Journal
of Wildlife
DIseases,
31(4), 1995, pp. 486-490
Disease
Association 1995
C Wildlife
STUDIES
ON THE
CENTRAL
JesUs
AND
M. Perez,
HYPODERMOSIS
SOUTHERN
Jos#{233}
E. Granados,
and Isidoro
and Vegetal Biology and
23071 Jaen, Spain
ABSTRACT:
November
From
order
this
and
to
estimate
ungulate
Sierras
a prevalence
was
a maximum
found,
classes.
Key
species.
de Cazorla,
of 92%,
of
although
The main
words:
Ecology,
The
of Experimental
observed
in prevalences
among
in deer
was in the back
tissues.
actaeon,
red deer, Cervus
elaphus,
genus
Species
Hypoderma
derma
(La-
1818)
is restricted
to the
and comprises
a number
1965).
After
oviposition,
the
first-instar
larvae
penetrate
dermosis
have
deer (Capreolus
actaeon
in the
or 97 to 100%
gifer
specially
Hypoderrna
November,
lineatum
submucosa
or in the
connective
of the
this
to autumn)
and migrate
via contissues
to reach,
about
February
to
(October
to November
in the south(Keilin,
in order
plates
happen
in about
on average,
case of Hypoderma
5 wk (Keilin,
is about
26
actaeon
HypoWithin
of hypoin roe
in red
in Hungary,
due
in red deer
due to
(Sugar,
caribou
to
H.
1976)
(Ran-
due
to H. tarandi
(Thomas
Hypoderma
of red deer
actaeon
in Europe
(Zumpt,
(1990)
1965).
In
found
H.
in red
deer
of 87%
determine
the
actaeon
among
of central
and
Spain.
MATERIALS
Larval
season
can
1944).
Then,
to orientate
to the open
vember
were
collections
when
be
AND METHODS
found
1992
shot
in
were made during
hunting
Hypoderma
spp.
larvae
forming
warbles.
Between
Noand February
1993,
455 red deer
feeding
non-selective
huntings
in
Sierra
de Alcaraz,
Montes
de Toledo
and Sierras
de Cazorla,
Segura
y Las Villas
Natural
Park,
central
and southern
Spain
(37#{176}30’to
39#{176}30’Nand 2#{176}00’to 5#{176}30’E).
Deer were sampled
4 to 10 hr after
death.
Morena,
Sierra
Larvae
were collected
from
hide was removed
a number
in deeper
tissues
(Fig.
1).
counted
and added
to those
1944).
This
days
in the
(Zumpt,
genus
in
air and begin
to actively
feed.
When
the
third-instar
larvae
are mature
they emerge
through
the orifice,
drop to the ground
and
pupate
into the soil. Adults
emerge
from
pupae
time,
age
1990).
parasite
a prevalence
southern
southern
the
Our
objective
was
to
prevalence
of Hypoderma
red deer
in several
locations
of cattle
(in the
host back
an orifice
spiracular
with
of diaphragm
would
a
to
host-specific.
prevalences
same
country
in Canadian
tarandus)
Kiliaan,
typical
host
Spain.
and strictly
host-specific
Spain,
Martinez
et al.
diana
caused
hypodermosis
of
the
summer
nective
March
ern U.S.) the
larvae
made
the posterior
U.S.
wall
is
paand
and
first-instar
larvae
are located
in
esophagic
tissues
and
different
been
reported:
98%
capreolus)
and 65%
deer
(Cervus
elaphus)
H. diana,
and 93%
hatching
small
into
the host
system;
occasionally
death
result
(Kettle
September,
October
belonging
are relatively
ungulates
high
wild
Holarctic
of species
skin through
the hair
follicles.
Larval
development
is subcutaneous
and during
migration
larvae
can damage
several
kinds
of host
tissues
and
organs,
including
the
nervous
and
host
1955).
In
Sciences,
were
larvae
whose
larval
stages,
commonly
known
as
grubs
or warbles,
are important
parasites
of Bovidae
and
Cervidae
hosts
(Zumpt,
central
ralysis
Utsi,
IN
1992 to February
1993, 455 red deer (Cervus
elaphus)
were surveyed
the prevalence
of warble
fly (Hypoderma
actaeon)
larvae
under
the skin of
Material
came
from
Montes
de Toledo,
Sierra
Morena,
Sierra
de Alcaraz,
Segura
y Las Villas
Natural
Park (central
and southern
Spain).
