Studies on the helminth fauna of Alaska. XVI. A survey of the helminth parasites of Ptarmigan (Lagopus spp.)


Babero, B.B.

Journal of Parasitology 39(5): 538-546

1953


Of 292 Alaskan ptarmigan, Lagopus spp., examined, 37% were found to be infected with helminths, viz., five species of nematodes, two species of trematodes and four species of cestodes. Trichostrongylus tenuis from the North American ptarmigan, Leucochloridium variae, Brachylaima fuscata, Aploparaksis galli and Davainea proglottina from the willow ptarmigan and Rhabdometra nullicollis from the rock ptarmigan are recorded for the first time.

STUDIES
ON
THE
HELMINTH
FAUNA
OF
ALASKA.
XVI.
A
SURVEY
OF
THE
HELMINTH
PARASITES
OF
PTARMIGAN
(LAGOPUS
SPP.)
BERT
B.
BABERO
1
References
concerning
the
diseases
and
parasites
of
ptarmigan
are
widely
dis-
persed
in
the
literature,
and
for
the
most
part
are
not
readily
accessible.
It
is
the
purpose
of
this
paper
to
report
the
helminth
parasites
obtained
from
191
willow
ptarmigan,
Lagopus
lagopus
Linn.
;
45
rock
ptarmigan,
L.
mutus
(Mont.)
;
and
56
white-tailed
ptarmigan,
L.
leucurus
(Rich.)
.
These
birds
were
collected
over
a
period
of
four
years,
and
were
taken
from
widely
separated
areas
in
Alaska.
(Fig.
1.)
MATERIAL
AND
METHODS
Although
most
of
the
birds
were
examined
while
fresh,
the
viscera
of
some
specimens
were
preserved
in
10%
forrnalin
solution
in
order
that
they
might
be
shipped
from
the
field
to
the
laboratory.
Near
the
end
of
this
survey,
blood
films
also
were
prepared
from
42
birds
(willow
ptarmigan).
These
were
stained
with
Wright's
blood
stain
and
examined
for
filariid
larvae.
All
helminths
other
than
microfilariae
were
fixed
in
alcohol-formalin-acetic
acid
solution
(AFA).
The
two
stains
employed
for
cestodes
and
trematodes
were
Semichon's
acid
carmine
and
aqueous
alum
cochineal.
Lacto-phenol
was
the
clearing
agent
used
for
nematodes.
THE
HELMINTH
PARASITES
One
hundred
and
nine
ptarmigan,
approximately
37
per
cent
of
the
total
number
examined,
were
infected
with
helminth
parasites
;
these
comprised
five
species
of
nematodes,
two
of
trematodes
and
four
of
cestodes.
The
results
of
these
findings
are
summarized
in
Table
1.
TABLE
1.—Summary
of
helminth
parasites
obtained
from
292
Alaskan
ptarmigan
(Lagopus
spp.),
1949-1953
Helminth*
Species
:
No.
of
each
No.
infected
of
total
Per
cent
infected
of
total
Rock
45
Willow
White-tailed
191
56
No.
infected
Nematoda
:
A.
compar
5
11
10
26
8.9
T.
tenuis
6
6
2.1
Capillaria
sp.
1
1
0.3
Trichostrongyle
(unid.)
1
1
0.3
Trematoda
:
L.
variae
1
4
3
8
2.7
B.
fuscata
11
16
6
33
11.3
Cestoda
:
R.
urogalli
2
4
3
9
3.1
D.
proglottina
8
3
5
16
5.5
H.
galli
6
2
8
2.7
R.
nullicollis
1
1
0.3
*
Does
not
include
M.
lagopodis
(see
text).
Received
for
publication,
January
29,
1953.
1
Parasitologist,
Animal-borne
Disease
Branch,
Arctic
Health
Research
Center,
Public
Health
Service,
Department
of
Health,
Education,
and
Welfare,
Anchorage,
Alaska.
