Behavioral Ecology Vol. 10 No. 5: 592-597
© 1999 International Society for Behavioral Ecology
Male-caused failure of female reproduction and its adaptive value in alpine marmots (Marmota marmota)
Research Institute of Wildlife Ecology, University of Veterinary Medicine, Savoyenstr. 1, A-1160 Vienna, Austria
Address correspondence to K. Hackländer. E-mail: Klaus.Hacklaender{at}vu-wien.ac.at .
Received 6 October 1998; revised 12 February 1999; accepted 3 March 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We studied reproductive performance of free-living alpine marmots (Marmota marmota) for 14 years in the National Park of Berchtesgaden, Germany. Female reproduction was influenced by body condition and social factors. Reproduction depleted fat reserves, and only females emerging from hibernation with sufficient body mass were able to reproduce successfully. Marmots lived in social groups in territories defended by a dominant male and female. Subordinate females never reproduced, regardless of body mass. Territory takeovers by males impaired reproduction of dominant females, but only if the takeover occurred after the mating period. Reproductive failures occurred despite clear signs of pregnancy such enlarged nipples or late molt. Decreasing progesterone levels after the mating period and the lack of evidence for direct infanticide by new territorial males suggest a block of pregnancy as a likely explanation for reproductive failures in groups with male takeovers during gestation. Rendering female reproduction impossible increased future reproductive success of new territory owners. Nonparous females saved the energetic cost of maternal investment and thus emerged with higher body mass in the following spring. In line with this, females failing to wean young had higher reproductive success in the subsequent year.
Key words: Bruce effect, females, infanticide, Marmota marmota, marmots, reproductive failure, reproductive suppression.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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There is an ever growing number of reports on the occurrence of infanticide in mammals (Hausfater and Hrdy, 1984
; Smuts and Smuts,
1993), especially in rodent species
(Labov et al., 1985).
Particularly among ground-dwelling sciurids, infanticide seems to be a common
male behavior (Blumstein,
1997; Coulon et al.,
1995; Dobson and Kjellgaard,
1985; Hoogland,
1985; McLean,
1983; Perrin et al.,
1994; Sherman,
1982; Steiner,
1972; Vestal,
1991). Males taking over a territory or social group are
especially likely to kill the present offspring. Apart from this classical
type of direct infanticide, there is another possibility for males to
manipulate female reproduction. Bruce
(1959) first reported that the
presence of an unfamiliar male can lead to a block of gestation in pregnant
mice. This "Bruce effect" has been found to exist in several
rodent species (Huck, 1984;
Schwagmeyer, 1979), primates
(e.g., Mori and Dunbar, 1985),
and wild horses (Berger, 1983).
Presumably male pheromones, for example, from urine, elicit the abortion or
resorption of embryos (Hafer,
1990; Keverne,
1983; Storey,
1990).
Most authors considered male-caused failure of female reproduction an
adaptive male strategy instead of assuming an accidental or pathological
origin (review in Hrdy, 1979).
Essentially, it has been suggested that females start the next reproductive
episode earlier if the current period of maternal investment is interrupted.
Therefore, males killing dependent juveniles sired by other males or blocking
such gestations can reproduce earlier and thereby increase their lifetime
reproductive success. However, in contrast to many descriptive reports,
theoretical models (Breden and Hausfater,
1990; Glass et al.,
1985), and experimental work in the laboratory (review in
Brooks, 1984), data on the
adaptive value of direct or indirect infanticide in free-ranging mammals are
rare (e.g., Dorges et al.,
1992; Packer et al.,
1990). Reasons are the lack of long-term observations of known
individuals, insufficient knowledge about the relationships among these
individuals (Brooks, 1984),
and the difficulty of observing infanticide in the field, especially in
burrow-dwelling rodents (Labov,
1984).
In contrast to the widely accepted and empirically supported view that
infanticide can be advantageous for males, the situation is less clear from
the female's point of view. At first glance, a conflict of interest should
exist, because infanticide implies a waste of reproductive investment for
females. In the case of direct infanticide, females may just not be able to
defend their offspring, because of the difference in physical strength between
males and females (e.g., in lions: Packer
et al., 1990). However, this constraint argument cannot explain
why females volunteer in the case of indirect infanticide. There must be a net
fitness benefit for females for a Bruce effect to evolve. The common argument
is that females may anticipate that a new male will be infanticidal or that it
will not provide paternal care. Females therefore should do better by
interrupting the current reproductive cycle immediately after a male takeover
to minimize the inevitable loss of reproductive investment
(Huck, 1984;
Schwagmeyer, 1979).
