Responses of female bank voles (Clethrionomys glareolus) to dominant vs subordinate conspecific males and to urine odors from dominant vs subordinate males


Hoffmeyer, I.

Behavioral and Neural Biology 36(2): 178-188

1982


BEHAVIORAL
AND
NEURAL
BIOLOGY
36,
178-188
(1982)
Responses
of
Female
Bank
Voles
(Clethrionomys
glareolus)
to
Dominant
vs
Subordinate
Conspecific
Males
and
to
Urine
Odors
from
Dominant
vs
Subordinate
Males
INGE
HOFFMEYER
Department
of
Ecological
Chemistry,
University
of
Lund,
Ecology
Building,
Helgonavagen
5,
S-223
62
Lund,
Sweden
Dominant
and
subordinate
male
bank
voles
from
stable
hierarchies
were
used
as
choice
objects
and
urine
donors
in
tests
with
estrogen-treated
females.
In
a
two-choice
male
preference
test
12
out
of
15
females
reliably
showed
a
preference.
All
12
preferred
the
dominant
male.
In
a
two-choice
odor
preference
test
the
females
were
presented
with
equal
quantities
of
normal
elimination
urine
from
dominant
and
subordinate
males.
Thirteen
of
fifteen
females
tested
individually
showed
a
preference:
Twelve
of
them
preferred
the
urine
of
a
dominant,
over
that
of
a
subordinate
male.
Other
females,
tested
in
groups
of
five,
were
presented
only
with
the
lipid
(dichloromethane)
fraction
of
urine.
In
this
case
11
of
12
groups
preferred
urine
lipids
of
dominant
males
to
urine
lipids
of
subordinates.
Cumulative
investigation
times
and
frequency
of
visits
were
used
to
determine
preferences.
The
results
are
discussed
with
regard
to
possible
causes
and
biological
function.
Female
preference
here
represents
a
case
of
sexual
selection
partly
by
olfaction,
and
may
augment
the
reproductive
success
of
dominant
males.
Male
bank
voles
reportedly
form
stable
dominance
hierarchies
in
both
the
field
(Viitala,
1977,
with
Clethrionomys
rufocanus)
and
the
laboratory
(S0rensen,
1981,
with
C.
glareolus).
Dominance
hierarchies
assign
priority
to
a
limiting
resource
such
as
food,
space,
and
mates.
Several
investigations
have
reported
the
relationship
between
male
dominance
and
male
re-
productive
success
in
small
rodents
(DeFries
&
McClearn,
1970;
Horn,
1974).
The
aim
of
the
present
investigations
is
to
elucidate
the
role
of
the
female
bank
vole
in
mate
selection.
The
hypothesis
was
that
female
preference
may
represent
a
case
of
sexual
selection
partly
by
olfaction.
It
was
therefore
necessary
to
determine
if
female
bank
voles
can
distinguish
between
dominant
and
subordinate
males,
or
their
odors,
and
if
they
prefer
one
type
of
male
or
odor
to
the
other.
Sex
attractants
are
found
in
the
urine
of
male
laboratory
mice
(Scott
&
Pfaff,
1970).
Furthermore,
the
dominance
status
of
males
may
be
expressed
through
odors
in
the
urine
(Jones
&
Nowell,
1974).
Data
on
the
urinary
marking
of
male
bank
voles,
Clethrionomys
glareolus
(Chris-
178
0163-1047/82
$2.00
Copyright
©
1982
by
Academic
Press,
Inc.
All
rights
of
reproduction
in
any
form
reserved.
FEMALE
BANK
VOLE
MATE
CHOICE
179
tiansen,
1980;
Hoffmeyer
in
prep.),
indicate
similar
functions
in
this
species.
Christiansen
(1976,
1980)
has
suggested
that
the
sex
attractant
of
male
bank
voles
is
produced
by
the
preputial
glands
and
mixed
with
the
urine,
as
in
mice
(Bronson,
1966;
Bronson
&
Caroom,
1971)
and
rats
(Rattus
norvegicus)
(Gawienowski,
1977).
Gustafsson,
Andersson,
&
Meurling
(1980)
found
that
dominant
male
bank
voles
have
larger
preputial
glands
than
subordinates,
suggesting
a
relationship
between
social
dom-
inance
and
the
rate
of
production
of
preputial
gland
secretion.
Here
two
kinds
of
experiments
were
performed
with
female
bank
voles.
The
first
tested
their
preference
between
dominant
and
subordinate
males.