538
BABERO—ALASKAN
HELMINTHS
539
NEMATODA
Ascaridia
com
par
(Schrank,
1790)
Huus
(1928)
and
Brinkman
(1922)
reported
A.
com
par
as
a
common
parasite
of
the
willow
ptarmigan
in
Norway
(the
latter
reporting
it
under
the
name
of
Heterakis
magnipapilla
v.
Linstow,
1906).
The
nematode
has
been
observed
fre-
quently
in
Alaskan
ptarmigan
(small
intestine),
and
has
been
obtained
from
birds
BARROW
0
ARCTIC
VILLAIE
IP0
(\\
ct,B
4
,1213
0
,
6
1,
FAIRBANKS
co,7!;
a
y.
p
O
COLD
BAY
O
FIG.
1.
Localities
from
which
ptarmigan
have
been
examined.
Solid
symbols
represent
wil-
low
ptarmigan
;
hollow
symbols
represent
rock
ptarmigan
;
symbols
with
dot
represent
white-
tailed
ptarmigan.
collected
over
much
of
the
Territory.
Infections
ranged
from
1
to
16
worms
per
host.
Through
the
courtesy
of
Mr.
Munthe-Kaas
Lund,
Bergen
Museum,
Oslo,
Nor-
way,
specimens
of
A.
cornpar
from
the
Norwegian
willow
ptarmigan
were
made
0
KOT
540
THE
JOURNAL
OF
PARASITOLOGY
available
for
comparison
with
the
Alaskan
worms.
They
differed
essentially
in
the
number
of
post-anal
papillae
on
male
specimens,
the
Alaskan
form
having
six
pairs
of
papillae
rather
than
five
as
has
been
found
in
the
Norwegian
worm.
This
difference
is
not
considered
sufficient
to
justify
separation
of
the
two
series
of
nema-
todes
into
two
different
species.
Trichostrongylus
tenuis
(Mehlis,
1846)
T.
tenuis
was
reported
by
Shipley
(1909a)
as
occurring
in
the
English
red
grouse,
Lagopus
scoticus
Lath.
It
has
also
been
reported
from
domestic
fowl.
Cram
and
Wehr
(1934)
cited
records
of
its
distribution
in
Europe,
Asia,
Africa
and
North
America.
T.
tenuis
has
been
obtained
in
Alaska
from
the
ceca
of
willow
ptarmigan,
only.
The
birds
were
collected
from
Cold
Bay
on
the
Alaska
Peninsula,
and
from
the
Talkeetna
Mountains,
near
Anchorage.
The
present
report
constitutes
the
first
record
of
the
species
from
North
American
ptarmigan.
Capillaria
sp.
A
single
specimen
of
a
female
capillarid
was
recovered
from
the
proventriculus
of
a
rock
ptarmigan,
collected
40
miles
north
of
Fairbanks.
Shipley
(1909a,
1909b)
and
Brinkman
(1922)
reported
the
occurrence
of
Trichosoma
longicolle
(Mehlis,
1831)
in
the
intestine
of
the
red
grouse
and
ptarmigan
(L.
scoticus;
L.
mutus),
respectively.
Read
(1949),
in
his
review
of
the
capillarids
of
North
American
birds,
pointed
out
that
T.
longicolle
is
a
synonym
of
C.
caudinflata
(Molin,
1858).
Em-
ploying
Read's
key
to
the
species
of
Capillaria
in
birds,
the
specimen
from
rock
ptarmigan
could
be
designated
C.
caudinflata.
However,
from
the
material
on
hand
it
is
impossible
to
establish
a
definite
identification.
C.
contorta
(Creplin,
1839),
a
species
not
considered
in
Read's
key,
was
re-
ported
as
occurring
in
the
crops
of
pinnated
grouse,
Tympanuchus
cupido
(Linn),
and
the
sharp-tailed
grouse,
Pedioecetes
phasianellus
(Linn),
by
Morgan
and
Hamerstrom
(1941).
Unidentified
Trichostrongyle
Several
trichostrongyle
nematodes
were
recovered
from
the
small
intestine
of
a
rock
ptarmigan
collected
at
Adak,
in
the
Aleutian
Islands.
These
specimens
were
turned
over
to
Mr.
Merle
Kuns,
Purdue
University,
for
identification.