Furthermore, subsequent reproduction may even be improved after a pause in
species that depend on body fat reserves for reproduction (e.g.,
Andersen et al., 1976;
Grizzel, 1955;
Rogers, 1976;
Samson and Huot, 1995;
Snyder et al., 1961). Although
these arguments are logical, there is virtually no evidence from field studies
that females indeed make the best of a bad job by interrupting gestation after
a male takeover.
We report in this paper increased reproductive failures of females after territory takeovers by males in a free-ranging, highly social ground squirrel, the alpine marmot. We further present evidence suggesting that reproductive failures may be caused by pregnancy blocks and demonstrate the adaptive value of male-caused failures in female reproduction in this species for both sexes.
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MATERIALS AND METHODS |
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Study animals and site
Alpine marmots (Marmota marmota) are large, herbivorous sciurids that are common in the Alps, the western Caparthians, the Tatra Mountains, and the Pyrenees. They occur on alpine meadows from 900 m up to 3200 m above sea level (Krapp, 1978
). Alpine
marmots typically live in family groups consisting of a dominant, territorial
pair and several subordinate members up to 5 years old
(Arnold, 1990b;
Lenti Boero, 1994;
Perrin et al., 1993). Female
alpine marmots are monoestrous. They mate within approximately 2 weeks after
emergence from hibernation in April. A gestation period of 34 days is followed
by a lactation period of about 40 days. Juveniles are weaned around the
beginning of July, the time when they first emerge from the natal burrow
(Psenner, 1956,
1960). However, only dominant
females reproduce successfully (Arnold,
1990b;
Hackländer
et al., 1998).
We studied alpine marmots from 1982 to 1996 in the National Park of
Berchtesgaden, Germany (47°36' N, 13°0' E, 1100-1500 m
above sea level). Marmots were captured with live-traps (National Live Trap
Corp., Tomahawk, Wisconsin.) throughout their active season from April to
September. Each year we trapped about 95% of all animals on the study site of
approximately 1 km2, most of them twice. Traps were checked at
least every other hour. Captured animals were transferred into a cone-shaped,
cotton handling-bag, weighed to the nearest 50 g with a hand-held spring
balance (Pesola, Switzerland), dye marked (Nyanzol D), and tattooed upon first
capture for permanent identification (for details, see
Arnold, 1990a,
b).
Assessment of territory takeovers and female reproductive
success
Trapping and observations of marked animals with binoculars (10x50,
Leica, Germany) during daily rounds in the study area provided comprehensive
information on composition and changes of about 20 study groups per year. New
dominant males within a group were recognized by their dye-mark, their
distinct social and territorial behavior, and by the disappearance of the
former territorial male. New territory owners usually expelled the former
territorial males immediately after winning the fight over the territorial
position. In six cases the intruding male was apparently not competitively
superior to the old territory owner, and both remained in the group up to 2
years. We discarded these groups with unclear dominance relationships among
males from analysis. Furthermore, we considered groups with male territory
takeovers only when the new territory owners arrived before the emergence of
juveniles and held their status at least during the next but one reproductive
season.
Most juveniles were trapped within 10 days after first emergence from the
natal burrow. Within this time span, it is possible to identify littermates
and the mother with certainty because juveniles still remain in close
proximity to the natal burrow (Arnold,
1990a). Females producing weaned young are called parous, others
are nonparous.
Endocrinological analysis
From 1988 to 1996 we collected blood samples from the saphenal vein for
endocrinological and paternity analysis. We took 4 ml blood within
approximately 5 min after approaching the trap and added anticoagulant (EDTA)
to the blood sample. Within 2 h, samples were centrifuged to separate plasma
and solid fraction and stored in dry ice in the field, and then later stored
in the laboratory at -70°C.