The
second
tested
their
preference
between
urine
odors
from
these
two
types
of
male.
MATERIALS
AND
METHODS
Animals
All
test
animals
were
laboratory-raised
descendants
from
a
wild
stock.
They
were
kept
in
standard
laboratory
mouse
cages
(40
x
20
x
15
cm);
photoperiod
of
18
hr
light
and
6
hr
dark;
temperature
of
22
±
5°C.
Voles
were
sexed
at
10
days
of
age
and
weaned
at
18-21
days
of
age.
Both
mother
and
father
were
present
until
the
age
of
weaning.
At
weaning,
the
young
were
separated
by
gender
and
placed
in
groups
of
five.
All
were
housed
in
the
same
room.
Fourteen
days
before
the
tests,
the
females
were
transferred
to
larger
cages
(80
x
40
x
15
cm)
similar
to
the
normal
breeding
cages;
they
were
fur-clipped
for
individual
identification.
Three
days
before
the
tests,
they
were
weighed
and
treated
with
estradiol
benzoate
(Ovex
B,
20
gg/
kg
bw)
to
make
them
receptive.
The
females
had
no
sexual
experience
(but
had
been
living
with
their
parents
and
brothers
until
the
age
of
18
days).
Nothing
was
done
outside
the
test
situation
to
determine
the
sexual
receptivity
of
the
females.
Vaginal
smears
from
female
bank
voles
do
not
provide
easily
identifiable
criteria
as
they
do
in
the
laboratory
rat
(Gustafsson
&
Westlin,
personal
communication).
Estrous
female
voles
are
recognizable
because
they
always
seek
and
stay
close
to
the
male
in
a
way
clearly
different
from
that
shown
during
agonistic
interaction.
The
males
used
for
female
choice
and
as
urine
donors
were
from
all-
male
groups
of
3-5
individuals
that
had
established
stable
dominance
hierarchies.
Each
individual
was
identified
as
dominant
or
subordinate
based
on
data
gathered
over
at
least
1
month
prior
to
tests
following
the
procedure
of
SOrensen
(1981).
This
was
done
to
assure
that
long-term
physiological
correlates
of
dominance
and
subordinance
status
with
odors
had
developed
(Bronson
&
Eleftheriou,
1964;
Lombardi
&
Vandenbergh,
1977).
Males
used
in
female
choice
tests
were
always
derived
from
the
same
male
group
to
minimize
agonistic
interaction
(by
scents
or
sounds)
between
the
males
during
the
test.
Ten
dominant:
subordinate
pairs
of
males
were
available
from
ten
all-male
groups.
180
INGE
HOFFMEYER
Urine
Collection/Stimulus
Odors
The
urine
of
dominant
and
subordinate
males
was
collected
in
special
"metabolism
cages"
similar
to
the
one
described
by
Jones,
Dilks,
&
Nowell
(1973),
but
modified
for
voles
with
separate
sleeping,
feeding,
and
urination
sections.
Single
males
were
housed
in
a
metabolism
cage
overnight
(from
1700
to
900)
for
urine
collection.
Each
night
two
males,
the
dominant
and
one
of
the
lowest
ranking
males,
from
a
group
were
used
as
donors.
They
were
then
put
back
into
the
male
group
from
which
they
came.
Urine
was
never
collected
from
a
male
for
more
than
one
night
at
a
time,
and
at
least
4
days
passed
before
the
male
donor
was
re-used
if
at
all.
Urine
was
placed
in
separate
tightly
sealed
vials
and
frozen.
For
Experiment
2a
urine
was
used
the
day
after
collection.
For
Experiment
2b
extracts
from
the
lipid
portion
of
urine
were
prepared
by
shaking
the
urine
with
twice
its
volume
of
dichloromethane
and
centrifuging
for
5
min.
When
the
layers
separated
the
dichloromethane
layer
was
collected
and
stored
in
tightly
sealed
vials
in
the
freezer.
Samples
of
the
dichloromethane
fraction
were
sometimes
briefly
thawed
and
refrozen.
The
two
samples
used
in
a
test
were
from
the
same
date
of
collection.
Procedure
The
females
were
tested
individually
in
their
home
cage.
The
other
females
in
the
group
were
removed
30
min
before
the
start
of
the
test
and
provisionally
placed
in
a
separate
cage.
Most
of the
wood
shavings
were
also
removed.
Tests
were
run
during
periods
of
daily
activity
in
light.