Because
of
his
being
called
into
the
armed
forces,
study
of
this
material
has
not
been
com-
pleted.
In
a
communication
received
from
Mr.
Kuns,
he
suggested
the
probability
that
these
specimens
may
belong
to
an
undescribed
genus.
It
is
hoped
that
the
identification
of
these
worms
can
be
given
in
a
later
publication.
Microfilaria
lagopodis
(
Sarnbon,
1907)
Although
no
attempt
was
made
to
search
for
blood
parasites
of
ptarmigan
until
this
survey
was
nearly
completed,
nineteen
of
forty-two
willow
ptarmigan
examined
were
positive
for
filariid
larvae.
2
From
Anaktuvuk
Pass
(North-Central
Alaska),
eleven
of
twenty-five
birds
examined
were
positive
for
these
larvae,
and
from
the
Arctic
Village
region
(lat.
68°8'
N.,
145°32'
W.),
eight
of
seventeen
birds
were
2
Six
of
the
forty-two
ptarmigan
from
which
blood
smears
were
made
harbored
trypano-
somes,
probably
Trypanosorna
lagopodis
Haaland,
1928.
BABERO—ALASKAN
HELMINTHS
541
positive.
Infections
ranged
from
one
to
seventeen
worms
per
low-power
field
(100x).
Filaria
smithi,
a
blood
nematode
from
the
red
grouse,
was
originally
described
by
Sambon
(1907,
as
cited
by
Haaland,
1928).
Although
she
considered
the
orig-
inal
description
inadequate,
Haaland
(1928)
was
of
the
opinion
that
blood
nema-
nematodes
which
she
obtained
from
Norwegian
willow
ptarmigan
were
probably
the
same
as
those
described
by
Sambon.
She
pointed
out,
however,
that
the
spe-
cific
name
used
by
Sambon
was
preoccupied
by
Cobbold's
species
from
the
elephant
and
proposed
the
name
F.
lagopodis
for
these
microfilariae.
Haaland
also
pre-
sented
a
more
detailed
description
of
this
species
based
on
her
material
from
willow
ptarmigan.
Brinkman
(1949)
considered
microfilariae
which
he
also
obtained
from
willow
ptarmigan
to
be
the
same
as
those
of
Haaland.
He
was
of
the
opinion
that
the
generic
name,
Filaria
Mueller,
1787,
could
only
be
used
for
the
adult
worm.
Since
only
the
microfilaria
was
known
in
this
case,
he
proposed
that
the
name
be
changed
to
Micro
filaria
lagopodis.
In
general,
the
morphology
of
the
blood
nematodes
from
Alaskan
ptarmigan
agrees
with
the
description
given
by
Brinkman
of
specimens
which
he
believed
to
be
the
same
as
those
of
Haaland.
However,
there
seems
to
be
some
question
re-
garding
the
presence
or
absence
of
a
red-staining
central
body.
Brinkman,
in
com-
paring
Haaland's
description
of
her
specimens
with
that
of
Sambon,
stated,
"Sam-
bon's
specimens
seemed
to
be
smaller,
and
he
had
not
mentioned
the
characteristic
red-stained
zone
(central
body)
which
seemed
to
be
so
prominent
in
Haaland's
specimens.
We
should
not,
however,
pay
too
much
attention
to
these
differences,
as
length
is
a
matter
of
the
microfilaria's
state
of
development,
and
the
figure
given
by
Sambon
(1907)
is
certainly
of
a
very
young
larva.
The
red
central
body
is
far
from
constant
in
my
specimens,
which
are
certainly
identical
with
the
Haaland
spe-
cies.
In
my
opinion
one
can
with
almost
certainty
assume
Sambon's
and
Haaland's
specimens
to
be
identical."
The
writer
observed
that
when
"old"
blood
was
used
for
films
the
worms
often
would
not
stain
completely,
and
in
some
instances
not
at
all.
This
might
be
another
reason
why
the
red-stained
zone
was
not
reported
in
Sambon's
description.
Filaria
sp.
has
been
recovered
from
the
subcutaneous
tissue
over
the
pectoral
muscles
of
seven
Alaskan
spruce
grouse,
Canachites
canadensis
(Linn.).
