Multiple exposures to adult males and reproductive activation of virgin female Microtus Ochrogaster

57

Behavioural Processes, 17 (1988) 57-61 Elsevier

MULTIPLE EXPOSURES TO ADULT MALES AND REPRODUCTIVEACTIVATION OF VIRGIN FEMALE MICROTUS OCHROGASTER

Joyce

E. HOFMANNand Lowell

Department Goodwin,

of

Ecology,

Urbana,

(Accepted

6

IL 61801,

May

L.

CETZ

Ethology,

and Evolution,

University

of

Illinois,

505 S.

U.S.A.

1988)

ABSTRACT Hofmann, J. E. and Getz, L. L., reproductive activation of Process. 17: 57-61

1988. virgin

Multiple exposures to adult female Microtus ochrogaster.

males and Behav.

Virgin female Microtus ochrogaster living in family groups were reproductively activated by twelve I-hr exposures over a 3-day period to Reproductive activation among virgin unrelated sexually experienced males. females receiving six or eight exposures over a 2- or j-day period did not differ significantly from that of unexposed control females. Thus, frequent multiple exposures to unfamiliar males (and repeated stimulation by a male urinary chemosignal) can override the reproductive suppression typically experienced by virgin females remaining in family groups. Prairie

KEY WORDS:

vole,

Microtus,

Reproductive

activation

INTRODUCTION The prairie system

vole,

in which

a typical

breeding

pair

observed

in free-living

groups

that

observed

Microtus

and their

form

that

do so

remained

young

remaining

females

and Hof mann , 1986; from

the

natal

Hofmann,

of

72 hrs

of

the

nonbreeding

the

natal

at the et

and paired

with

male-female

groups

prairie

vole;

are

most

(Getz,

rarely

such

unrelated

Unpubl.).

We have and females,

past

and that

nest

the

age of

typically

were

All

1987a).

an adult

68 and 75% of the males

nest

natal

al.,

of

social

periods

populations

is et

of

a male

voles

male

and Stehn,

stimulated

et

al.,

0376-6357/88/%03.50

et

by this 1980,

activated (Carter

et

(Richmond 1976;

by a non-volatile Dluzen

1980;

stimulation

reproductively

prairie

Richmond

al.,

(Carter

chemosignal

female

an unfamiliar

1974;

activation

male

populations

at

virgin

sniffs

Nalbandov,

(Carter

consists

Nonfamily

during

Getz

nest

unit

a monogamous mating

females

became

weaning

nonreproductive

known to

have

reproductive

(Getz

dispersed

(Getz

and

1986).

Estrus genital

social

displays

offspring.

in free-living

respectively,

ochrogaster,

1980;

induced

Getz

et

chemosignal Females if

they

Only 20% of being

stimulated et

when the

and Conaway, Carter

1981).

chemosignal,

1986).

without al.,

al.,

is

al.,

1969;

al., in

the

Getz,

Hasler

and

Reproductive

male

urine

estrus

in the

females

by the 1983;

naso-

1980).

achieve

remain

young

female

presence

become

male

within

urinary

Unpubl.).

0 1988 Elsevier Science Publishers B.V. (Biomedical Division)

24of

a

58

When housed voles

do not

Batzli

et

These

with

their

normally

al.,

females

1977;

they

Carter,

1980;

Gruder-Adams

prairie

voles

may contain

activation that

housed their et

a single

in family nose

al.,

groups

population

Getz,

1986;

sniffing

than

the

in greater

77.1% Getz

multiple to

reproductive

reproductive

father

al.,

siblings

the

suppresses

(Getz

urine

of

and

female

reproductive

Only 21.4%

of

young

chemosignal

or had female

1977;

1976;

1985).

chemosignal

or male

urinary

prairie

and Stehn,

and Cetz,

In addition,

1983).

male

female

estrus-inducing

siblings

et

McGuire

of

al.,

females

1987a).

unfamiliar

that

17.6% of

males (Getz

repeated

experienced activation study

virgin activation

the

females

and were urine

placed

and Getz,

young females

at low population

such

densities

suppression

exposures

female

only

of

et

of

The present

densities.

Cruder-Adams

that

al.,

the

(Batzli

reproductive

We hypothesized

overrides

lead

or with

at low population

1987a).

