The study area encompassed. 350km2 of gla- cial valley near. KJuane. Lake in the ..... loon. (Gava immer). Females of S. euryadmninicubum were evi- dently ..... animal health,. 7th. ed. MacMillan. Publishing. Co.,. New. York, pp. 148-149.
Journal
MORTALITY FLY
HEMATOPHAGA
D. Bruce 2
IN FLEDGLING
Hunter,1
Department Department
Centre Canada
AND
C. Rohner,2
of Pathology, of Zoology,
for Biodiversity M5S 2C6
Ontario University and
GREAT
HORNED
Diseases, © Wildlife
OWLS
33(3), Disease
FROM
pp 486-491 Association 1997
1997,
BLACK
LEUCOCYTOZOONOSIS
and
D. C. Currle3
Veterinary of British
Conservation
of %Vildlffe
College, Columbia,
Biology,
University Vancouver,
Royal
of Guelph, Guelph, British Columbia,
Ontario
Museum,
Ontario, Canada
Queen’s
100
Canada N1G V6T 1Z4
Park.
Toronto,
2W1
Ontario,
Black fly feeding alone and in concert with Leucocytozoon spp. infection caused in fledgling great horned owls (Bubo virginianus) in the Yukon, Canada 1990 to 1991. These mortalities occurred during a year of food shortage corresponding with a decline in the population of snowshoe hare (Le’pus americanus), the main prey for great horned owls. We hypothesize an interaction between food availability and the consequences of host-parasite interABSTRACT:
mortality
actions. Key
Bubo
words:
virginianus,
anemia,
host-parasite
INTRODUCTION
Rohner response
( 1994) of great
ginianus) americanus) the boreal Canada.
to
cycle
of
well
documented
to
snowshoe
Alaska 8 to
(USA)
11 year
in
flies
Yukon,
gists
hare
in
follow
a
black lished
cycle
(Krebs
cycle
with 1995).
(Rohner,
a time Snowshoe
lag
flies but reports
chicks oming
snowshoe
and of
hare
population
Hunter, nest
sites
dividuals
with dead
tions, were
carcasses during
tense
black
of 1989
of causes
nithophilic
with
the
of death
driving
black
bacterial interesting to feeding
flies
(Diptera:
and
troduced
site
Cain
bioloby
(pers.
pubor
comm.)
in
red-tailed
hawk
he
in northern attributed
to
causing chicks
parasite
Wy-
in-
anemia
and
their
nests
from
Leucocytozoon
of in-
(USA)
(Bra
nta Refuge
birds
ly associated tality. There
with
cytozoon spp. from raptorial documentation In this findings horned
al.,
1993)
spp.
et
but,
al.,
1975),
the
Canada the Seney Michigan infection spp.
clinical disease many reports
of
is rare-
of
or morLeuco-
being found in blood smears birds (Peirce, 1981) but of pathogenicity
paper
in-
para-
with
at
Leucocytozoon
with are
been the
in juvenile
canadensL) in northern
(Herman
infecfindings by or-
486
for
et
carcass-
Simuli-
have
enzootic
of epizootics
wild
idae) and in several birds concurrent infections with the blood parasite Leucocytozoon spp. (Rohner and Hunter, 1996). The prevalence of parasitism and preda-
which
areas
(Bennett
geese Wildlife
us
chickens
into
exception
owls found observed a
in these
and
most attributed
the
provided
black
Raptor tormented
can be a serious pathogen in immunologically naive captive or domestic waterfowl,
(Rohner
tracking
39 juvenile to 1991. We
trauma
of
S.
fly feeding
occasionally
monitoring
radio-telemetry
including
but lesions
decline
Extensive
combined by
variety
es,
1996).
year
as and
were unable to find clinical consequences
mortality
turkeys,
first
we of
(ButeojamaicensLs) (USA) which
decreased
the
increased (Rohner
of ornithophilic
mortality.
sities in the study area peaked in 1989 to 1990 and began to decline in 1991 (Rohner, 1996). The survival of juvenile owls was very high during 1989 and 1990 but 1991,
mortality
decreased
is poorly documented. often observe nestlings
prematurely. The blood
in
platforms.