The
sev-
eral
blood
films
examined
from
this
host
species
were
negative.
The
helminth
para-
sites
of
Alaskan
grouse
will
be
reported
in
a
separate
publication
and
it
is
anticipated
that
a
more
complete
identification
of
this
adult
nematode
can
be
given
at
that
time.
TREMATODA
Leucochloridium
variae
McIntosh,
1932
(Fig.
1)
Among
a
series
of
trematodes
of
the
genus
Leucochloridium
Carus,
1835,
de-
scribed
by
McIntosh
(1932)
were
L.
pricei,
from
an
Alaskan
spruce
grouse
[Cana-
chites
canadensis
(Linn.)
]
and
L.
variae
from
a
Michigan
warbler
[Mniotilta
varia
(Linn.)
].
Kagan
(1952)
in
his
revision
of
LEUCOCHLORIDIINAE,
synonymized
L.
pricei
with
L.
variae,
since
his
studies
revealed
that
the
characters
upon
which
McIntosh
based
the
differentiation
were
subject
to
considerable
variation.
This
542
THE
JOURNAL
OF
PARASITOLOGY
species
was
also
reported
by
Mueller
(1941)
from
a
gallinaceous
bird
[Bonasa
um-
bellus
(Linn.)
]
collected
in
New
Hampshire.
Specimens
of
L.
variae
were
recovered
from
members
of
each
species
of
Alaskan
ptarmigan
(Table
1),
and
the
number
of
parasites
ranged
from
1
to
214
per
bird.
Morphologically,
these
trematodes
agree
with
the
original
description.
The
present
report
constitutes
new
host
records
for
L.
variae.
As
pointed
out
by
McIntosh
(1932),
since
grouse
[and
ptarmigan]
are
non-
migratory
birds,
the
immature
stages
of
this
trematode
probably
occur
in
a
snail
of
the
immediate
habitat.
Although
terrestrial
gastropods
in
Alaska
are
limited
as
to
species
and
abundance,
they
are
widely
distributed.
A
locally
collected
spruce
grouse
which
harbored
L.
variae
also
had
several
snails
[Euconulus
fulvous
alas-
kensis
(Pilsby.)
]
in
its
ventriculus.
Stagnicola
yukonensis
Baker
and
Succinea
strigeata
Pfeiffer
(identified
by
Dr.
Harald
Rehder,
U.
S.
National
Museum)
were
collected
at
Circle,
Alaska.
Kagan
(1951),
in
his
historical
review,
included
sev-
eral
records
of
snails
of
the
genus
Succinea
reported
as
harboring
sporocysts
of
Leucochloridium.
Brachylaima
fuscata
(Rud.
1819)
(Fig.
2)
This
trematode
has
been
observed
more
frequently
in
Alaskan
ptarmigan
than
has
any
other
helminth
parasite.
Infections
ranged
from
1
to
265
specimens
per
bird.
B.
fuscata
(=
Brachylaemus
fuscatus)
has
been
found
to
be
of
wide
distribu-
tion
in
Alaska,
having
been
collected
from
various
points
within
an
area
bounded
on
the
north
by
Anaktuvuk
Pass,
on
the
west
by
Kotzebue,
and
on
the
south
by
the
Anchorage
area.
B.
fuscata
has
been
recorded
previously
from
Bonasa
umbellus
Linn.
and
Centro-
cercus
urophasianus
(Bonaparte).
Besides
recovering
this
trematode
from
the
three
species
of
ptarmigan
in
Alaska,
the
writer
has
also
collected
it
from
the
ruffed
grouse,
B.
umbellus;
the
sharp-tailed
grouse,
P.
phasianellus
and
spruce
grouse,
C.
canadensis.
CESTODA
Haploparaxis
galli
Rausch,
1951
The
original
description
of
H.
galli
from
the
rock
ptarmigan
constitutes
the
first
record
of
this
genus
from
gallinaceous
birds,
insofar
as
the
writer
is
aware.
In
the
present
study,
this
species
has
been
collected
six
times
from
the
rock
ptarmigan
and
twice
from
the
willow
ptarmigan.
