BIOLOGY OF REPRODUCTION 22, 192—196(1980)
Infanticide and PregnancyFailure: Reproductive Strategiesin the Female
Collared Lemming (Dicrostonyx groenlandicus)
FRANK F. MALLORY'
Department
and RONALD J. BROOKS
of Zoology,
University
of Guelph,
Guelph, Ontario, Canada N1G 2W1
ABSTRACT
Inseminated female collared lemmings were exposed to strange males, stud males and changes
in the physical environment
during gestation.
In addition,
strange, nonpregnant
females were intro -
duced into the cages of maternal females and neonates on Days 1 and 3 postpartum. Strange males
significantly
postcoitum,
reduced
whereas
the incidence of pregnancy when introduced into the female's cage on Day 4
stud males did not. Handling 3 times during gestation also significantly lim
ited the success of pregnancy. The incidence of infanticide was significantly greater (77%) on Day
1 postpartum compared with Day 3 postpartum (49%) when strange females were introduced into
the home cage of maternal females. Body weight of maternal females appears to be a significant
factor influencing pup survival on Day 1, but not on Day 3 postpartum.
they apply to current population theories.
INTRODUCTION
Mallory and Brooks (1978) first demon
strated that strange male Dicrostonyx
groen landicus present in the nest area shortly after
parturition
severely
reduced
the
postpartum
survival of young. In that study, the incidence
of infanticide was highest on Day 1 postpartum
(36.7—50%
of neonates
killed) and significantly
lower on Day 3 postpartum
(12.8% of neonates
killed). Stud males never killed offspring sired
by themselves.
The present study is an attempt to further
our understanding
of the interrelationships
be
tween
individuals
of this
ence fetal and neonate
effects
of
handling
species,
as they
influ
survival. In addition,
during
the
latter
the
part
of
gestation were studied, because breeding colony
data indicated that gravid females whose cages
were cleaned had fewer litters.
The reproductive
success of female rodents
has been shown to be highly susceptible to
social
and
environmental
disturbances.
Preg
The data are discussed
as
ford, 1971), M. ochrogaster
(Stehn and Rich
mond,
1975)
and Clethrionomys
glareolus
(Clarke and Clulow, 1973). Changes in the
physical environment also produce a decrease in
pregnancy rates in M. musculus (Chipman and
Fox, 1966) and P. maniculatus (Eleftheriou
et
a!., 1962). In addition, strange males present in
the nest area shortly after parturition
severely
reduce the postpartum
survival of young in M.
musculus (Gandelman,
1973).
This paper reports the effects of strange
males, stud males, and changes in the physical
environment
on pregnancy
in D. groenlandicus.
In addition, incidence of infanticide, caused by
strange, nonpregnant,
nonlactating
female 1cm mings is documented
and the results are dis
cussed in relation to reproductive strategies and
population dynamics of this species.
MATERIALS
AND METHODS
Mature lemmings, bred from stock trapped during
several years at Churchill, Manitoba and Eskimo Point,
nancy blockage by strange males was demon strated in Mus musculus (Bruce, 1959), Pero myscus maniculatus
(Bronson and Eleftheriou,
N.W.T., Canada
1963),
Microtus
1968),
M. pennsylvanicus
Purina guinea pig ration were supplied ad libitum and
temperature
(17 ±2°C) and light (22L:2D) were con
trolled.
In the first experiment, each female was placed in a
agrestis
(Clulow
and
(Clulow
Clarke,
and Lang
were used in these experiments.
The
animals were weaned at 30 days of age and housed in
pairs of the same sex in polycarbonate
cages (36 X 30
x 16cm)provided
withcorngritsubstrate.
Water
and
clean polycarbonate cage (50 X 39 X 21 cm) with a
Accepted October 12, 1979.
Received February 28, 1979.
1 Present
Laurier
3C5.
address:
University,
Department
Waterloo,
male for 7 days. The male was then removed
of
Biology,
Ontario,
Canada
Wilfrid
N2L
and the
female was left undisturbed until the end of gestation.
At parturition, 32 females with litters were placed
randomly into 2 treatments (Table 1). In treatment A,
each female and her litter were exposed to a strange
192
INFANTICIDE AND PREGNANCY BLOCKAGE IN FEMALE LEMMINGS
(i.e., not having previously been with the maternal
female), nonpregnant, nonlactating female for 24 h on
Day 1 postpartum. In treatment B, each female and
litter were exposed to similar conditions on Day 3
postpartum.