Plasma progesterone (P4) was analyzed by enzyme immunoassays. We extracted
300 µl plasma in 5 ml of diethylether by shaking (30 min). After storing at
-20°C, the ether was transferred to a new vial and evaporated (40°C),
the residue reconstituted with assay buffer, and analyzed (for details, see
Bamberg et al., 1991). Mean
recovery rate of progesterone was about 90%; intra- and interassay
coefficients of variation varied between 10% and 15%.
Statistical analysis
For statistical analyses we used SPSS for Windows, Release 7.5 (SPSS Inc.).
Parametric tests were applied whenever the necessary preconditions were
fulfilled. Sample sizes between tables and figures may differ due to variable
trapping success.
Paired comparisons of mass data were performed after averaging data from repeated measurements of individuals for years with and without production of weaned young.
For investigating the course of progesterone titers during the time window
of gestation among parous females, we drew 63 blood samples from 35
individuals. As progesterone titers did not differ significantly among these
subjects (H test, 
2 = 35.25, df = 34, p
=.409), we considered samples as the appropriate statistically independent
units for comparing parous females with territorial females from groups with
male takeovers (Figure 1).
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RESULTS |
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The effect of male territory takeovers on female reproduction
We totally detected 21 territory takeovers. Eight of them occurred during the mating period in April. These early changes of the territorial male had no significant influence on female reproduction. Four of the eight territorial females reproduced successfully, which is similar to the average fecundity of territorial females of 64% (Table 1).
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Most of male territory takeovers took place after the mating period and before the end of lactation (13 of 21). As expected from the average fecundity of territorial females, 8 of these 13 territorial females should have weaned young, but only 1 of them reproduced successfully. This is a significantly reduced reproductive rate (p <.001).
Mechanisms of reproductive failure
In none of the reported cases of reproductive failure after a change of the
territorial male did we obtain evidence of direct infanticide. We never found
injured juveniles or carcasses, nor did we observe fights between the new
territorial male and the territorial female. For five territorial females that
did not wean any young after a territory takeover, we have further evidence
that they indeed attempted to reproduce, because they were trapped during the
typical time window of advanced gestation or observed later in the season. All
of them either had enlarged nipples, or molted late during July/August like
dams. In contrast, clearly nonparous females always had little nipples and
molted simultaneously with males during June.
Progesterone in parous territorial females remained high from the mating
period until the approximate time of littering
(Figure 1). Progesterone data
were also available from six territorial females failing to reproduce after a
male takeover. Two values matched the pattern found in parous females (gray
squares in Figure 1) and came
from a female that lived in a group where the new dominant male took over on
June 13 (i.e., certainly after the typical period of littering in alpine
marmots). In contrast to parous females, progesterone concentrations of the
remaining five females seemed to decrease during the time window of gestation
from initially high levels (Figure
1), indicating either a failure to conceive or a block of
gestation. One should not overestimate this borderline significant difference
because the sample of territorial females from groups with male takeovers is
rather small, and exceptionally low levels of progesterone have been found in
parous females as well (Figure
1). Low levels may be due to sampling outside of the period of
gestation because we did not know the exact time of conception and
parturition, or due to the fact that progesterone secretion between pregnant
individuals can vary substantially
(Concannon et al., 1984;
Sinha Hikim et al., 1991).
However, the course of progesterone in the two groups of females is certainly
not contradictory to the view that reproductive failures after male takeovers
were caused by block of gestation.
Body mass and reproduction
Sufficient vernal body mass (body mass measured within 14 days after
emergence from hibernation) was apparently mandatory for successful
reproduction in females. In groups without male takeovers, emergence body mass
of territorial females was on average 141 g (SD = 182 g) higher in years with
successful reproduction than in years when the same individuals did not wean
young (t test for paired comparisons, t = -4.043, df = 26,
p <.001, see also Figure
2). However, vernal body mass of territorial females from groups
with male takeovers during the time window of gestation corresponded to the
grand mean of parous and nonparous females
(Figure 2). Therefore, one
would expect that their reproductive rate should approximate the population
mean as well (64%; Table 1). Hence, other reasons than condition must have been responsible for the
reproductive failure of these females. Logistic regression analysis revealed
that a male takeover during gestation was such a reason for reproductive
failure of territorial females. Independent of the positive effect of vernal
body mass on reproduction (logistic partial correlation statistic R
=.165, p =.003, n = 181), a change of the territorial male
after the mating season significantly decreased the probability that a
territorial female produced weaned young (R = -.163, p
=.004).