Infections
have
consisted
of
one
to
four
worms
per
bird.
The
localities
from
which
this
parasite
was
collected
were
Tulugak
Lake
(Brooks
Range),
Fairbanks,
Nome
and
Kotzebue.
Davainea
proglottina
(Davaine,
1860)
(Fig.
3)
D.
proglottina
has
been
observed
to
be
one
of
the
more
common
parasites
of
Alaskan
ptarmigan.
This
cestode
was
recovered
from
birds
of
three
general
locali-
ties
as
follows
:
Tulugak
Lake,
Fairbanks,
and
the
Kenai
Peninsula
(near
Hope).
The
specimens
from
Alaskan
ptarmigan
resemble
D.
tetroensis
Fuhrmann,
1919,
but
that
species
differs
in
having
a
double
row
of
rostellar
hooks
and
a
larger
number
of
testes
(about
thirty).
Segment
number
is
not
always
a
reliable
charac-
BABERO—ALASKAN
HELMINTHS
543
ter
in
distinguishing
the
two
forms.
Although
D.
proglottina
has
been
reported
from
related
birds,
such
as
grouse
and
partridge,
there
appears
to
have
been
no
previous
record
of
its
occurrence
in
ptarmigan.
Raillietina
urogalli
(Modeer,
1790)
This
cestode
is
known
to
occur
commonly
in
the
small
intestine
of
the
willow
ptarmigan
and
the
red
grouse.
In
Alaska,
R.
urogalli
has
been
recovered
nine
times,
with
infections
ranging
from
one
to
four
worms
per
bird.
The
rock
and
white-tailed
ptarmigan
constitute
new
host
records
for
the
species.
The
localities
in
which
the
infected
birds
were
collected
are
Anaktuvuk
Pass,
Anchorage,
and
Talkeetna
Mountains
(90
miles
north
of
Anchorage),
and
Lake
Schrader
(Ro-
manzof
Mountains
of
northeastern
Alaska).
Rhabdometra
nullicollis
Ransom,
1909
(Figs.
1
6)
A
cestode
belonging
to
the
genus
Rhabdometra
Cholodkovsky,
1906,
was
re-
covered
from
the
small
intestine
of
a
rock
ptarmigan,
collected
during
the
summer
of
1951
at
Lake
Schrader.
A
review
of
literature
revealed
that
several
species
of
this
genus
have
been
reported
from
gallinaceous
birds
:
R.
nigropunctata
(Crety,
1890)
was
reported
from
a
Siberian
partridge,
Perdix
perdix
(Linn.)
;
R.
odiosa
(Leidy,
1887)
was
reported
from
the
sharp-tailed
grouse
in
North
America
;
R.
nullicollis
Ransom,
1909,
also
from
North
America,
has
been
reported
from
the
pinnated,
sharp-tailed,
and
sage
grouse
;
R.
tomica
Cholodkovsky,
1906,
was
de-
scribed
from
the
black
grouse,
and
again
later
reported
from
the
willow
ptarmigan
in
Russia
;
and
R.
cylindrica
Beddard,
1914,
was
reported
from
North
African
grouse.
Except
for
a
minor
difference,
testes
number,
the
specimens
from
the
rock
ptarmigan
fit
the
description
of
R.
nullicollis
as
given
by
Boughton
(1937).
The
vaginal
bulb
situated
close
to
the
genital
sinus,
present
in
R.
nullicollis,
was
not
observed
with
certainty
in
the
proglottids
of
the
Alaskan
material
studied.
The
occurrence
of
this
cestode
in
rock
ptarmigan
constitutes
a
new
host
record.
DISCUSSION
For
the
most
part,
the
helminth
parasites
of
ptarmigan
appear
to
be
widely
distributed
geographically
and
are
not
limited
to
a
given
ptarmigan
species.
Van
Cleave
and
Rausch
(1951),
in
their
study
of
the
parasites
of
eider
ducks,
pointed
out
that
when
suitable
intermediate
hosts
are
present
under
ecologically
similar
conditions,
the
local
bird
populations
are,
through
food
habits,
exposed
to
infection
by
identical
species
of
parasites.