We observed
with a mean
± SD intensity
of 35.7
± 41.3
grubs
per
parasitized
host; there
317
larvae
per
host. No significant
differences
in prevalence
by host sex were
significant
differences
location
of feeding
Warble
fly, Hypoderrna
dipteran
DEER
Ruiz-Martlnez
Faculty
INTRODUCTION
treille,
region
RED
SPAIN
Department
of Animal
Box 63, Jaen University,
in
AFFECTING
1965).
486
the hide,
of larvae
These
larvae
and
as the
remained
larvae
within
were
war-
PEREZ
ET AL.-HYPODERMOSIS
IN THE RED DEER
487
\\
--
1.
FIGURE
(arrows)
after
removal
bles
deeper
and
spp.
larvae
were
defined
as mean
according
age
age
Taber
with
total
and
2 yr,
to
skin
and
three
stage
of
larvae
skin
surface;
lopov
and
in
in
aggregated
or
it was
Zharkov
prevalence
host
and
larvae.
and
were
eval-
yr.
formed
classes
test.
the
Software
using
Statistical
ifornia)
in
order
tween
host
age
Regression
developmental
in each
area
of host
according
Possible
parasitism
age
of a chi-square
same
calculated
(1988).
of
sex
the
between
were
tested
analysis
(arrows)
Larvae
to So-
differences
different
by means
was
per-
program
BMDP
7.0 (BMDP
Inc. 1993,
Los Angeles,
Calto evaluate
the relationship
beand intensity
of parasitism.
identified
were
Brauer,
Sugar
recorded.
were
grouped
and
phalon
in the
considered:
headneck, anterior
extremities,
back, abdomen,
posterior
extremities,
and hind-quarters.
Locations
of all larvae
were
identified
within
these
areas.
We
defined
the
term
grouping
index
as the
number
regions
In-
to Larson
>5
Larvae
and
prevalence
et al. (1982).
classes
and
2.
within
deer
skin. Scale
2 cm.
=
taeon
(intensity).
were
age
5 yr
2)
Hypoderma
the host
intensity
bar
5 cm.
=
(Fig.
of
according
3 to
body
the
FIGURE
larvae
tissues
bar
number
surveyed
estimated
(1980)
uated:
1
Several
Scale
to Margolis
of animals
was
spp.
subcutaneous
skin.
parasitizing
as
and
to
deer
the
well
tensity
Deer
the
removed
as
Hypoderma
attached
of
recorded
Sex
The
remained
1858
as
according
(1976),
by
location
Zumpt
instar
(1965)
pseudoce-
of the
spinulation
of second
size of posterior
peritremes
ac-
Hypoderma
to
larvae
of third
and
instar
RESULTS
We
(92%)
observed
of 455
red
Hypoderma
deer;
the
very
similar
in both
with
host age (Table
significant
differences
different
0.01,
nificant
=
host
sex
df = 1, P
differences
age
actaeon
prevalence
was
sexes,
and
increased
1). Nevertheless,
no
in prevalence
among
were
=
found
host
square
=
A mean
26.47,
df = 2, P
(± SD) intensity
classes
were
<
larvae
per host (ranging
was obtained,
with the
from
highest
ber
with
associated
(chi-square
0.898);
however,
sigin prevalence
among
different
of larvae
in 419
found
(chi-
0.0001).
of 35.7
± 41.3
one to 317)
mean
numthe
older
deer
JOURNAL
488
TABLE
OF W1LDUFE
Parasitism
Spain.
1.
February
DISEASES,
455
in
31, NO.4,
VOL.
red
deer
by
OCTOBER
Hypoderma
1995
by sex
actaeon,
and
age
class,
November
to
1992
1993,
Age
1 to 2 yr old
Number
Number
Range
Mean
in infected
animals
(±SD)
intensity
62
70
74
113
70
66
51
58
70
107
69
65
82
83
95
95
99
98
1-157
1-105
2-256
1-317
1-232
2-263
(Table
1). Host
31
age
in years
ber of larvae
(y) were
related
by means
of the equation:
y
(R
32
±
32
± 28
(x) and
in host tissues
another
12%
(Table
2).
Comparatively,
few grubs
were
removed
from
the remaining
host body
areas
considered.
The grouping
index
of larvae
obtained
reached
83%.
No data
about
first-instar
larvae
were
all larvae
or third-instars.
instar
larvae
vember
of these
collected
The
increased
percentage
from
were
second
73%
of thirdin No-
to 100% in late-February;
over
were
nearly
ready
to pupate.
half
ent
among
prevalence
of
similar
Martinez
TABLE
different
southern
Host
to the prevalence
et al. (1990)
2.