Frequency
of
visits
or
cumulative
investigation
time
were
used
to
determine
the
preference
of
the
females.
EXPERIMENT
1
Female
Choice
between
Dominant
and
Subordinate
Males
The
two
males
used
in
each
preference
test
with
a
given
female,
were
placed
in
separate
live-traps
(UGGLAN
Special
with
netting
boxes;
mesh
width
=
3
mm)
on
a
Plexiglas
plate
adapted
in
size
to
the
bottom
of
the
female's
cage.
This
plate
was
covered
with
filter
paper
fixed
with
tape.
An
8-cm
large
zone
("trap
zone")
was
delineated
around
each
trap.
The
traps
were
attached
at
adjacent
corners
of
the
plate
such
that
when
placed
in
the
female's
cage
one
of
the
trap's
long
sides
pressed
against
the
side
wall
of
the
cage,
and
the
entrance
side
against
the
end
wall.
The
entrance
holes
of
the
traps
were
blocked.
The
males
were
put
into
the
traps
10
min
before
the
start
of
a
test.
While
the
female
was
briefly
removed,
the
plate
with
the
two
traps
attached
was
placed
inside
her
cage.
The
female
was
then
put
at
the
middle
of
the
wall
opposite
the
side
with
the
two
traps.
Recording
started
when
the
female
had
visited
both
traps
once,
and
was
continued
for
10
min.
The
following
criteria
were
used
during
recording:
(1)
"approach
to"
was
transgression
of
the
FEMALE
BANK
VOLE
MATE
CHOICE
181
trap-zone
border;
(2)
"visits
to"
were
stays
of
shorter
or
longer
duration
within
the
trap-zone
border;
and
(3)
"to
be
near"
was
being
within
the
trap-zone
border
and
intermittently
sniffing
the
trap.
Results
All
the
females
that
approached
the
males
(12
of
15)
spent
more
time
near
the
dominant
male
(Fig.
1,
left,
p
<
.01,
Wilcoxon
matched-pairs
test,
two
tailed).
All
of
these
12
females
also
made
a
greater
number
of
visits
to
the
dominant
male
than
to
the
subordinate
one
(Fig.
1,
right,
p
<
.01,
Wilcoxon,
matched-pairs
test,
two
tailed).
The
females
sometimes
showed
long
latencies
before
they
approached
one
of
the
males, but
once
they
made
a
sniffing
contact
there
was
a
change
in
the
behavior.
Eight
of
the
twelve
females
showed
the
clearest
behavioral
signs
of
being
receptive:
they
crouched
close
to
the
trap
with
the
selected
male
and
performed
a
characteristic
"flat
run"
alongside
the
trap,
sometimes
rubbing
the
flank
or
belly
against
the
trap.
A
"flat
run"
is
a
swift
running
bout
during
which
the
female's
body
appears
somehow
flattened
out
through
a
lowering
of
the
body
and
slight
depression
of
the
back.
There
may
be
elements
of
intention
to
lordosis
in
this
behavior.
Three
of
the
twelve
females
showed
lordosis
in
front
of
the
trap
with
the
male
chosen.
There
was
no
variation
in
general
outcome
with
the
different
pairs
of
males
used,
However,
one
of
the
dominant
males,
known
to
be
particularly
aggressive
in
male—male
interactions,
induced
flight
reactions
in
one
of
the
females.
Only
two
females
urinated
on
the
filter
paper
between
the
males,
and
the
urinations
were
in
a
few
large
spots.
EXPERIMENT
2
Female
Choice
between
Dominant
and
Subordinate
Male
Urine
(2a.)
Whole
urine.
The
same
set-up
as
in
Experiment
1
was
used.
The
empty
traps
were
thoroughly
cleaned
and
covered
with
filter
paper
on
top,
sides
and
end.
Immediately
before
the
start
of
a
test,
the
urine
of
a
dominant
male
was
placed
on
one
trap
and
urine
of
a
subordinate
on
the
other.
Equal
quantities
of
each
urine,
freshly
collected
from
the
metabolism
cages
were
distributed
equidistantly
in
0.02-ml
drops
on
the
filter
paper
covering
the
trap.
Two
drops
were
placed
on
the
top,
two
on
the
long
side,
and
one
on
the
end
side.
Recording
began
after
the
female
had
visited
each
of
the
traps
once,
and
the
cumulated
time
as
well
as
the
frequency
of
visits
were
noted
for
5
min.
Results.
Thirteen
out
of
the
fifteen
females
approached
urine
from
both
dominant
and
subordinate
males.