1996).
observed
of 1 to 2 hare den-
of
pathogenicity
nestling
Predators such as the great which use the snowshoe hare food source, follow a similar
population
causes
The
1993
tethering
densities
Hunter,
(Lepus
southwestern of
and
et al., 1992). horned owl as a primary years
1988
as
hare
numerical (Bubo vir-
hare
from
forest
Canada
the owls
snowshoe
Populations
boreal
tion
evaluated horned
the
interactions,
we
from 28 owl carcasses
describes of
is lacking. the
necropsy
the juvenile obtained during
great the
HUNTER
great
horned
(Rohner the role
owL/snowshoe
and Hunter, of ornithophilic
Leucocytozoon
spp.
juvenile
owls
fledging
period.
The
MATERIALS
AND
area
valley
em
Yukon, Canada owl nests
and black
in causing the
cial
hare
1996)
during
study
ET AL-PARASITE
study
discusses flies and
mortality
fledging
and
in post-
METHODS
encompassed Lake
350km2
of gla-
Between banded and
in the southwest(60#{176}57’N, 138#{176}12’W). Great were located either by tnanpairs (Rohner and Doyle, females with radio-trans1989 and 1991, 116 nestlings monitored from 1 wk of age
until
fledging.
part
ioral
study
horned
gulating 1992)
millers. were
near
KJuane
hooting or
monitoring
As
of
a feeding
and
INDUCED
MORTALITY
IN GREAT
HORNED
OWLS
487
and the Yukon Territory (Curne, 1997). Further, many northwestern species have not been formally described, or belong to unresolved sibling complexes; flies from these latter cornplexes require examination of the polytene chromosomes of the larvae for species-level identification. Adults were identified to the lowest taxonomic-level possible through cornparisons with confirmed material in the Royal Ontario Museum (Toronto, Ontario, Canada) and the Canadian National Collection of Insects (Ottawa, Ontario, Canada). Voucher specimens were deposited in the entomological collection of the Royal Ontario Museum, with a voucher specimen number of ROM 979999. RESULTS
behav-
owlets were transferred to tethering platforms at a height of 3.5 m above the ground (Rohner, 1994). Fifty-five owlets (13 naturally fledged, 42 released from the platforms) were equipped with radio transmitters. During the pre-fledging period the owlets were checked two to four times per week, and between fledging and dispersal (post-fledging) the birds were radio-monitored at least once a week. During 1990 and 1991, 28 juvenile great horned owl carcasses were located. These were placed in individual plastic bags, labelled (band number, location, age, approximate time of death), frozen and shipped to the Ontario Vetennary College, University of Guelph, Guelph, Ontario, Canada. Each bird was necropsied and, if carcass preservation warranted, selected tissues (lung, liver, spleen, kidney, and heart; in some birds sections of skin and eyelid, brain, and digestive tract) were fixed in 10% buffered formalin, embedded in paraffin, sectioned at 6 p. and stained with hematoxylin and eosin for light microscopic examination. Specimens of black flies were carefully removed from these owls from areas where lesions were most numerous such as eyelids and auricular openings. The condition of individual flies varied according to the state of preservation of the host owls. Most were in an advanced state of decay and badly fragmented. Identifications were possible only for the most completely preserved individuals. Genitalia were cleared with lactic acid and examined at up to 130 under a stereomicroscope. Identification of black flies was further hindered by a lack of recent keys. The only taxonomic treatments for northwestern North America are long out of date (Stone, 1952; Sommerman, 1953) and include fewer than half of the 76 species now known from Alaska
A cause
86
of
the
too
of death
28
badly
ropsy
was
carcasses. autolysed
and
three
partially
for
a meaningful carcasses
scavenged.