(Richmond

1985).

et

to

populations

densities

naso-genital

young

active

1981;

on Getz

Unpubl.)

became

and Hofmann,

(Getz

estrus

In free-living family

their

a chemosignal

exposure

groups

achieved

1983;

the

sniff

and Getz,

females

siblings,

1981;

acquire

naso-genital

in other

received

and Getz,

do not

because

and/or

reproductively

McGuire

presumably seldom

parents

become

at high

were reproductively

active

(Getz

Opportunity

for

multiple

by young

females

is

1986;

Getz

and Hofmann, stimulation

young

experimentally female even

prairie though

in

while

by females of

remaining

densities,

from

voles the

to

the

unfamiliar

females

were

of at high

al., males

groups,

at higher

investigated

et

unfamiliar

in family

females

bouts

greater

resulting

population possibility males living

that would

in family

groups. METHODS The prairie voles used in this study were laboratory-reared from stock originally trapped in the vicinity of Urbana, Illinois. For this study family groups consisting of a breeding pair and two successive litters (with at least one female in the older litter) were housed in 37 x 47 cm plastic cages with wood chip bedding. Purina rabbit chow and water were provided ad libitum and Females from the older litter in each family a 15L:9D light cycle maintained. were used either as experimental or control animals when 41-45 days of age. A small patch of fur was clipped on each of these females for individual recognition. Stimulus males were unpaired sexually experienced adults. They were housed individually in 16 x 27 cm plastic cages in the same room in which the family groups were located. Females were removed from the family group cages and placed individually in 23 x 44 cm plastic cages with fresh wood-chip bedding. A stimulus male was introduced into the cage of each experimental female for 1 hr. Behaviour of the voles during the exposure period was observed for occurrence of nasogenital sniffing or mating. Females that were sexually receptive on the first day of an experiment were eliminated from the study since this indicated reproductive activation had occurred prior to experimental stimulation. Control females were similarly isolated from family groups for 1 hr, but were not exposed to unfamiliar males. All females were returned to their family group cages following the 1 hr exposure or isolation.

59

Four groups of females were exposed to males on the following schedules: (1) two males per day for three consecutive days; (2) three males per day for two consecutive days; (3) four males per day for two consecutive days. Females were days ; and (4) four males per day for three consecutive exposed to different males on a given day; sometimes they were placed with the Each day’s exposure periods were separated by at same male on different days. Four groups of control females were isolated for 1 hr periods on least 3 hrs. corresponding schedules. On the afternoon of the day following completion of exposure to males or isolation controls, each female was placed in a 23 x 44 cm cage with an experienced male for 10 min and observed for sexual receptivity. Two additional mating tests were conducted on the next day, one in the morning and one in the evening (48 hrs after the final exposure or isolation period). Following the mating trials all females remained with their family groups for 10 days, after which they were sacrificed using C02, weighed and necropsied. The presence of embryos, if any, or the weight of the uterus of nonpregnant was recorded. Uterine weights were adjusted to a 25-g body weight, females, the approximate weight of an average adult female. Receptivity during a mating trial, pregnancy or an adjusted uterine weight greater than 28 mg indicated that reproductive activation had occurred (Carter et al., 1980). The proportion of reproductively activated experimental and control females for each treatment were compared by chi-square or a Fisher exact test of a 2 x 2 contingency table; the Fisher exact test was used when expected cell frequencies were <5. Differences in uterine weights were compared by the Mann-Whitney U-test (Siegel, 1956). RESULTS AND CONCLUSIONS More experimental all

four

treatments;

only

for

1).

The proportions

three

group

groups

differ of

the

exposed

weights

experimental

of

control

groups

17.5k1.3

mg, respectively. 4 and the

the

0.05

weights

level

The overall eight

exposures

were

similar

male

to

stimulation

to

the

males

those

four

placed

al.,

McGuire

of

that

control

became

housed

with

and Getz,

1981;

regimes

sibling

noses Getz

et

al.,

2,

3 and 4 were

are

in

consistent

(10.3

and

females at

uterine with

activated.

and those

of

Uterine 16.8t1.7

were significant

differences

receiving

and 22.4%. females

females

(21.4%)

The mean

experimental

reproductively

studies

exposures,

16.9t1.8, the

not

was

eight

1,

did

proportion

respectively.

groups

the

activated

in other

on their

in groups

between

females

in the

the

or

(Table

period

P < 0.005).