Twelve
of
the
thirteen
females
spent
more
time
near
the
urine
from
a
dominant
male
than
near
that
of
a
subordinate
male
(Fig.
2,
left,
p
<
.02,
Wilcoxon
matched-pairs
test,
500-
a
E400
E
ott
E
O
-0
Es
300
-
o
O
5
*3
*14
.2
•II
13
6
1
w
40
E
a
7
C
30
.;
200-
0
.
E
0
`‘2,
20
100-
12
10
a
15
z
SO
100
200
300
400
10
20
30
40
Time
in
secs
near
subordinate
male
No
of
visits
at
sudordinate
male
FIG.
1.
Female
bank
vole
preference
between
dominant
and
subordinate
conspecific
males.
Each
point
represents
one
female.
(Left)
Preference
measured
by
the
cumulated
time
spent
within
the
trap
zone
of
each
type
of
male
(p
<
.01).
(Right)
Preference
measured
by
the
frequency
of
visits
to
each
type
of
male
(p
<
.01).
In
one
point,
C),
the
values
of
two
females
coincide.
(p
based
on
Wilcoxon
matched-pairs,
signed-ranks
tests,
two
tailed).
oo
2I3Ag
IA
ld,
3
0H
gDNI
400-
0
11
0
2
E
300-
E
O
V
200-
Time
in
secs
w
it
h
100
-
20-
'3
0
10-
.
100
200
300
400
10
20
30
40
50
Time
in
secs
with
subordinate
male
odor
No
of
visits
at
subordinate
male
odor
Fig.
2.
Female
bank
vole
preference
between
urine
odors
from
dominant
and
subordinate
conspecific
males,
in
Experiment
2a,
where
the
females
were
tested
individually.
Each
point
represents
one
female.
(Left)
Preference
measured
by
the
cumulated
time
with
each
type
of
odor
(p
<
.02).
(Right)
Preference
measured
by
the
frequency
of
visits
to
each
type
of
odor
(p
<
.01).
(p
based
on
Wilcoxon
matched-pairs,
signed-
ranks
tests,
two
tailed).
F
EM
ALE
BANK
VOLE
MAT
E
C
HOIC
E
00
184
INGE
HOFFMEYER
two
tailed).
Nine
of
these
twelve
visited
the
trap
spotted
with
urine
from
a
dominant
more
frequently
(Fig.
2,
right,
p
<
.01,
Wilcoxon
matched-
pairs
test,
two
tailed).
However,
the
females
showed
smaller
differences
in
the
cumulated
times
spent
at
the
two
types
of
odor,
than
was
the
case
with
the
two
types
of
male
(U
=
24,
p
<
.002,
Mann—Whitney
U
test,
two
tailed).
Furthermore,
the
hesitation
in
choice
(measured
by
the
number
of
shifts
between
the
stimulus
objects)
was
greater
in
preference
tests
with
the
urine
odors
(Experiment
2a)
than
in
those
with
the
males
(Experi-
ment
1).
(2b.)
Lipid
fraction
of
urine.
Here
a
special
device
for
recording
the
response
to
olfactory
stimuli
in
rodents
was
used
(see
Christiansen,
DOving,
&
MOrk,
1977)
and
the
stimuli
were
from
the
lipid
portion
(dichloromethane
extract)
of
equal
volumes
of
dominant
and
subordinate
male
urine.
Ten
microliters
of
each
of
the
dichloromethane
extracts
was
presented
per
test.
The
stimulus
odors
were
placed
inside
plexiglass
tubes
equipped
with
photocells
which
sense
the
presence
of
the
test-animal's
snout.
The
females
were
tested
in
their
home
cage
and
in
groups
of
five
because
in
pilot
tests
we
found
that
single
females
generally
would
show
a
very
low
frequency
of
approaches
to
the
apparatus.
Twelve
female
groups
were
tested;
the
test
period
for
six
of
these
was
2
hr,
and
for
the
other
six
groups
it
was
16
hr
(overnight
1700-900).
Results.
All
the
groups
approached
the
detecting
unit
with
the
extract
of
dominant
male
urine
more
often
than
they
did
the
unit
with
extract
of
subordinate
male
urine.
However,
for
one
group
tested
for
only
2
hr,
the
total
number
of
approaches
was
very
small.
Therefore
this
group
was
omitted.
For
the
remaining
11
groups,
p
<
.01.
For
the
groups
tested
overnight,
p
<
.05.
DISCUSSION
(1.)