Histologic
carried
out
The
quality
of the
were
on
poor tissues
less
lesions
of these
current
tethering
platform.
tablished Fourteen
for
wk
anemic
lesions
attributed
birds
had
Four
and tion.
one No
two
remaining
feeding. of con-
infection.
two between
birds. 10
seven
and
had fly
birds severe
died
of
of
age.
the
highway
on
the
the
Four and
skin spp.
from
birds
in this
age
owlets
were
older
of no
these
trauma
diagnosis
bird.
Three
of
owls
had
megaloschizonts
impacfor the group.
were
last
than
14
killed
on
was the
and
Five
Leucocytozoon birds
es-
were
feeding.
died as a result of cloacal diagnosis was established
Five
One septiceon the was
to black
concurrent
infections.
fly
diagnosis
these,
seskin
cellulitis and injury sustained No
were
and
lesions
spp.
Of
dehydrated,
killed
black
the remaining owlets were
of age.
of age
extensive
histologic
had a localized related to an
wk
had
to had
was
or freezthe birds
of anemia
Leucocytozoon
bird mia
14
10 wk
and
attributed
Four
birds.
preserved.
died
dehydration
17
sections
autolysis many of
than
Six birds
examined. vere
well
owlets
necwere
from
histologic to
23
were
evaluation
tissues
due from
surprisingly Nine
for
carcasses
additional
was
sometimes ing but
established
Five
reached
four
road-
in
liver
488
JOURNAL
OF WILDLIFE
and
myocardium
DISEASES,
but
no
VOL.
33, NO. 3, JULY
evidence
dothelial
of par-
zonts
asitemia. The
skin
feeding
lesions
were
areas
and
ventral raised,
rounding
small
cent feathers Black flies with
the
surfaces
were often
caked were
the
black
flies
one
skin
individual.
lesions
creased
from
resented
just
number
of
owls,
but
were
selected
Helodon
(Malloch),
n
ii
and
3;
reptotal the
basis
of
taxa
The as
pleuralis (Parahelodon) ra = Fries
aureum
Simuhium
(Dyar
onicolurn
the
preservation. to four
(Twinn),
(Eusimuliurn) =
Shannon)
complex,
Leu
cocytozoon
spp.
characterized on
as mild
numbers
served
of circulating
within
schizonts
or
n
vessels
of Leucocytozoon and
loschizonts Five
and
group,
had
cocytozoon
spp.
in
every
birds
had
of in
gametocytes
tissues, the
10
or
usually to
14
gametocytes
and occupied
in schizonts
fly
spleen. related
skin
10 wk of age spp. infections
had and
had sefly feedspp.
Leucocyto-
Severe
in
vessels. within
a
findings,
black
horned
owls
10 wk
of
and in concert with Leucocytozoon infections in owls 10 to 14 wk of age determined as the cause of death in of the 28 owl carcasses examined. additional road-killed owls had his-
tologic
evidence
fection The
but owl
of Leucocytozoon
were chicks
fly feeding. These ized by localized thrombosis the eyelids
feeders
of vessels. In were swollen
some of the closed.
to channel
that penetrate craterous
or
lets
labium
to initiate Iver, 1984).
were charactertissue necrosis
first record of black owls. Black flies
slashing
biting
action which
blood flow In addition
localized initiate
in-
on unfeathered underside of the caused by black
lesions edema,
(as opposed
and
spp.
in good body condition. examined in this study
had dozens of bite wounds areas of skin of the face, wings and inguinal areas
and may
fly feeding
under
flies are
from pool
feeders
like
the lesions
skin and using a
involving
the
lacerate
capillaries
(Sutciffe to direct
and blood
styMcloss
skin trauma, black fly attacks systemic illness, allergic reac-
within
tions
mega-
(1979) refer to a systemic reaction to black fly bites in humans known as “black fly fever” characterized by headaches, fever,
the wk
parasitemia
erythrocyte numerous
numbers observed
schizonts
marked spp.
tually
the
ob-
mild infections had based on observation
occasional within
owlets
were
gametocytes
our
the mosquito) produce small
depending
megaloschizonts
tissues. Birds with low level parasitemia vessels
infections or severe
on
This is the great horned
can-
38.