18.0+1.6,

Thus,

females

six

mg +lSE,

and control

exposure of

observed

and then

urine

females

U-test).

3-day

by 12 exposures

1 d.f.;

3 and 4 were

period

activated

or

However,

receiving

The differences

proportion

a 2-

= 7.97,

experimental

proportions

had female 1980;

2,

became

over

in

significant

a 3-day

that

activated females

(x2

over

P > 0.10).

and 24.7k3.2 1,

other

from

in the

8 hrs

experimental

(Mann-Whitney

resulting

differences

of

group

15.5*1.4

of

group

that

of

to males

2 d.f.;

activated

was statistically

females 6 or

reproductively than

weights

17.1+1.5,

for

= 3.28,

as a single

uterine

15.7f1.6,

12 exposures

males

females

were reproductively

difference

to

greater

when considered

females

the

of

(x2

experimental

significantly

control

receiving

significantly

adjusted

than however,

or

six

respectively)

receiving family

(Batzli

et

1983;

Getz,

al.,

or

groups 1977;

Unpubl.).

a single or Carter

that et

60

Table 1. Reproductive activation provided multiple 1-hr exposures males. The number that mated is design.

Group

(Exposures)

Experimental No. Activated

N 1 (2/day,3

days) days) days) days)

2 (3/day,2 3 (Q/day,2

4 (Q/day,3

*Chi

21 24 22

6(5) 7(6) 2(2)

25

14(12)

Exact

Controls No. Activated

N

28.6 29.2 9.1

20 23 23

56.0

22

sig. %

3(l) 3(O)

p>o.4* p>o.3* P=o .61** P
15.0 13.0

l(1) 2(2)

4.11 9.1

Test

The proportion unfamiliar

than,

high

record

the

during

this

a level

of

in the

that

Hofmann,

1986;

Getz

of

high

most for

in the

prairie

of et

the

remains,

young

unpaired

young males also

females: of

do not 14 of

the

explain

within very et

family

rapid

al.,

social

groups;

population

growth

as

when there (Cetz

effects

and of

of

observed

males

such

groups

level

in population

unfamiliar

of

males,

suppressive

increased

has been

if

activation

social

achieve

during

density

may be

reproductively

this that

may,

in part,

frequently

occur

1987b).

however, paired

adjacent

as to

which

males

adult

males

of

social

know which females

that

Increases with

the the

to

determine

densities, of

not

population

unfamiliar

population

during

males

necessary

in the

of

was less

We did

unfamiliar

was to

home range

females

groups

at high

to

can overrride

density.

of

result

high

could

encounters

(Getz

the

All

1987a),

among young

periods vole

would

the

family

in

respectively).

that

study

The level period

exposures

to

exposures

of

into

This

young females

activate

We

periods

al.,

of

exposures

a 3-day

with

this

multiple

males

groups.

population

The question

females.

frequent

when frequent

account

males.

males

activation

accelerated

of

groups.

over

encounters

comparable

eight

(17.6%).

living

frequency

in family

during

in family

the

or

in free-living

density

and 77.12,

of

unfamiliar

incursion

reproductive

activate

that

may occur

remaining

(56.0

The purpose

to

observed

young females

activation

living

increased

for

determine

field.

exposures

We conclude

periods

or

that

by six

by 12 exposures

number or duration

study

females

to

low population

density

reproductive

densities

those

that

were activated

similar of

population

actual

that

produced

approached,

of

virgin

periods

activation

but

multiple

females

was also

during

reproductive

periods

of

males

populations

is

B

square

**Fisher

to

of virgin female Microtus ochrogaster when to unfamiliar sexually experienced adult in parentheses. See text for experimental

males

that

groups

or wandering

mate with

became

in the

adjacent

the

pregnant

population social unpaired

reproductively during

groups,

this

adult activated

study

had

61

been

observed

However, males not

it

within

mate,

mating

either

also

possible

is

their

males

are

with that

families.

activated

and laboratory

observations

some of

Although

capable

reproductively

stimulus

of

mating

(McGuire will

males

or during

these

females

were

housed

together

siblings with

sibling

and Getz,

1981).

be necessary

to

a mating

females

typically

that

Additional answer

these

test.

impregnated

have field

by do

been studies

questions.

ACKNOWLEDGEMENTS This

study

was supported

by NIH Grant

HD09328 to

LLG.

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