The
findings
of
the
present
study
seem
to
support
this
statement.
Few
species
of
trematodes
parasitize
ptarmigan.
Prosthogonimus
ovatus
(Rud.,
1803),
reported
from
Lyrurus
tetrix
(Linn.)
by
Fediushin
(1949),
is
the
only
species
recorded
prior
to
this
study
insofar
as
the
writer
has
been
able
to
determine.
This
may
be
attributable
to
the
arctic
and
subarctic
conditions
under
which
these
birds
live,
and
the
restricted
geographical
distribution
of
suitable
snail
intermediate
hosts
in
such
regions.
On
the
other
hand,
species
of
nematodes
have
been
frequently
reported
from
ptarmigan.
A.
compar,
for
instance,
is
apparently
geographically
unrestricted
in
its
range.
R.
urogalli,
likewise,
is
of
wide
occurrence.
544
THE
JOURNAL
OF
PARASITOLOGY
Although
in
the
present
study,
no
recognized
pathological
effects
could
be
attributed
directly
to
helminth
parasitism,
several
of
the
worms
recovered
from
Alaskan
ptarmigan
have
been
previously
incriminated
as
causes
of
"die-offs"
among
certain
game
birds.
Perhaps
the
most
significant
of
these
is
the
cecal
nematode
T.
tennis
and
the
cestode
R.
urogalli.
The
etiological
significance
of
these
parasites
in
the
health
of
the
English
red
grouse
has
been
reported
in
detail
by
Shipley
(1909a,
1909b)
and
Leslie
and
Shipley
(1911-12).
The
part
that
helminthiasis
may
play
in
the
reduction
of
ptarmigan
numbers
in
Alaska
is
un-
determined.
The
study
of
the
helminth
parasites
of
these
hosts,
particularly
as
they
effect
young
birds,
should
be
emphasized
in
relation
to
general
faunal
in-
vestigations
in
the
Territory.
Acknowledgment
The
writer
is
especially
grateful
to
Dr.
Robert
Rausch
and
Mr.
Everett
L.
Schiller,
of
this
laboratory,
for
their
identification
of
all
cestode-material
and
as-
sistance
rendered
throughout
this
study.
SUM
MARY
A
summary
of
the
helminth
parasites
of
Alaskan
ptarmigan
(genus
:
Lagopus)
is
presented.
Of
292
ptarmigan
examined,
109
were
found
to
be
infected
with
one
or
more
of
eleven
species
of
worms.
From
the
willow
ptarmigan,
two
trematodes,
L.
variae
and
B.
fuscata,
and
two
cestodes,
H.
galli
and
D.
proglottina,
are
reported
for
the
first
time.
The
rock
ptarmigan
constitutes
a
new
host
record
for
the
cestode
species
R.
urogalli,
D.
proglottina,
and
R.
nullicollis.
An
unidentified
trichostrongyle
(possibly
belonging
to
a
new
genus)
and
the
trematodes
L.
variae
and
B.
fuscata
are
also
reported
from
this
host
for
the
first
time.
Apparently,
the
helminth
parasites
reported
herein
from
the
white-tailed
ptarmigan
are
the
first
published
records
from
this
host.
REFERENCE
S
BOUGHTON,
R.
V.
1937
Endoparasitic
infestations
in
grouse,
their
pathogenicity
and
correla-
tion
with
meteoro-topographical
conditions.
U.
Minn.
Agr.
Exp.
Sta.
Tech.
Bull.
121:
50
p.
BRINKMAN,
A.
1922
Lirypens
Entoparasiter.
Bergens
Mus.
Arbok,
Nat.
vid.
rekke
nr.
3:
3-41.
BRINKMAN,
A.,
JR.
1949
On
the
morphology
of
Micro
filaria
lagopodis
(Haaland,
1928).
U.
Bergen
Arbok,
Nat.
vid.
rekke
nr.
4:
1-13.
CRAM,
ELOISE
B.
AND
WEHR,
E.
E
1934
The
status
of
species
of
Trichostrongylus
of
birds.
Parasitology
26:
335-339.