=
than
histology.
in great
and owls
Simucomplex,
3;
(Eusimuhium)
and
and
age spp. was 13 Three
with
on
1; Helodon
=
in-
were
the
(Distosirnulium)
decemarticulatus
hum
of
associated
their complete state of 45 intact females belong follows:
flies These
portion
flies
Based alone
edema,
carcasses.
a small black
on
owls
the
localized
owl
Leucocytozoon
DISCUSSION
by
of adjacent capillaries. intact female black
recovered
with black
count-
hemorrhage, considerable necrosis, inflammation,
thrombosis Forty-five
owlets had
surrounding were
megaloschi-
and
spp. infections were only observed between 10 to 14 wk of age.
zoon
dried blood. associated
characterized
vascularization,
infection
adja-
Microscopically,
were
subcutaneous local tissue
sur-
The
with found
or within
Sixty-five
on
areas
and
muscle
two of the birds in this age group vere skin lesions related to black ing but no evidence of Leucocytozoon
patagiwith
sites.
lung
heart
lesions. Birds less mild Leucocytozoon
jugular
erythematous
of the
of the infections
spp. of
edematous
cells in liver,
All
fly
corners
of the
were puncture
lesions
feathers. ed
cere, openings,
eyelids
multiple
black
in unfeathered
eyelids,
auricular
The
urn.
to
mainly
as the
beak,
groove
related
found
such
the
1997
liver. of
age Leuvir-
These en-
or
even
death.
Harwood
nausea, adenitis, generalized and allergic asthma. In Alberta katchewan tacks have
(Canada), caused
intense widespread
and
James
dermatitis and Sasblack fly vascular
atle-
sions 1969;
and mortality Harwood and
pathogenicity not
of
been
well
reported
HUNTER
ET AL-PARASITE
INDUCED
in cattle James,
( Fredeen, 1979). The
by
black
flies
for
established.
egg
birds
Edgar
production
drops
has
the
may
cells
by
mature
mune-mediated increased
evacuation
of
in
nests
by
Wyoming
black fly attacks. The attraction bird corpses was
of female previously
and Wood (1964), a thousand individuals
Lowther
over
(Eusimubiuni)
attracted
corpses
of great
attracted
Black to
although black
were
a
none
of
blood
feeding
the
The prevented cies
implicated
to
restnffi
and and
vectors
complex, ravens
Fallis, 1971). S. canonicobum
been
evaluated
for
Evaluation for fection was limited sections. We were culating blood within smears or birds
condition establishing of of
elongate vessels and tissues. were not tethered
is
the
of
dead
flies spe-
have already of Leucocytozoon
of
(Khan
Females of H. pheuralis complex have not
gametocytes stages of Unfortunately, obtained from on platforms.
spp. spp.
intissue only cirwithin schizogony blood nestlings
fly
cytozoon in owls
normal
1996).
and
spp. infection, tethered on
of
necrosis
with
little
mega-
associated
in-
Schizonts capilwith
the
Leucocyto-
may
have
altered
blood
flow
and
as has smithi
concurrent
af-
been infecto
Leuco-
was observed platforms. The
only teth-
on platforms 3.5 m above the have interfered with their fly avoidance behavior comindividuals that could and elevation of roost increased black fly ex-
and subsequent transmission (Rohner The
sec-
tissue
and combined circulating
pared to untethered choose the location sites. This may have posure spp.
in
(Siccardi et al., 1974). anemia, attributed
feeding
of owls may black
gaand
areas
pulmonary function in Leucocytozoon from
he-
circulating schizonts
observed. in pulmonary
pulmonary
in turkeys
during
evidence of sigspp. infection. Al-
gametocytes
Mortality
ering ground
been be-
response numerous
spp.