The number
of live young were recorded
before and after the strange female was introduced
and interactions were observed for the first 30 mm of
each replicate. Both females were weighed to the
nearest gram prior to being placed together.
In the second experiment, each female was placed
in a clean cage with a male (hereafter referred to as the
stud male). Stud males were kept with receptive fe
males for 24 h after coitus was observed. Forty-eight
mated females were then randomly distributed into 3
treatments
(Table 2). In the control
treatment
(A), the
females were left undisturbed (they were not handled
or exposed to other animals, nor were their cages
changed)
until
the end of the experiment.
In treat
ment B, the stud male was reintroduced into the cage
of the female for a further 24 h on Day 4 postcoitum,
and in treatment C, a strange male (a male which had
not previously mated with the female) was introduced
for a 24 h period on Day 4 postcoitum. In all treat
ments, the number of pregnancies terminating in suc
cessful parrurition
was recorded.
In the third experiment, 40 females were placed in dividually
in clean cages (50 X 39 X 21 cm) with a stud
male for 7 days. At the end of this period, stud males
were removed and the females were placed randomly
into 2 treatments (Table 2). In control treatment A, the
females were left undisturbed
until the end of the exper -
iment and in treatment B, the females were handled
(picked up and held gently) for a period of 30 sec on 3
different days during the remaining gestation period.
Thenumberof litters produced in the 2 treatment groups
was recorded. Data from all 3 experiments were com pared by x2 analysis and Student's t tests.
RESULTS
In the first experiment, strange, nonpregnant
females
were
attacked
immediately
when
placed with a female and her litter on Days 1
and 3 postpartum
and fighting usually lasted
for the entire 24 h period. Fighting was intense.
Two maternal females and 2 strange females
were killed on Day 1 postpartum and 2 strange
females were killed on Day 3 postpartum.
In
both treatments,
more than 48% of the pups
were killed and in all instances this mortality
was caused by strange females, usually within
the first 30 mm after they were introduced into
the maternal female's home cage.
A significant difference in the number of
young killed (Table 1) was observed between
Days 1—3postpartum
0(2 = 7.16; P<0.01). In
both treatments,
strange females killed pups by
biting
them
in the head
region.
Cannibalization
of dead pups was not observed. Maternal fe
males were never observed killing the young,
although they licked pups that were bleeding
and often carried them to other corners of the
cage.
193
The mean weight of maternal females in all
situations was heavier than the mean weight of
strange females. Differences
in body weight
between
maternal
and strange females were
compared when all young were killed and when
some young survived. On Day 1 postpartum the
mean difference
in body weight, between
maternal and strange females, when all young
were killed was 12.76 ±7.06 g (mean ±SEM,
n = 12). This difference was not significant (t =
1.81; P>0.05).
In
young survived, the
±13 .29 g (n = 4),
3 .3 9; P< 0.05). On
nificance
was
those instances when some
mean difference was 45.00
which was significant (t =
Day 3 postpartum,
no sig
found
in the
mean
difference
body
weight,
when all young
(18.41 ±10.22 g; n = 7, t = 1.80;
when some young survived (6.56
n = 9, t = 0.49; P>0.05).
When estrous females and stud
caged
together,
some
initial
in
were killed
P>0.05), or
±1 3.47 g;
males were
fighting
was
ob
served; however this usually changed quickly
into the typical sniffing and chasing bouts as
described by Banks (1968) and Brooks and
Banks (1973) and often resulted in copulation.
When stud males were reintroduced
to the fe
male's cage on Day 4 postcoitum, females most
often
attacked
immediately
; however,
once
contact was made, the male was accepted and
no further fighting was observed. In contrast,
strange males, placed with inseminated females
on Day 4 postcoitum,
were immediately
at
tacked
and this incompatibility
frequently
lasted for the entire 24 h period. No mortality
was observed.
No significantdifference(x2
was observed
nancies
between
treatment
“¿-I 70%
B (stud
of
= 0.16;P>0.05)
in the number
pregnant
treatment
male)
of successful preg
A
(control)
and in both
animals
and
treatments
produced
litters
(Table 2). However, when a strange male was
introduced on Day 4 (treatment C), the propor
tion of successful pregnancies fell dramatically
to 13%. A 3 x 2 X2 test indicated a significant
difference
in pregnancy
success when treat
ments A, B and C were compared separately
(x2 15.19;P<0.001).
