AN ABSTRACT OF THE THESIS OF
Christine L. Dalton for the degree of Master of Science in Wildlife Science
presented on January 29, 1998. Title: Effects of Female Kin Groups
on Reproduction and Demography in the Gray-tailed Vole (Microtus
canicaudusl.
Redacted for Privacy
Abstract approved:
The 3-5 year cyclical fluctuations in populations of many vole and
lemming species have perplexed ecologists for many years. Numerous
hypotheses have been proposed to explain microtine rodent cycles,
including various aspects of social behavior. Microtine rodents
commonly form kin groups composed of related females. Charnov and
Finerty (1980) proposed that the formation and breakup of kin groups
could, in part, explain the rates of population increase and decline
associated with cycles. My experiment sought to determine if kin groups
provided population-level benefits in gray-tailed voles, Microtus
canicaudus. I compared unmanipulated populations with populations in
which kin-structuring was experimentally disrupted to determine if kin
groups affected population growth rates and size, reproduction,
pregnancy and lactation rates, and recruitment, movement and survival
of juveniles. I monitored demography and reproductive behavior in eight
0.2 ha experimental enclosures during a summer breeding season. I
found no differences in demographic or female reproductive parameters
between control and treatment enclosures, with the exception of a
delayed time to first pregnancy for females introduced into the treatment
enclosures. In addition, I found no differences in the time to sexual
maturation or dispersal movements of juvenile males between control
and treatment enclosures. I conclude that disrupting the formation of
kin groups does not adversely affect demographic or reproductive
parameters at the population-level in gray-tailed voles, and suggest that
the contribution of kin groups to social behaviors that may affect
population regulation is probably quite small.
Effects of Female Kin Groups on Reproduction and Demography in the
Gray-tailed Vole (Microtus canicaudus)
by
Christine L. Dalton
A THESIS
submitted to
Oregon State University
in partial fulfillment of
the requirements for the
degree of
Master of Science
Presented January 29, 1998
Commencement June 1998
Master of Science thesis of Christine L. Dalton presented on January 29,
1998
APPROVED:
Redacted for Privacy
Major Profess , repre nting Wildlife cience
Redacted for Privacy
Chair of Departme
f Fisherij and Wildlife
Redacted for Privacy
Dean of Graduate School
I understand that my thesis will become part of the permanent collection
of Oregon State University libraries. My signature below authorizes
release of my thesis to any reader upon request.
Redacted for Privacy
Christine L. Dalton, Author
ACKNOWLEDGMENTS
I thank my major professor, Jerry 0. Wolff, for his critical role in
all aspects of this research. The field work would not have been possible
without the assistance of my colleagues, Monica Bond, Tracie Caslin,
Robert Skil len, Kelli Walker and Guiming Wang, all of whom I thank for
their hard work and dedication to the communal nature of our individual
projects. Finally, I thank my parents, Helen and Oliver Dalton, for their
support of my goals, and Patrick Byrne for his belief in my abilities. This
research was supported by NSF Grant 93-06641 to J. 0. Wolff.
TABLE OF CONTENTS
Page
INTRODUCTION
1
METHODS
8
Study Species
8
Research Facilities
8
Trapping Procedures
9
Experimental Procedures
9
Data Analysis
Demography
Reproduction and Recruitment
Survival
RESULTS
10
11
11
12
13
Demography
13
Reproduction and Recruitment
16
Female Recruitment
16
Movement
Time to Maturity and Pregnancies
Survival
Male Recruitment
Movement
Time to Maturity
Survival
16
20
20
20
20
21
21
DISCUSSION
22
SUMMARY AND CONCLUSIONS
31
TABLE OF CONTENTS (Continued)
Page
BIBLIOGRAPHY.