Location
skin areas
Spain
body
of
region
(89%)
found
for
Hypoderma
Number
larvae
58
314
Hind-quarters
Anterior
extremities
Posterior
of
13,598
Abdomen
extremities
is
by
spp.
larvae
into
red deer
from
central
and
1992 to February
1993).
Head-neck
Back
parasitism
Hypodernsa
of 455
(November
92%
actaeon
was observed
level
of parasitism
1,954
Percent
of
total
0.36
84.10
1.94
12.08
Range
in
infected
animals
1-3
1-298
1-24
1-58
80
0.49
1-5
165
1.02
1-10
47
red
deer
Females
50
± 47
in
Spain,
± 49
and
the
for H. actaeon
in red
found
by Sugar
(1976);
to prevalence
of differspp.
(Sugar,
affecting
1976;
other
Thomas
and
wild
Kiliaan,
1990).
In
this
study,
both
intensity
of red
actaeon
increased
level of parasitism
the
prevalence
and
deer
parasitism
with
with
age, although
was not statistically
H.
the
dif-
ferent
from
the younger
deer.
Perhaps
older deer,
with
their
larger
body,
tended
to
harbor
a higher
number
of larvae
than
younger
deer
(Table
is in contrast
noted
goats
A mean
± 42
Hypoderma
cervids
cies
DISCUSSION
of red deer
with
H.
in this
study.
This
35
Males
prevalence
(93%)
deer
in Hungary
it also was similar
=
available;
± 43
diana
num-
to each
other
9.05 + 7.50x
=
0.38,
P < 0.001).
The distribution
of grubs
were
84%
in the back,
and
were
found
in the hind-quarters
38
Females
y r old
Females
(%)
Males
>5
Males
evaluated
infected
Prevalence
3 to 5 yr old
1).
with
This
level
in cattle
(H.
(Przhevalskiana
observation
of warble
bovis)
silenus).
fly spe-
and domestic
In these host
species
and their
associated
warble
fly parasites,
the younger
animals
were
the more
susceptible
than
repeatedly
exposed
older
animals
and had a higher mean
intensity
of parasitism
than
older
animals
(Tarry,
1987;
Puccini
et al., 1987).
An acquired
resistance
H. bovis
three
is established
in
and
H. lineatum
infestations
observation
deer
alence
increased
flies
and
the
and
other
(Dama
wild
intensity
with
host
of
age
Bunch,
1989;
Ruiz
and
Ruiz
et al., 1993).
Based
on the proportion
by
cases
our
in para-
dama)
spp.
to
or
Yet
trend
hemionus)
(Pharyngomyia
spp.).
In these
cattle
two
1987).
with
deer
deer
(Odocolleus
geal bot
phenemyia
(Boulard,
agree
sitism
of red
such as fallow
older
after
cervids
or mule
pharyn-
and Ceboth
prev-
parasitation
(McMahon
Palomares,
of second
also
and
1993;
and
PEREZ
third
instar
larvae
the
may
sampling
start
in
Our
observations
recovered
of
larval
flies
our
According
the
to Esch
distribution
on the
parasitized
hosts
since
mean
Mar-
per
derina
or
than
their
puparia
the
deer
direct
et al. (1990)
notes
individ-
Hypoderrna
in
species
a very
contrast
animals
April-May
in
similar
in this
parasitized
prevalence
of
parasitizing
area
study
by
H.
H. diana
identified
H.
actaeon
red
of
we
Spain.
found
In
no
diana,
but
the
was
high.
discrepancy
between
our observations
those
of Martinez
et al. (1990)
could
The
and
have
been
due to their
dependence
upon
Zumpt
(1965)
for species
description.
Thus,
in our
opinion,
the
material
obtained
by these
authors
would
descriptions
(1976)
for
ma species
same
a revision
in the
near
using
the
(1965)
and
Sugar
of the Hypoder-
involved,
since
species
in almost
host
Perhaps
need
of Zumpt
identification
they studied
the same
future,
the
area.
a classification
system
of Oestridae
and Hypodermatidae,
based
on biochemical
and
genetic
techniques,
can be developed
as a tool for identification
of these
parasites
of ungulates.
laboration
in
of Valcaza
(Ciuthe deer
for this
go to Mr.
F. G#{243}mez and
University)
for
their
colwork.
LITERATURE
BOULARD,
C.
1987.
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France
control
in
Europe,
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with
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of
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(1987)
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that
the H. bovis
population
can be described
as a negative
binomial
distribution.
Based
on our results,
adult
H. actaeon
can emerge
from
in
36:
D. S.,
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