In the third experiment,
of 20 females han
dled during gestation, only 2 produced litters,
one of which
was killed by
a few hours after parturition.
the female
Thirteen
within
of the
20 females left undisturbed
produced
litters
(Table 2) and all pups survived until weaning.
This difference
in the number of successful
MALLORY
194
AND BROOKS
TABLE 1. Differences in neonate mortality induced by strange, nonpregnant, nonlactating females, on Days 1
and 3 postpartum.
Littersn
Treatment1n
femaleA.Day
Young
surviving
to weaning%
Youngn
Litters with
some neonates
killed%
Young killed
by strange
1 postpartum:
female1650a109477B.Day
strange, nonpregnant
3 postpartum:
strange, nonpregnant female1646225649
aTen pups died before weaning (7 in treatment A, 3 in treatment B) and were not killed directly by the
strange female.
Number of young killed was significantly different (x2 = 7.16; P<0.01) between treatments.
pregnancies
was
significant
0(2
12.90;
P<OMO1).
period. On Day 3 postpartum,
body weight were not significant
it apparently
DISCUSSION
Infanticide,
directed towards the young of
other conspecifics,
can have obvious selective
advantages
for an individual
(Mallory and
Brooks, 1978). In the present study, strange
females killed significantly fewer young on Day
3 than Day 1 postpartum.
The lower level of
pup killing on Day 3 postpartum is presumably
due to an increase in postpartum
aggression in
maternal females (Mallory and Brooks, 1978).
Differences in body weight between maternal
and strange females supported this conclusion.
On Day 1 postpartum,
only maternal females
which were significantly heavier than strange
females, were able to protect some of their off
spring. Therefore, body weight appears to be an
important factor in defending young during this
was
not
a major
differences in
and therefore
factor
affecting
the survival of the young. Because maternal
females that were not significantly heavier than
strange females were able to protect some of
their
young
during
this
period,
increases
in
postpartum
aggression appear to have occurred.
In Mus musculus (St. John and Corning, 1973)
and Rattus norvegicus (Erskine et al., 1978)
postpartum
aggression toward strange conspe
cifics is low just after parturition, but increases
during lactation and peaks from Day 3 to Day
10 postpartum.
In these species a significant in
crease in female aggression towards males after
48 h of nursing, compared with 24 h, supports
the hypothesis that nursing is the stimulus that
induces this behavior (Svare and Gandelman,
1976; Erskine et al., 1978).
Data from this study support the conclusion
that strange, nonpregnant
females are a greater
TABLE 2. Pregnancy success of female collared lemmings in various experimental
Experi
Success2A.Control,
mentTreatmentn
situations (see text for details).
Successful
pregnancies%
Femalesn
undisturbed161275B.Stud
4postcoitum161169C.Strange
male on Day
postcoitum162133A.
male on Day 4
undisturbed
11B.Control,
Handled (3 times) during gestation20
Experiment
2. Number
of successful
pregnancies
265
2013
was significantly
different
between
10
A , B and C (x2 =
15.19; P<0.001) when compared in a 3 X 2 x2 test, but there was no difference between treatments A and B
(x2 0.16; P>0.05).
I S Experiment
(x2
3 .
Number
12.90; P<0.001).
of
successful
pregnancies
was
significantly
different
between
treatments
A
and
B
INFANTICIDE
AND PREGNANCY
threat to maternal females and their litters on
Days 1 and 3 postpartum,
than are strange
males (Mallory and Brooks, 1978). In addition,
as strange females can kill a significant number
of neonates on Day 3 postpartum,
when mater
nal postpartum
aggression is presumed to be
established, it is likely that they are a signifi
cant threat throughout lactation. This contrasts
with strange males (Mallory and Brooks, 1978)
which are only an important threat during the
first 24 h after parturition.
Differences in neonate mortality caused by
strange males and females may represent dif
ferent reproductive
strategies. The advantages
of infanticide
to strange males seem clear
(Mallory and Brooks, 1978). However, if males
are unable to kill young, they can potentially
mate with maternal females and/or other fe
males and have progeny in the next generation.