33
APPENDIX
40
LIST OF FIGURES
Figure
Page
1. Mean (SE) population size of gray-tailed voles in control and
treatment enclosures at Hyslop Agronomy Farm, Benton
County, Oregon, 1997
14
2. Mean (SE) population growth rates of gray-tailed vole
populations in control and treatment enclosures at Hyslop
Agronomy Farm, Benton County, Oregon, 1997
15
3. Mean (SE) proportion of adult females in reproductive
condition, expressed as the number of reproductive females
per total number of adult females, in control and treatment
enclosures at Hyslop Agronomy Farm, Benton County,
Oregon, 1997
17
4. Mean (SE) juvenile recruitment, expressed as the number of
recruits per adult female in reproductive condition 4 weeks
earlier, in control and treatment enclosures at Hyslop
Agronomy Farm, Benton County, Oregon, 1997
18
5. Mean (SE) proportion of vole populations composed of
recruits (__30 g), in control and treatment enclosures at
Hyslop Agronomy Farm, Benton County, Oregon, 1997
19
EFFECTS OF FEMALE KIN GROUPS ON REPRODUCTION AND
DEMOGRAPHY IN THE GRAY-TAILED VOLE (MICROTUS CANICAUDUS)
INTRODUCTION
A common feature of the social organization of many mammals is
that young females are philopatric and remain in female kin groups
throughout their lives, while juvenile males disperse from their natal site
and do not associate with kin as adults (Boonstra et al. 1987, Pusey
1987, Brandt 1992, Wolff 1993a). Kin groups commonly occur in social
species such as many species of primates (Smuts et al. 1987) and
ungulates (Estes 1974, Jarman 1974), but also form in territorial species
in which daughters occupy territories adjacent to or that overlap those of
their mothers, such as ground squirrels, Spermophilus spp. (Sherman
1981, Murie and Michener 1984) and prairie dogs, Cynomys ludovicianus
(Hoogland 1985). Microtine rodents typically follow this general
mammalian pattern of social organization in which young females are
philopatric, young males disperse, and female neighbors are closely
related (e.g., prairie voles, Microtus ochrogaster, Getz et at 1990;
meadow voles, M. pennsylvanicus, Bollinger et al. 1993; root voles, M.
oeconomus, Ims et al. 1993; Townsend's voles, M townsendii, Lambin
1994a; gray-tailed voles, M canicaudus, Wolff et al. 1994).
The formation of kin groups may benefit both males and females as
in predator vigilance and group defense (e.g., Sherman 1985, Cheney
and Seyfarth 1990) or group hunting (Mech 1970, Pusey and Packer
1997). Female kin groups also may benefit females directly (and males
only indirectly) as in cooperative breeding (Emlen 1997, Solomon and
French 1997), or reducing the risk of infanticide (Wolff 1993b, Lambin
and Yoccoz 1998). Female philopatry and the formation of kin groups
2
may provide inclusive as well as individual fitness benefits to females
(Hamilton 1964).
In species in which females form kin groups within or adjacent to
their natal home range, young males typically disperse. Male-biased
juvenile dispersal is considered a mechanism to reduce resource or
reproductive competition within the natal site (Dobson 1982, Waser
1985, Anderson 1989) or, more likely, to avoid inbreeding (Greenwood
1980, Pusey 1987, Brandt 1992, Wolff 1992, 1993a, Bollinger et al.
1993, Lambin 1994a). Sexual maturation appears to be associated
negatively with the presence of opposite-sex relatives (Wolff 1993a,
Lambin 1994a), and juvenile emigration frequently is correlated with the
presence of opposite-sex relatives at the natal site indicating that
dispersal functions to prevent inbreeding (Wolff 1993a, Wolff 1997) and
perhaps hasten the time to sexual maturation for dispersing individuals.
Thus, a form of social organization in which females remain in kin
groups and males disperse has a number of possible fitness benefits for
both male and female mammals. Females may increase individual and
(or) inclusive fitness, and males that disperse may hasten time to
maturity and therefore increase individual fitness.
Several field studies have shown that shared use of space by
female kin in territorial species is more likely to occur at high densities
than at low densities (e.g., Jannett 1978, Madison and Mc Shea 1984,
Pugh and Tamarin 1990, Wolff 1992, Lambin and Krebs 1993, Lambin
1994a). At low densities vacant space is available for colonization, and
juveniles are more likely to emigrate from their natal site and establish
independent home ranges than at high densities when the habitat is
saturated and a "social fence" of aggressive males and territorial females
may deter juvenile emigration (Hestbeck 1982, Wolff 1995). Thus, low
3
densities are typified generally by solitary nesting, increased emigration
of juveniles, and greater movements of adults (Lambin and Krebs 1991,
Wolff 1992, 1994a, 1997) whereas extended families, communal nesting
and the formation of kin groups appear to be a consequence of delayed
emigration at high densities (Lambin and Krebs 1993, Lambin 1994a,
Wolff 1994 b) .