black
was
of
deim-
because of fragility
associated
there
endothelium numbers
tions
(body owls.
taxa collected, and members
Leucocytozoon to formalin-fixed able to identify
focal
spleen
fected suggested
Leucocytozoon
Leucocytozoon
were
and
However,
important
corax)
there
in
normal
red cell 1977),
or osmotic
numbers of the numerous
though
the
system
observed
flammatory were very
circulation
anti-erythrocytic
were
zoon
of the which
(Corvus
and
liver
Erythro-
the
suspected
tions of five owlets nificant Leucocytozoon
lary large
1991).
from
to be produced (Kocan, 1968).
large
chemical orient fe-
evidence
of engorgement lacking from
Two
as vectors
raptors
most
a
loschizonts,
on spe-
had the
decemarticubatus
S. aureum
of
located.
specimens
as
owls.
probably
thus other serve to
because
served
spp. to Hebodon
from
as in waterfowl.
is
deteriorated us from
eviuro-
concentrated
host
for initiation and C02) are
were
anemia
reticulo-endothelial
megaloschizonts
substances,
gland
developed
thought schizogony
The
in the are
by
factor patic
489
erythrocytes
Riper,
processes erythrocyte
caused
OWLS
produce
of parasite-induced (Maley and Desser,
metocytes
immer).
collected
odiferous
of the body; clues might
once
clues heat
collected Simubium
(Gava
owls
uropygial flies
cific parts or visual
the
similar
the
males
to by
Davies
flies horned
markedly
Most
black flies reported
to a substance
oil.
as
to
euryadminicubum
pygial
not
due
who of
from a single common loon Females of S. euryadmninicubum dently
red-tailed
(USA)
can
removed
of the
because formity
chicks
Van
be
HORNED
of infected
and
(Atkinson
cytes
laying
spp.
destruction
chickens tormented by black flies. S. Cain (pers. comm.) observed mortality and prehawk
IN GREAT
Leucocytozoon
(1953) in
MORTALITY
importance
Leucocytozoon
and of
the
Hunter, tethering
process in influencing mortality is difficult to determine. Mortalities due to parasitism were infrequent on the platforms in 1989 (n dant
=
0) and 1990 (n food supply, but
= 3), years in 1991 the
of abunfirst year
of the snowshoe hare decline, ten owlets died from parasitism (Rohner and Hunter, 1996). Presumably tethered birds were cx-
JOURNAL
490
posed
to
years.
The
OF WILDLIFE
black
flies
DISEASES,
in
necropsy
skewed
tethering
tion
and
each
of
sample
towards
the
VOL.
the
was
tethered
ACKNOWLEDGEMENTS We are grateful to J. C. Sutcliffe and G. F. Bennett for helpful advice during the study. Funding was provided by NSERC (grant to L. J. Krebs, Department of Zoology, University of British Columbia) and through cooperation with the staff of the Department of Pathology, Ontario Veterinary College, University of Guelph and the Canadian Cooperative Wildlife Health Laboratory, Ontario Region, Guelph, Ontario, Canada.
because
facilitated were
observa-
located
more
quickly.
We
have
owls
evidence
that
naturally
fledged
zoon
were spp.
also Only
infected with six carcasses
were
med
and
because
of autolysis
or
ing,
tissues
from
suitable
for
were
road
schizonts The
infections and
was
erate
to
thors pete
postulated for critical
only low
food
and
fected during
years
curred
in
are
able
in a year
of
1989 from
parasites
the
and
food
fledgling
survival
Decreased
fledgling
black
fly
and
in
coincided
the
snowshoe
Hunter,
1996).
parasite
availability tethering
of disease age
hare The
ering platforms in raptor studies black
flies
the but
prevalence
period
of food
researchers
to enhance should
using
arising
from
and
Leucocytozoon
exposure spp.