Factors
Determining
Female
Choice
There
are
two
aspects
to
female
choice:
(a)
the
stimuli
provided
by
the
choice
objects,
and
(b)
the
motivational
state
of
the
female.
(a)
Female
preference
for
the
dominant
males
over
the
subordinates
was
more
clear-cut
than
preference
between
the
urine
spots
from
these
males.
This
must
be
due
to
the
more
composite
stimulation
offered
by
the
males.
Male
ultrasonic
vocalizations
possibly
occurred
(Geyer,
McIntosh,
&
Barfield,
1978;
Sales
&
Pye,
1974)
and
in
laboratory
mice
such
sound
emissions
may
show
correlations
with
social
dominance
(Nyby,
Dizinno,
&
Whitney,
1976).
This
is
also
the
case
with
composite
body
odors.
The
ability
of
rats
and
mice
to
discriminate
between
the
body
odors
of
dominant
and
subordinate
males
(Krames,
Carr
&
Bergman,
1969;
Carr,
Martorano,
&
Krames,
1970)
is
attributed
to
a
difference
in
hormone
secretion
with
higher
androgen
levels
in
the
dominants
and
FEMALE
BANK
VOLE
MATE
CHOICE
185
possibly
higher
adrenal
corticosteroid
levels
in
subordinates
(Brown,
1979).
A
similar
situation
is
presumed
for
the
bank
vole.
Concerning
odors
in
the
urine
of
males
the
choice
by
the
females
was
between
equal
quantities
of
urine
from
dominant
and
subordinate
males
collected
in
metabolism
cages.
The
female's
preference
therefore
was
not
due
to
a
difference
in
quantity
of
urine
as
might
come
from
the
higher
frequency
of
urine
marking
by
dominant
males
(Hoffmeyer
in
preparation);
but
the
preference
indicates
differences
between
the
odors
of
urine
per
se
from
dominant
and
subordinate
males.
The results
correspond
to
findings
in
laboratory
mice
(Jones
&
Nowell,
1974)
and
brown
lemmings
(Huck,
Banks,
&
Want,
1981).
Also
male
bank
voles
react
differently
to
the
two
types
of
urine
(Hoffmeyer
in
preparation).
The
difference
in
odors
of
the
urine
from
dominant
and
subordinate
males
may
result
from
several
things.
Dominant
males
generally
have
higher
testosterone
levels
than
subordinate
males.
This
may
affect
their
urine
odors
directly
and
indirectly
through
a
greater
concentration
of
androgen
derivatives
or
exudates
in
the
urine
from
a
higher
metabolic
rate
(Stoddart,
1980),
or
by
acting
on
scent
glands,
the
secretions
of
which
are
added
to
the
urine,
possibly
already
from
glandular
tissue
in
the
kidneys.
The
urinary
factors
may
be
of
the
kind,
which
advance
the
onset
of
female
puberty
in
mice
since
urine
from
dominant
male
mice
was
found
to
be
more
effective
in
stimulating
female
maturation
than
was
urine
from
subordinate
males
(Lombardi
&
Vandenbergh,
1977).
Bronson
(1976)
has
suggested
that
in
mice
secretions
from
the
preputial
glands
are
added
to
the
urine.
If
the
secretions
are
added
continually
to
all
urine
eliminated
by
a
male,
a
higher
rate
of
production
by
the
preputial
glands
of
dominant
males
(indicated
by
the
larger
size
of
these
glands,
p)
should
lead
to
higher
concentrations
of
glandular
secretion
in
their
metabolic
urine,
as
there
seems
to
be
no
difference
in
the
quantities
of
urine
excreted
by
dominant
and
subordinate
males
(Desjardins,
Maruniak,
&
Bronson,
1973,
Mus
musculus;
Hoffmeyer
unpublished,
Clethrionomys
glareolus).
Glandular
secretions
could
be
added
to
the
urine
specifically
during
urine
marking.
Christiansen
(1980)
has
suggested
that
in
the
bank
vole
preputial
secretions
are
deposited
by
males
in
the
special
"trace-urina-
tions",
which
according
to
my
own
results
are
much
more
frequent
in
dominant
than
in
subordinate
male
bank
voles.
The
papers
by
Christiansen
suggest
a
dual
function
of
the
preputial
glands.
Besides
the
hypothesis
of
a
sex
attractant
function
the
scent
of
preputial
secretions
may
signal
aggression/teritoriality/social
dominance,
as
originally
suggested
by
Brown
and
Williams
(1972)
in
their
monograph.