A common feature of mammal populations at high densities,
associated with delayed emigration, is delayed sexual maturation of
juveniles (e.g., Jannett 1978, Corbett 1988, McGuire and Getz 1991,
Wolff 1992, Lambin 1994a, Wolff 1997). Two hypotheses have been
proposed to explain the mechanism by which delayed sexual maturation
occurs. In young female mammals, reproductive suppression may be an
intrinsic mechanism to conserve reproductive effort in the face of adverse
conditions created by the presence of dominant adult females (e.g.,
threat of infanticide), or the presence of male relatives (to avoid
inbreeding ) (Wolff 1997). Inbreeding avoidance (due to the presence of
their fathers) probably does not affect mating behavior of females in
promiscuous/polygynous species such as voles, because females are
exposed to many males other than their fathers (Wolff 1997). However,
considerable supportive evidence exists for reproductive suppression in
female voles in the presence of dominant older females (reviewed in Wolff
1997).
Infanticide has been proposed as a form of reproductive
competition among females in which intruding females kill offspring of
the resident female and then occupy the space vacated by the victimized
female (Hrdy 1979, Sherman 1981, Wolff and Cicerello 1989). Infanticide
by strange females has been well-documented in rodents (Brooks 1984,
Wolff 1993b and references cited therein). Female small mammals
4
aggressively defend territories against other adult females (Ostfeld 1985,
Wolff 1993b), however, the function of these territories is equivocal.
Wolff (1993b, 1997) contends that females defend space to deter
infanticide by other females. Females that are in kin groups and (or) that
have related females in neighboring territories would be less prone to
commit infanticide than females surrounded by unrelated females
(Sherman 1981, Wolff 1993b). Lambin and Yoccoz (1998) suggest that
increased preweaning survival in a field study of Townsend's voles might
be due to a differential rate of infanticide by established females towards
offspring of their related and unrelated neighbors. If female kin groups
contribute to a decrease in infanticide by dominant females, juvenile
recruitment should be greater for females in kin groups than for females
with non-kin as neighbors.
Reproductive suppression in young male rodents may be a
response to threats from dominant males (Jannett 1978) or to the
presence of female relatives (Wolff 1992). Sexual maturation appears to
be associated negatively with the presence of opposite-sex relatives (Wolff
1992, Lambin 1994a). In environments in which mothers and daughters
form extensive breeding families, young males can either disperse to find
unrelated mates, or, if dispersal is not feasible (for example, due to a
social fence) reproduction may be suppressed. Therefore, young males
should be more apt to grow faster and become sexually mature more
quickly if female relatives are absent, than if they are present.
A common feature of many microtine populations is that they cycle
on a 3-5 year periodicity (Krebs and Myers 1974, Norrdahl 1995).
Numerous hypothesis have been proposed to explain this cyclic
phenomenon (summarized in Batzli 1992 and Norrdahl 1995) including
various aspects of social behavior (Chitty 1960, Krebs 1996). Charnov
5
and Finerty (1980) proposed that the formation and breakup of kin
groups could, in part, explain the rates of population increase and
decline associated with cycles. According to their model, low and
increasing populations are comprised of neighbors who are kin
("friends"), whereas at high densities, neighbors are more apt to be nonkin ("strangers"). An implication of the model is that kin will behave
amicably toward one another resulting in high juvenile recruitment,
whereas non-kin neighbors will be more aggressive resulting in poorer
recruitment and eventual population decline. Thus, the relatedness of
individuals may influence their behavioral interactions and could play a
role in regulating the density of microtine rodent populations (Charnov
and Finerty 1980, Pugh and Tamarin 1990).
While the Charnov and Finerty model has great appeal,
experiments have produced mixed results (Boonstra and Hogg 1988,
Ylonen et al. 1990, Sera and Gaines 1994), and in general do not support
the model (Kawata 1990, Pugh and Tamarin 1990, Lambin and Krebs
1993). The experimental design most commonly used to test the
Charnov and Finerty hypothesis has been to establish enclosed
populations consisting of related females and others of unrelated
females, add an appropriate number of males, and monitor the
populations for survival, growth, and reproductive parameters (e.g.,
Boonstra and Hogg 1988, Ylonen et al. 1990, Sera and Gaines 1994).