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Maternal effort and future reproduction
The energetic consequences of reproduction influenced future reproduction.
Female vernal body mass was on average 177 g (SD = 272 g) lower after a year
of reproduction (t test for paired comparisons, t = -2.759,
df = 17, p =.013) than after years when the same females failed to
wean young. Apparently, the annual energetic demands of reproducing females
exceeded the amount of body fat that could be accumulated during one summer,
due to the additional costs for gestation/lactation and the cost of warming
juveniles during winter (Arnold,
1993). Without the burden of maternal investment, females not only
reestablished their energy reserves during summer to meet the energetic
requirements for the next hibernation, but emerged in the subsequent spring
with higher body masses compared to the previous spring
(Figure 3). The difference of
vernal body mass from year to year, a measure of the body fat reserves
available after hibernation, was positive in nonparous but negative in parous
females, and significantly influenced the next reproductive output
(Table 2). Parous females were
less likely to produce a litter in the following year (56% of 110) than
pausing females (69% of 81, 2 = 3.22, df = 1, one-tailed
p =.036).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Mechanisms of female reproductive failure
Alpine marmots typically emerge from hibernation before the thaw is completed, and no food is available for up to 53 days after emergence (median 16 days; Arnold, 1990a
). Hence,
the energetic cost of reproduction must to a considerable degree be paid from
the fat reserves that remained after hibernation. Many females apparently
emerged with an insufficient vernal body mass to fulfill these requirements
and forfeited reproduction in order to replenish their fat reserves.
Besides body condition, social relations within and between the sexes
influenced female reproduction. In line with previous reports
(Arnold, 1990a;
Lenti Boero, 1994;
Perrin et al., 1993), we never
found more than one reproductive female per group in our study, and this was
without any doubt the dominant, territorial female (exceptions under
conditions of unclear dominance; Barash,
1976; Goossens et al.,
1998). Three-year-old and older subordinate females did not show
any signs of lactation and never weaned young, although they emerged with body
masses similar to those of successfully reproducing territorial females.
However, we frequently noticed signs of estrus and gestation in subordinate
females and sometimes observed copulations. Therefore, territorial females are
apparently not able to prevent subordinate females from copulation and
fertilization but achieved complete reproductive suppression of subordinate
females during gestation (Arnold,
1990b;
Hackländer
et al., 1998).
Female reproduction is further affected by males. Almost all territorial females failed to reproduce in years when the territory owner was replaced by a new male after the mating season. Insufficient body mass could be excluded as a reason for these failures. There are three possibilities for how new territorial males could manipulate female reproduction: (1) by killing juveniles, (2) by causing the mother to commit infanticide, or (3) by blocking gestation.
There are numerous reports of observed or assumed infanticide in other
ground-dwelling sciurids (Armitage et al.,
1979; Balfour,
1983; Betts, 1991;
Blumstein, 1997;
Brody and Melcher, 1985;
Dobson and Kjellgaard, 1985;
Hare, 1991;
Hoogland, 1985;
Lacey, 1992;
McLean, 1983;
Perrin et al., 1994;
Sherman, 1982;
Steiner, 1972;
Trulio, 1996;
Trulio et al., 1986;
Vestal, 1991;
Waterman, 1984;
Wiggett and Boag, 1986).
Coulon et al. (1995) observed
that a new territorial alpine marmot male killed a juvenile and assumed that
infanticide by new males was responsible for the death of juveniles in several
other cases. However, we have no evidence for direct infanticide after a male
takeover in our study population. We never found carcasses of juveniles killed
by conspecifics. During 14 years of study we only once detected juveniles that
had been attacked by other marmots. In this case, the juveniles were offspring
of a former subordinate female who expelled the previous territorial female,
her mother, from the territory. Two of four juveniles became severely injured
during the struggle for dominance between the two females. Furthermore, we
have no evidence for defense behavior of territorial females, a possible
indication for infanticidal new males
(Elwood et al., 1990).
