stored at
minus
15
degrees
C
for
29
months .
No
positive
identification was made because of the immaturity of these
nematodes
( Figure II).
The absence of lungworms in this study is of interest.
Perostrongylus
pridhami
(Barber and Lockard,
was
reported
in mink
from
Montana
1973) and Crenosoma coloradoensis was
reported in marten from Colorado (Craig and Anderson,
Olsen,
1952).
1972;
It is possible that one or more intermediate
hosts for these nematodes are not present in the study area.
31
The nasal n e m a t o d e s S kr j a b i n g y Ius c h i t w o o d o r u m Hill, 19 39
and
S.
nas ico la
L e u c k a r t , 1842
have
been
found
mustelids from North America (Lankester, 1983).
in
many
It is not
kn o w n w h y these n e m a t o d e s appear to be absent in the study
area.
There
was
no
indication
of
parasitism
by
any nasal parasites.
Dracu nc ul us
sp., the guinea worm,
w h i c h is a c o m m o n
parasit e of raccoon, mink, and otter in On tario (Crichton
and S e v e r I y - B u r t o n , 1974), was not found in m a r t e n during
this
study.
Surveys
of
local
ponds
in
the
study
area
revealed an abundance of a potential intermediate host; the
crusta cean
Cyclops
sp.
It
is
possible
that
lack
of
a
paratenic host may explain the absence of this nematode in
northern
regions.
The intensity of infections for all parasite species in
this study are similar to the frequency distibution of many
other helminth infections in both free ranging and domestic
animal populations. Most positive animals had low intensity
infections,
counts.
wi t h only a few a n ima ls having high parasite
This approximates
a negative binomial
described by Froyd and Clarke (1962)
equation as
(Figure XII).
The food habit data in this report are limited.
trappers
frequently.
check
their
traplines
once
a
week
Many of the marten gastrointestinal
this study were empty upon examination.
or
Man y
less
tracts
in
Marten digest their
food after being caught and are unable to feed again.
Gray
32
Taenia sp.
Molineus patens
Number of Parasites per Host
Alaria mustelae
Number of Marten with Indicated Number of
Parasites.
Figure
XII.
Frequency distribution of helminths from 141
Alaskan marten.
33
j a y s , or "camp robbers",' P eriosor eus c a n a d e n s i s , often get
caught in marten traps and are left for bait when the traps
are reset.-
This is probably why gray jays were found in 11
of the 36 marten that contained identifiable animal material
in their stomachs.
The food habit data from this report
suggest that Clethrionomys rutilus is the preferred item in
the marten's diet.
Red squirrels and s now sh oe hare wer e
also abundant in the study area, but seem to be taken less
frequently.
The
C l e t h r i o n o m ys
high
rut i Ius
frequency
as
a
food
of
red-backed
item
of
marten
vol es ,
is
of
interest as a probable explanation for the high prevalence
of Taenia sp. found in m a r t e n during this study.
Raus ch
(1952) found many Taenia cysticerci in red-backed voles from
Alaska.
Prokopic
cysticer ci
in
1205
(1970)
voles
reco vered
examined
nine
from
Tae nia
Czechoslovakia.
Adult cestodes developed when these cysticerci were
short-tailed weasels, Mustela erminea.
m artis
fed to
34
SUMMARY
One hundred and forty one marten,
collected
Martes americana were
in the Yukon Flats and Fairbanks areas of Alaska.
This r ese arc h was the first s y s t e m a t i c survey on internal
parasites ',of marten from Alaska. Carcasses were examined for
the
prese nce
tract,
of ,helminth
fauna
other internal organs,
in the
gas tro in tes ti nal
and skeletal muscle.
The stomach nematode Soboliphyme baturini Petrov,
1930
was found in one marten. M olineus patens (Dujardin, 1845)
was
identified
specimens.
in
the
small
intestine
of
7
This is the first report of this
.8 % of the
nem a t o d e
in
marten. The following helminths were also recovered from the
small
intestine:
Taenia
m artis
Ala ri a
m ust el ae
(Z e d e r , 1803),
unidentified ascaroid nematode,
Muscle
Bosma,
(3.6%);
1931,
Taenia
sp.,
(11.1%);
(38.2%);
(0 .7 %).
digest revealed Trichinella spiralis Railliet,
1895 in 12.7% of the marten. An u ni de nti fi ed i n t r a m u s c u l a r
nematode
was
also pres ent
in 24.1% of the digests.
Trichinella larvae
were observed from six carcasses frozen
at -15
for
degrees
C
3
to
16
months. Five
I Swiss Webster mice became infected after
I
Live
oral
of
twelve
inoculation
with the recovered T. spiralis larvae.
Marten pelts are an important source of income for many
people in the survey area. Carcasses are sometimes consumed
/
35
as
a dietary
supplement.
This
practice
increases
the
possibility of infection with T. spiralis since 12.7% of the
marten surveyed were positive for this nematode.
of
local people could prevent possible
Trichenellosis.
Education
future outbrakes
of
36
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