The methods and interpretations of most of these experiments, however,
are equivocal and may not be an adequate test of the model (Wolff 1995).
In a field experiment to determine if kin groups conveyed a reproductive
advantage for female Townsend's voles, Lambin and Yoccoz (1998)
manipulated unenclosed populations of voles to create kin and non-kin
treatments (kin treatments were created by removing immigrants and
6
preventing predation by birds, and non-kin treatments by removing
members of family groups). They found greater preweaning survival in
kin than in non-kin groups and concluded that females that have
relatives for neighbors had greater reproductive success than those that
had strangers as neighbors. Lambin and Yoccoz (1998) present an agestructured demographic model suggesting that such differences in preweaning survival may have a substantial impact on population growth
rates. Their study, however, was not designed to measure populationlevel responses, nor did they examine post-weaning survival and
reproductive success of young females. In fact, none of the
aforementioned studies has adequately tested how the presence or
absence of kin groups affects population growth rate, and thus could
contribute to population cycles.
The advantages that kin groups confer to microtine rodent
populations are poorly understood, but may include deterrence against
infanticide, communal and/or cooperative breeding, and reduced energy
expenditure in territorial defense (refs op cited). Even if kin groups may
provide individual fitness advantages to females, these fitness benefits
may not translate to population-level responses, may not be density-
dependent, and thus may not contribute to population cycles. The role
of kin groups in juvenile recruitment, population growth rate, and timing
of dispersal and sexual maturation of young males and females has not
been tested experimentally.
The objective of my study was to compare population growth rates,
juvenile recruitment and survival, reproductive rates of females,
dispersal behavior of young males, and time to sexual maturation for
young males and females in populations comprised of kin or non-kin
groups. This replicated experiment was conducted in enclosed
7
populations in which I controlled for other external variables that could
affect these response variables. To meet these objectives, I tested three
hypotheses regarding microtine kin groups: (1) populations that
consisted of females in kin groups would grow at a faster rate and reach
higher densities than populations in which neighboring females were
non-kin; (2) females that remained in kin groups would have higher
survival rates, decreased time to first reproduction, higher juvenile
recruitment, and more rapid growth rates than females that were forced
to disperse and settle among non-kin; and (3) juvenile males would
disperse farther and mature less rapidly in populations in which their
female siblings were present than in populations in which they were
removed.
To test these hypotheses, I used the gray-tailed vole in semi-
natural enclosures as an experimental model system (Ims et al. 1993,
Wiens et al. 1993). Four control enclosures were left unmanipulated
throughout the study, allowing kin groups to develop normally. In four
treatment enclosures, I removed all female recruits and switched them
among the enclosures so that juvenile females did not settle near their
siblings or parents. I monitored the demography and reproduction of
populations in the eight enclosures for 4 months.
8
METHODS
Study Species
The gray-tailed vole is a common, grassland, small mammal
species of the Willamette Valley of western Oregon. Gray-tailed voles are
similar in appearance, behavior, and ecology to other Microtus species
(Tamarin 1985). Breeding occurs from March through November, modal
litter size is six, juveniles are weaned at 15-18 days, and females can
start breeding when they are 18 g (18-20 days old) (Wolff et al. 1994).
The mating system, like that of most mammals, is polygynous or
promiscuous. Juvenile females are philopatric, and juvenile dispersal is
male-biased. Home ranges of males are twice as large as those of
females. Female home ranges are relatively exclusive of other unrelated
females, but male home ranges overlap those of each other and those of
one or more females (Wolff et al. 1994, Wolff et al. 1996).
Research Facilities
The study was conducted at a small mammal enclosure facility
located at the Hyslop Agronomy Farm of Oregon State University,
approximately 10 km north of Corvallis, Oregon (Wolff et al. 1994, Edge
et al. 1996). The experimental units consisted of eight, 0.2 ha (45 by 45
m) enclosures planted with a mixture of pasture grasses. Each enclosure
is constructed of galvanized sheet metal approximately 90 cm high and
buried ca. 90 cm deep to prevent escape or entry by burrowing animals
(Edge et al. 1996). A 1-m wide strip along the inside of the fence within
each plot was kept bare to minimize use by small mammals. Eighty-one
trap stations were established in each enclosure in a 9 by 9 array with
9
5 m between trap stations. One large Sherman live trap (8 x 9 x 23 cm)
was placed at each trap station.