In addition, as males frequently mate with a
series
of females,
they
may
have
greater
prob -
lems identifying
their own offspring. These
factors could lower strange male aggression
towards offspring, when the risk is high, due to
female aggression. Strange females, on the other
hand, would not have the above options or
problems of recognizing
offspring. They can
not reproduce through other individuals or have
their young survive in unprotected
areas. The
acquisition of a nest site and territory is essen -
tial if females are going to reproduce success
fully. Evidence that female microtines are more
territorial than males, supports this conclusion
(Bujalska,
1973 ; Boonstra,
1977; Madison,
1978; Jannett,
1978; Webster, personal corn
munication).
In
addition,
radiotelemetry
studies have indicated that females move to
new nest sites after weaning litters (Brooks,
unpublished)
and after losing litters to pred ators (Brooks and Banks, 1973). This would
increase
would
usurp
competition
favor
the
for
individuals
territories
available
aggressive
of others.
The
sites
enough
short
and
to
life
BLOCKAGE IN FEMALE LEMMINGS
195
these phenomena
occur in the wild, as sug
gested for M. pennsylvanicus
(Mallory and Clu low, 1977) and that they provide some repro
ductive advantage.
To date, pregnancy block has been found in
many rodent species; however most authors do
not
suggest
any
selective
advantage
for block
age, other than to relate it to avoidance of
inbreeding (Bruce and Parrott, 1960) or to state
simply
that
it may
somehow
regulate
popula
tion numbers. We hypothesize
that pregnancy
blockage is advantageous
to both sexes under
certain
circumstances
For males, there
vantages
in
but
for different
are a number
inducing
reasons.
of selective ad
pregnancy
failure
in
females. A strange male decreases the reproduc tive fitness of other individuals in the popula
tion relative to his own and causes the female
to return to estrus early (Mallory and Clulow,
1977), increasing the likelihood that he will be
able to mate with her. In addition, blockage
decreases the time required for his offspring to
enter the population, as females would not take
the current pregnancy to term prior to mating.
Stud males, on the other hand, may contribute
to their reproductive success by protecting their
own females and offspring from disturbance or
attack
by
strange
males.
Although
male
1cm -
mings maintain
large home ranges which in
dude areas inhabited by several females, there
is only limited or indirect evidence that they
defend these areas (Brooks and Banks, 1971;
Bowen and Brooks, 1978). If this occurs, the
ability of a male to maintain his home range
and protect his females and offspring is prob
ably inversely related to density and becomes
minimal during peak years.
Under demographic
conditions
where the
survival of young would be minima! due to
infanticide
or other extrinsic factors, natural
selection would favor females that lose litters at
an early stage of development,
prior to a great
investment
of energy.
This
reproductive
span and arctic breeding season of this species
strategy
would further necessitate a high and continued
level of aggression by nonterritorial
females
toward maternal females and neonates, even
though the chances of injury would be great.
In these experiments,
incidence of preg
nancy was depressed in females exposed to
strange males or to changes in the external envi
ronment. This did not occur if females were
exposed to stud males or were left undisturbed.
The extreme sensitivity of these animals to
and increase the female's chances of surviving
until better
reproductive
conditions
prevail
(Millar, 1975 ; Pianka, 1976). As reproductive
efficiency
requires that fecundity
be appro
priate to resources likely to be available to
young (Williams, 1975) and, because each pup
weaned may have different reproductive value
(a nonconstant
contribution
to the fitness of
these
factors
makes
it
highly
probable
that
would
the mother)
maximize
energy
conservation
in different population
densities,
the selective advantage of immediate
repro duction
vs delayed
reproduction
probably
196
MALLORY AND BROOKS
depends
upon
current
cal conditions
nancy
failure
demographic
(Williams,
appears
to
and physi
1966).
be one
Thus,
aspect
preg
of a
facultative
response, which allows the female
to maximize her reproductive output in a rapid
ly changing demographic and physical environ
ment.
In
Dicrostonyx,
population
density
fluctuates
greatly from year to year (Krebs,
1963) and there is still no satisfactory explana
tion for this phenomenon
(Mallory and Brooks,
1978). We suggest that the competing repro
ductive strategies of individuals decrease re cruitment
of
young
animals
during
high
densities and ultimately produce a population
with a greater proportion
of older animals.
These density dependent
phenomena
would
reach a climax during peak years and contribute
to a marked decline, due to the normal attrition
of older animals.
ACKNOWLEDGMENTS
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