Nevertheless, the lack of evidence for direct infanticide in our study does
not exclude this possibility. Infanticide would not be detected if it occurred
inside burrows, nor would cannibalism, a widespread behavior in
ground-dwelling sciurids (Armitage et al.,
1979; Hare, 1991;
Holmes, 1977;
McLean, 1983;
Plotnikov, 1997;
Trulio et al., 1986;
Vestal, 1991). In fact, one of
the females from groups with male takeovers presumably lost her young after
parturition (gray squares in Figure
1), suggesting that her juveniles had been killed.
The third explanation for female reproductive failure, male-caused blocking
of gestation, is well documented for a variety of rodent species under
laboratory conditions (reviews in Huck,
1984; Schwagmeyer,
1979). However, apart from one study about pregnancy interruption
in Microtus ochrogaster under seminatural conditions
(Heske and Nelson, 1984),
there is to our knowledge only one study showing the existence of this cryptic
pathway of reproductive suppression in wild rodent populations under natural
conditions (in Microtus pennsylvanicus;
Mallory and Clulow, 1977).
Three lines of evidence suggest that in alpine marmots a block of gestation is
a likely reason for the lack of successful reproduction after a change of the
territorial male. First, territorial females failing to reproduce after a male
takeover showed clear signs of pregnancy early in the season, but did not wean
any young. Second, direct infanticide seems to occur infrequently
(Coulon et al., 1995; this
study). Third, the decrease in circulating progesterone in these females after
the mating season suggests abortion or resorption of litters, a common
phenomenon in marmots (Bibikow,
1996).
The adaptive value of male-caused reproductive failure
Darwin (1871) pointed out
that killing unrelated juveniles is advantageous for males if females then
come into estrus earlier, offering the infanticidal male an immediate chance
for reproduction. This specific advantage does not exist in monoestrous
species like marmots. However, infanticide would still be beneficial for a
male if females are more likely to produce young (or have larger litters)
after a year with no or negligible maternal investment
(Hoogland, 1985;
Michener, 1982). Parous female
alpine marmots bear not only the considerable energetic costs of gestation and
lactation, they also have higher mass loss during winter because juvenile
alpine marmots must be warmed during their first hibernation
(Arnold, 1990b). This is
energetically costly for dams even when supported by their mate or by
offspring from previous years (Arnold,
1993). Consequently, parous females had a lower vernal body mass
in the year after reproduction and therefore had less reproductive output. In
contrast, nonparous females, and in particular females failing to reproduce
because of a male takeover, had a higher chance of producing young in the
following year. Hence, by blocking gestation new territory owners most likely
increased their lifetime reproductive success. The cases of successful
reproduction despite a male takeover further support the view of an adaptive
male manipulation of female reproduction. Female reproduction was not impaired
if the new male was probably the sire of the young because the former
territory owner had been expelled during the mating season.
However, gestation is a under female control, in contrast to male
infanticide. Why should females abort or resorb their unborn young after a
male takeover? A frequently offered answer is that females avoid useless
maternal investment by interrupting gestation if infanticide by the new male
is expected (Huck, 1984;
Schwagmeyer, 1979). This
explanation may hold for alpine marmots, too. Mothers presumably could not
protect their young from infanticidal males because juveniles are active in
the group's entire territory within a few days upon emergence from the natal
burrow. On the other hand, we have to consider that females may interrupt
gestation not only to minimize inevitable losses of reproductive investment.
Reproduction with the new male could have additional advantages. An intruding
male that repelled the territorial male is typically in better condition
(Arnold, 1990a), possibly
indicating superior genetic quality. To summarize, as long as the residual
reproductive value of a female does not becomes too small, it may well be
advantageous for females to give up the present reproduction and mate with the
new territorial male as early as possible.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We are grateful to everyone who helped us in the field, especially to Fredy Frey-Roos. The Berchtesgaden National Park administration provided housing and equipment. We thank Erich Möstl for supporting and Alexandra Kuchar-Schulz carrying out the enzyme immunoassays at the Institute of Biochemistry, University of Veterinary Medicine, Vienna. We also thank Thomas Ruf for helpful comments on earlier drafts. This study was financed by grants from the Max-Planck-Society and the Deutsche Forschungsgemeinschaft (Ar 180/1-1; SFB 305, project C8).
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