Trapping Procedures
Animals were trapped for 4 consecutive days (trap period) at 2­
week intervals from 12 May to 12 September 1997. Traps were baited
with sunflower seeds and oats. During trap periods, traps were set 1 h
of sunset and checked at sunrise the following morning. During nontrapping weeks, traps were propped open and baited once to encourage
voles to enter traps.
Captured animals were ear-tagged for individual identification,
and data on body mass (measured to the nearest 1 g with Peso la spring
scales), sex, reproductive condition of females, and trap location was
recorded for each capture. Animals were considered adults if their body
mass was ?_30 g. Females were considered to be in reproductive
condition if they were lactating, noticeably pregnant, or had widely
parted pubic symphyses. Testes of males are relatively small and cannot
be measured externally, so males were considered to be reproductive if
their body mass was _30 g (Wolff et al. 1994).
Experimental Procedures
Six adult females and six adult males not closely related to one
another were introduced into each of eight enclosures in late April, 1997.
The founding voles were given approximately 2 weeks to adjust to the
enclosures before trapping began 12 May 1997. These densities and a
1:1 sex ratio are within the normal range of wild Microtus populations
(Taitt and Krebs 1985, Wolff et al. 1996).
10
The experimental populations were assigned randomly to the eight
enclosures. In four control enclosures, populations were unmanipulated
throughout the experiment (except for biweekly trapping to collect data)
and kin groups were assumed to form naturally.
In four treatment enclosures, juvenile female recruits were
removed at first capture and switched among the treatment enclosures.
Each juvenile female removed was replaced by a juvenile female removed
from a different treatment enclosure (supplemented with voles from
surplus enclosure populations as needed). Juvenile females were
introduced at the same trap station from which a removal animal was
taken. To control for age differences, removal animals were replaced by
juvenile females of similar weights. This experimental design served to
disrupt any female kin groups that might form in the treatment grids,
while not manipulating the natural size and age-structure of the
populations.
Data Analysis
I used the Statistical Analysis System (SAS Version 6.0; SAS
Institute, 1989) to conduct repeated-measures analysis-of-variance
(ANOVA), and one-way ANOVA to test for differences between means.
The arcsine square-root of proportional values was analyzed to satisfy
assumptions of statistical tests, however I report non-transformed
proportions. The enclosures were used as replicates for all analyses
(N = 4). Statistical significance was assumed when P 0.05. Original
data and sample sizes within the enclosures for one-way ANOVA
analyses are given in the Appendix.
11
Demography
I used program CAPTURE (Rexstad and Burnham 1992) to
estimate population size for each enclosure and trap period. Population
growth rates (r) were determined by r = [loge (Nt/NO)] /t, where Nt is the
estimated population size one trap period, Ne is the estimated population
size the previous trap period, and t is the time between trap periods (in
this experiment t = 2).
Reproduction and Recruitment
I measured reproductive rate as the proportion of adult females
(?_30 g) that were in reproductive condition relative to the total number of
adult females in each enclosure. I measured recruitment as the logtransformed number of recruits captured in an enclosure per adult
female in reproductive condition captured in the same enclosure 4 weeks
(two trap periods) earlier. The time lag allowed recruits to reach
trappable size. In addition, I measured the proportion of recruits per
total number of animals in each enclosure each trap period.
I measured rate of maturation of male and female juvenile animals
by the number of weeks for an animal first caught at <30 g to reach
adulthood (30 g), and additionally, for males, by the mean weight change
per week for animals recruited at <30 g. I measured the time to first
pregnancy of juvenile females as the number of weeks it took for female
recruits first captured at <30 g to reach first pregnancy, and included
only animals that eventually became pregnant.
To determine the number of females that were nursing their young
after giving birth, I measured the proportion of females lactating per total
number of females recaptured within 12 days of parturition. As an
12
estimate of reproductive rate, I measured the mean number of
pregnancies and the mean interval between births per recruited female.
To determine if juvenile animals remained in their natal or
introduced sites, I measured the distance an individual moved from first
capture (or its release site) to its capture location when it weighed ?_30 g.