En-
ASHFORD.
and
patho-
27:
(Diptera:
993Simuli-
to
North
role
the
black
America.
In
In-
London,
England,
1969.
H.
1975.
at
the
of
Wildlife R.
York,
National
AND
A.
transmission,
and
birds.
corvid
fly
Quaes-
1979.
7th. ed. pp.
(;nats, in
MacMillan
148-149.
JR.,
AND in
Wildlife
I.
B.
TAR-
Canada
geese
Refuge.
Journal
404-411.
11: M.
black
In Entomology
BARROW
Diseases
A.,
JAMES.
health,
H.
the
Alberta.
Leucocytozoonosis
Seney
of hens.
341-72.
forms.
New
J.
M.,
effect
laying
of in
T.
related
Co., C.
M.
animal
Publishing
the of
Outbreaks
AND
and
of
(Malloch) 5:
F.,
and
study
production
779-780.
32:
J.
flies,
human
in
egg
Science
R.
KHAN,
field
A on
Entomologicae
SHIS.
FALLIS.
of
Leucocytozoon
Journal
Canadian
Speciation,
1971.
schizogony
of Zoology
49:
1363-1367.
short-
K0CAN,
R.
M.
erythrocyte
teth-
data collection be aware of the
risk
W
reference
Press,
articuin
HERMAN,
by
the
on
M.
Oxford,
R.
flies
with
1953. bites
F.
tiones
and
The
AND
Black
Academic
A.
HARWOOD,
to
mediated
Yukon,
Simulium
of host-
factors.
1997.
the
fly
black
decline
(Rohner
likely
other
platforms during
1991
cycle are
and
is unclear,
potential
the
S.
Poultry
spp.
consequences
interactions
food of
with
A. PEIRCE,
C.
(ed).
black
remains
Leucocytozoon
and
19-48.
of northwestern
FREDEEN,
the
due
ens.
Loye
273-305.
EDGAR,
and
survival
of
Kreier
oc-
by
D.
pp.
owls
infection
J. Press,
L.
University
1991.
Haensoprot
and
interactions,
P., M.
fly fauna
and
caused
III. haematozoa:
sects of the Yukon, H. V. Danks and J. A. Downes (cdi.). Biological Survey of Canada (Terrestrial Arthropods), Ottawa, Canada, in press. DEsSER, S. S., AND G. F. BENNETF. 1993. The genera Leucocytozoon, Hernoproteus and Hepatocystis. In Parasitic protozoa, Vol. 4, 2nd ed., J. P.
proas
of
haematozoa: Mortality Journal of Natural History
idae)
in-
young
fight
high. infection
the
RIPER,
Avian
CURRIE,
to black
supply,
1990,
C.
1001.
northern
We
VAN
epizootiology
Oxford
G.
1993.
au-
become
anemia
feeding
the
conditions
to successfully
recover
every
BENNETF,
CITED
Lencocytozoon,
Bird-parasite
genicity.
may comthe female
spp.
high and
et
of mod-
is exposed
normal
AND and
(eds.). gland, pp.
re-
and
subsequently
under
T,
Zuk
Tengmalm’s Finland. This
Leucocytozoon
that
In
blood
ziemanni
egg-laying. almost
C.
Pathogenicity
understood
female in
chick
many with
pose
of
that parasites resources of
owl
ATKINSON,
Plasmodium,
availability,
for that
horned
Both
Korpimaki
L.
observed
owls necessary We suspect flies
that
LITERATURE
were parasitic
poorly
1993).
size in funereus)
effect
exam-
scaveng-
these
numerous
are
reported
clutch (Aegobius
of
and myocardium. consequences
Bennett,
(1993)
great
had
in liver ecological
Leucocyto-
examination.
but
(Desser duced owls
two
histologic kills
parasite al.
only
1997
three
strongly
birds
process carcasses
33, NO. 3, JULY
to
cocytozoon ology KORPIMAKI, NETT.
success
1968. destruction infections.