FEDIUSHIN,
A.
V.
1949
Helminths
and
helminthiasis
of
grouse
and
phasianic
birds
of
Western
Siberia
and
the
Southern
Urates.
(Russian
text.)
Biul.
Moskov.
Obsh.
Ispyt.
Prir.
Otdel.
Bil.
v.
120
n.
s.
54:
22-29.
HAALAND,
MARGIT
1928
Elodparasitter
hos
lirypen
(Lagopus
lagopus).
Bergens
Jaeger-og
Fiskerforenings
Rypeundersiikelse
Meddel.
nr.
23:
3-25.
Huus,
J.
1928
Darmparasiten
des
norwegischen
Moorschneehuhns
(Lagopus
lagopus
L.).
Nematoden
and
Cestoden.
Bergens
Mus.
Arbok,
Nat.
vid.
rekke
nr.
3:
3-49.
KAGAN,
I.
G.
1951
Aspects
in
the
life
history
of
Neoleucochloridium
problematicum
(Magath,
1920)
new
comb.
and
Leucochloridium
cyanocittae
McIntosh,
1932
(Trematoda
:
Brachylaemidae).
Trans.
Amer.
Micro.
Soc.
70:
281-318.
1952
Revision
of
the
subfamily
Leucochloridiinae
Poche,
1907.
(Trematoda
:
Brachylaemidae).
Amer.
Mid.
Nat.
48:
257-301.
LESLIE,
A.
S.
AND
SHIPLEY,
A.
E.
1911-12
The
grouse
in
health
and
disease
being
the
final
report
of
the
Committee
of
Inquiry
on
Grouse
Disease.
2.
London.
BABERO—ALASKAN
HELMINTHS
545
MCINTOSH,
A.
1932
Some
new
species
of
trematode
worms
of
the
genus
Leucochloridium
Carus,
parasitic
in
birds
from
Northern
Michigan,
with
a
key
and
notes
on
other
species
of
the
genus.
J.
Parasit.
19:
32-53.
MORGAN,
B.
B.
AND
HAMERSTROM,
F.
N.,
JR.
1941
Notes
on
the
endoparasites
of
Wisconsin
pinnated
and
sharp-tailed
grouse.
J.
Wildl.
Mgt.
5:
194-198.
MUELLER,
J.
F.
1941
Some
parasites
newly
recorded
for
the
ruffed
grouse,
Bonasa
umbellus,
in
the
United
States.
Proc.
Helm.
Soc.
Wash.
8:
14-15.
RAUSCH,
R.
1951
Studien
an
der
Helminthenfauna
von
Alaska.
IV.
Haploparaxis
galli
n.
sp.,
ein
Cestode
aus
dem
Schneehuhn,
Lagopus
rupestris
(Gmelin).
Zeit.
Par-
asitenk.
15:
1-3.
READ,
C.
P.
1949
Studies
on
North
American
helminths
of
the
genus
Capillaria
Zeder,
1800
(Nematoda)
:
III.
Capillarids
from
the
lower
digestive
tract
of
North
American
birds.
J.
Parasit.
35:
240-249.
SHIPLEY,
A.
E.
1909a
The
threadworms
(Nematoda)
of
the
red
grouse
(LagoPus
scoticus).
Proc.
Zool.
Soc.
London.
pp.
335-350.
1909b
Internal
parasites
of
birds
allied
to
the
grouse.
Proc.
Zool.
Soc.
London.
pp.
363-368.
VAN
CLEAVE,
H.
J.
AND
RAUSCH,
R.
1951
The
acanthocephalan
parasites
of
eider
ducks.
Proc.
Helm.
Soc.
Wash.
18:
81-84.
PLATE
I
FIG.
1.
L.
variae,
ventral
view.
FIG.
2.
B.
fuscata,
ventral
view.
FIG.
3.
D.
proglottina.
FIG.
4.
R.
nullicollis,
scolex.
FIG.
5.
R.
nullicollis,
mature
proglottid.
FIG.
6.
R.
nullicollis,
gravid
proglottid.
546
THE
JOURNAL
OF
PARASITOLOGY
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