This
could
also
explain
the
interest
that
females
show
in
preputial
odors
of
their
own
sex.
Whatever
the
cause,
the
stronger
effects
of
the
urine
per
se
from
dominant
males
found
here
with
voided
metabolic
urine
will
be
enhanced
by
the
higher
urinary
marking
frequency
of
these
animals.
If,
furthermore,
186
INGE
HOFFMEYER
some
specific
attractant
is
added
during
marking
only,
and
perhaps
just
with
special
types
of
urinations,
female
interest
should
become
more
pronounced
by
using
extracts
of
marking
urinations
from
dominant
males
instead
of
the
urine
collected
in
metabolism
cages
or
bladder
urine.
Behavioral
tests
and
chemical
analyses
are
in
process
concerning
this
question.
(b)
Factors
influencing
female
preferences
are
the
hormonal
state
and
experience
of
the
females
(e.g.,
Doty,
1972;
Nevo,
Bodmer,
&
Heth,
1976;
Caroom
&
Bronson,
1971;
Hayashi,
1979).
In
the
present
experiments,
all
the
female
bank
voles
were
estrogen
treated.
The
hormonal
control
of
female
preference
is
unclear
(Brown,
1979)
but
naive
females
have
to
be
receptive
before
they
show
a
preference
for
male
urine
odor
(Carr,
Loeb,
&
Dissinger,
1965,
for
rats;
Jones
&
Nowell,
1974,
for
mice),
and
estrogen
may
enhance
the
interest
in
odor
from
male
preputial
glands
in
ovariectomized
female
mice
(Bronson,
1976).
The
female
bank
voles
had
no
sexual
experience,
but
had
been
living
with
their
mother,
father,
and
brothers
until
the
age
of
weaning.
Sexual
experience
does
not
seem
to
be
necessary
for
female
mice
or
rats
to
show
preferences
for
the
urine
odors
of
sexually
active
males
over
those
of
castrated
males
(review
by
Brown,
1979),
but
it
enhances
their
preference
for
odor
from
male
preputial
glands
(Caroom
&
Bronson,
1971).
However,
also,
juvenile
experience
with
the
mother's
odors
may
determine
female
preference
for
preputial
odors
(Hayashi,
1979).
It
did
not
seem
to
matter
that
the
female
bank
voles
were
not
familiar
with
the
males
used.
(2.)
Possible
Biological
Functions
Females
may
play
an
active
role
during
mate
seeking
(Mazdzer,
Capone,
&
Drickamer,
1976)
and
possibly
also
with
mate
choice
in
polygynous
mating
systems
(Orians,
1969;
Kleiman,
1977).
Female
preference
for
a
dominant
male
may
increase
her
chances
of
successful
reproduction
in
several
respects.
Obviously,
a
female
might
(perceptually)
combine
social
dominance
and
sexual
attraction
signals,
as
they
are
possibly
two
aspects
of
the
trait.
In
natural
populations
a
mechanism
of
female
choice
may
be
particularly
important
for
dispersing
females.
It
assists
to
increase
the
contribution
of
dominant
males
to
the
gene
pool.
In
consideration
of
the
fact
that
the
dominant
males
used
in
the
present
experiments
had
all
been
identified
through
their
aggressiveness
to
strange
male
intruders,
studies
concerning
the
heritability
of
aggression
in
this
small
rodent
species
are
suggested
for
future
research.
Sexual
selection
in
visually
oriented
animals
like
birds
results
in
dif-
ferences
between
males
in
coloration
and
structures
used
in
displays.
Many
mammals
for
which
olfaction
is
important
may
depend
on
differences
in
male
odor
(Blaustein,
1980).
This
is
suggested
by
differences
in
scent-
gland
size
between
males
found
in
many
mammal
species
(Mykytowycz
FEMALE
BANK
VOLE
MATE
CHOICE
187
&
Dudzinski,
1966;
Bronson
&
Marsden,
1973;
Gustafsson
et
al.,
1980).
Tests
on
female
preference
between
the
odors
from
males
of
different
social
status
(Jones
&
Nowell,
1974;
Huck
et
al.,
1981;
and
the
present
bank vole
results)
provide
some
evidence
of
the
role
of
male
odor
in
intersexual
selection.
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in
cyclic
subarctic
populations
of
the
voles
Clethrionomys
rufocanus
(Sund.)
and
Microtus
agrestis
(L.).
Annales
Zoologici
Fennici,
14,
53-93.