13:
Anemia
and
mechanism
in ducks The
of
acute
with
Journal
of
Len-
Protozo-
465-468. E.,
1993.
H.
HAKKARAINEN,
Blood
of Tengmalm’s
parasites
owls:
(;.
AND
and
F. BEN-
reproductive
Detrimental
effects
HUNTER
ET AL-PARASITE
on females but not on males? Functional ogy 7: 420-426. KREBS, C. L., R. BOONSTRA, S. B0UTIN, M. S.
HANNON,
N.
M. SMITH,
drives
K.
the
kon?
In
MARTIN,
snowshoe
hare
Wildlife arid
R. Barrett
pp.
886-896.
of a black vies,
toward
AND
Entomologist MALEY,
AND
kin
S.
anemia, of
horned
Yu-
euryadminiculum common
loon.
F.
Da-
AND
infections.
gametocytemia, in
Canadian
naturally Journal
of
Anemia 1.
Quantifi-
and
osmotic
ley, \Vest
1981.
(eds.).
Chiron
D.
Publications,
I.
Pc-
Zoology
55:
Leucocytozoon
Diseases
Keigh-
1995.
Great
Canada, horned
pp. owls
42-43, and
of the
55:
258-273.
0.
RUTHERFORD,
M.
A.
1952.
The
of
Washington
54:
J.
1953.
F,
AND
of
Simuliidae). Society
Simuliidae
the
T
Alaskan
of Washington
of Alaska
(Diptera).
Entomological
Society
69-96. S.
ics of blood-feeding muliidae). Journal Received
\V.
Proceed-
B.
MCIvER. in
black
1984. flies
for publication
Mechan-
(Diptera:Si-
of Morphology
180:
23 January
1995.
145-147. snowshoe
sur-
AND
Identification
(Diptera:
Entomological
Proceedings SUTCLIFFE
First-year
a peak and deCanadian Jour-
Pathology and prevention of smithi infection of turkeys. Avian
fly larvae
ings STONE,
1996.
owls during hare cycle.
18: 21-32. K.
black
Jour-
1092-1097.
H. 1974.
locating
forest.
26: 33-35.
HUNTER.
74:
W,
DERIEUX.
pp. 15-19. ROHNER, C. response of great horned hare cycle in the boreal forest. Ph.D. thesis, Department of Zoology, University of British Columbia, Vancouver, Columbia,
B.
horned of the snowshoe
SICCARDI,
infected
England, numerical snowshoe
Research
demog-
of
boreal
great Con-
359-370.
65:
Methods
nests in the
owl
cline nal of Zoology
in
Current
Yorkshire, 1994. The owls to the
491
on
Ecology 1992.
I. DoYLE.
of great
vival
‘floaters”
of Animal
nal of Raptor
knowledge of the haeof raptors. In Recent advances in the of raptor diseases, J. E. Cooper, and A. C. A.
(;reenwood
British
AND
Canadian
1977.
OWLS
response of hare cycle:
non-territorial
Journal
SOMMERMAN,
M.
matozoa
study
of
raphy.
Specificity
355-358. PEIRCE
owls
sequences
McLondon, D.
1964.
DESSER.
erythrocytes
ducklings.
The numerical to the snowshoe
1996.
What
Canada’s
HORNED
61-68.
J.
911-913.
sirnondi
of
fragility
WooD.
the
S.
Leucocytozoon cation
M.
host,
96:
J.,
C.
in
IN GREAT
hares: What causes the time lag in the numerical response of predators to cyclic prey? Oikos 74:
DALE,
SINCLAIR, 1992.
cycle
Sirnulium
its
Ecol-
MORTALITY
great horned
D.
fly,
E.
Populations, (eds.). Elsevier,
2001:
England,
J. K.,
R.
R. TURKINCTON.
AND
Cullough LOWrHER,
A.
INDUCED
125-144.
of