I limited this analysis to animals first caught at __15 g. Because juvenile
gray-tailed voles are weaned at 15-17 g, at _1.5 g I assumed them to be in
their natal territory.
Survival
I estimated juvenile survival as the proportion of recruits (first
caught when they weighed <30 g) caught in the first 6 weeks of the
experiment that were recaptured as adults (.30 g).
13
RESULTS
Demography
I caught 640 voles 2,457 times between 12 May and 12 September
1997. I captured 130 female recruits (57. = 33; SE = 6.4) in control and
113 female recruits (5 = 28; SE = 6.3) in treatment enclosures. In
treatment enclosures I removed all juvenile females at first capture and
replaced 110 out of 113 (97%) with a recruit not born in that enclosure.
Eighty-four percent of the young females were replaced with animals that
weighed _6 g of the removed female's weight.
Population size increased from the initial 12 animals per enclosure
in May to means of 65 (SE = 6.31) in control and 82 (SE = 14.45) in
treatment enclosures at the end of the study (Fig. 1). Based on 0.185 ha
of available habitat per enclosure, densities reached means of 351
animals/ha in control and 443 animals/ha in treatment enclosures.
Population size differed over time (F 7,42 = 25.4; P < 0.001), but not by
treatment (F1,6 = 0.001; P= 0.980), nor did I detect a time by treatment
interaction (F 7,42 = 0.929; P = 0.491). The population sizes generally
increased throughout the summer, but did not differ between control and
treatment enclosures.
Population growth rates fluctuated between weeks and generally
declined throughout the summer, but I detected no time (F 7,42 = 1.24;
P = 0.301) or treatment (F 1,6 = 0.880; P = 0.384) effects, nor a time by
treatment interaction (F 7,42 = 0.874; P = 0.539) (Fig. 2).
14
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Figure 1. Mean (SE) population size of gray-tailed voles in treatment
and control enclosures at Hyslop Agronomy Farm, Benton County,
Oregon, 1997.
15
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ee
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Figure 2. Mean (SE) population growth rates of gray-tailed vole
populations in control and treatment enclosures at Hyslop Agronomy
Farm, Benton County, Oregon, 1997.
S.,f5e
0
16
Reproduction and Recruitment
The proportion of females in reproductive condition differed over
time (F6,36.7.710; P < 0.001), but not by treatment (F1,6= 0.020;
P = 0.898) nor did I detect a time by treatment interaction (F6,36 = 0.440;
P = 0.848). In both control and treatment populations the proportion of
females in reproductive condition generally increased during the first 4
weeks of the summer, and decreased gradually thereafter (Fig. 3).
The mean number of recruits per adult female in reproductive
condition differed over time (F6,36 = 4.770; P = 0.003), but not by
treatment (F1,6 = 0.020; P = 0.888), nor did I detect a time by treatment
interaction (F6,36 = 0.990; P = 0.445). The number of recruits per adult
female in reproductive condition decreased gradually throughout the
summer in both control and treatment enclosures (Fig. 4).
The mean proportion of recruits differed over time (F6,36 = 3.800;
P < 0.005), but not between treatments (F1,6 = 0.000; P = 0.959), nor did I
detect a time by treatment interaction (F6,36 = 0.520; P = 0.787)(Fig. 5).
The mean proportion of female voles lactating within 12 days of
parturition did not differ between control (R = 0.60; SE = 0.077) and
treatment (R = 0.62; SE = 0.097) populations (F1,6= 0.021; P = 0.889).
Female Recruitment
Movement
The distance that female recruits first caught at <15 g moved from
their presumed natal territory to their established territory upon
reaching maturity differed between control (R = 5.4 m; SE = 2.35 m) and
treatment (R = 17.0 m; SE = 2.57 m) populations.
17
Figure 3. Mean (SE) proportion of adult females in reproductive
condition, expressed as the number of reproductive females per total
number of adult females, in control and treatment enclosures at
Hyslop Agronomy Farm, Benton County, Oregon, 1997.
18
10 June 24 June 8 July 22 July
5 Aug
19 Aug
3 Sept
Figure 4. Mean (SE) juvenile recruitment, expressed as the number of
recruits per adult female in reproductive condition 4 weeks earlier, in
treatment and control enclosures at Hyslop Agronomy Farm, Benton
County, Oregon, 1997.
19
I
1
6'
9
.<9
e
Figure 5. Mean (SE) proportion of vole populations composed of
recruits (<30 g), in control and treatment enclosures at Hyslop
Agronomy Farm, Benton County, Oregon, 1997.
i
0
-4?,
20
Time to Maturity and Pregnancies
The proportion of female recruits that eventually became pregnant
did not differ between control (5-< = 0.91; SE = 0.051) and treatment
(R = 0.94; SE = 0.036) populations (F1,6 = 0.039; P = 0.849). The time to
first pregnancy (in weeks) for female recruits that eventually became
pregnant differed between control (>7 = 3.13; SE = 0.333) and treatment
(5-( = 4.18; SE = 0.129) populations, after accounting for the effect of
weight at first capture (F1,5= 6.59; P = 0.050). The interbirth interval for
female recruits that eventually became pregnant did not differ between
control (R = 5.08; SE = 0.661) and treatment (>7 = 3.59; SE = 0.506)
populations (F1,6 = 3.230; P = 0.123).
Survival
The proportion of female juvenile recruits first captured at <30 g
that survived until maturity (_30 g) did not differ between control
(R = 0.97; SE = 0.020) and treatment (>7 = 0.93; SE = 0.025) populations
(F1,6 = 0.973; P = 0.362).
Male Recruitment
Movement
The distance that male recruits first caught at .15 g moved from
their presumed natal territory to their established territory upon
reaching maturity did not differ between control (R = 17.6 m;
SE = 1.71 m) and treatment (5-< = 16.8 m; SE = 1.91 m) populations.
21
Time to Maturity
Weight gain per week between first capture and first week of
maturity of male recruits first caught at <30 g did not differ between
control (g = 13.2; SE = 0.57 g) and treatment (R = 13.5; SE = 0.94)
populations, after accounting for the effect of weight at first capture
(F1,5= 0.373; P = 0.568). In addition, the mean number of weeks to
sexual maturity for this same sub-population of male recruits did not
differ significantly between control (R = 2.22; SE = 0.096) and treatment
(R = 2.48; SE = 0.108) populations after taking into account initial weight
of the recruits (F1,5= 1.76; P = 0.242).
Survival
The proportion of male juvenile recruits first captured at <30 g that
survived until maturity (?_30 g) did not differ between control (R = 0.96;
SE = 0.023) and treatment (x = 0.85; SE = 0.059) populations
(F1,6 = 1.89; P = 0.218).
22
DISCUSSION
This study provided a replicated population-level comparison
between unmanipulated gray-tailed vole populations and treatment
populations in which juvenile females were removed, disrupting the
formation of kin groups. The objective of my research was to determine if
kin-structuring in populations affected population growth rate and size,
reproduction, pregnancy and lactation rates, and juvenile recruitment.
My first hypothesis, that control populations in which kinstructuring was allowed to develop would grow faster and reach higher
densities than treatment populations in which kin groups were
disrupted, was not supported. I found no statistically or biologically
significant differences in population growth rates or population size
between control and treatment populations. Populations grew from the
initial 12 voles/enclosure to means of 65 in the control (351 voles/ha)
and 82 voles/enclosure in the treatment (443 voles/ha) in about 90-100
days. Growth rates were fairly consistent throughout the season,
peaking in mid-June in the control populations and in early June in the
treatment populations. The growth rate was positive throughout the
summer in both control and treatment populations with the exception of
the final week of the experiment (early September) when the control
populations experienced a slight decline.
Similarly, my results did not support my second hypothesis. The
number of adult females in reproductive condition, the number of
juveniles per reproductive female, and the proportion of the populations
composed of juveniles did not differ between control and treatment
populations. These analyses included all adult females (founding
females plus recruits that subsequently were caught as adults), and
23
indicates that reproduction in the treatment populations did not suffer
as a result of replacing female recruits with females from different
populations. The lack of difference in these reproductive parameters is
reflected in the similar sizes and growth rates of the control and
treatment populations.
Two reproductive parameters measured for the recruited (or
introduced) females, proportion of females that eventually became
pregnant, and birth intervals, did not differ between control and
treatment populations. However, treatment females took 1 week longer
to experience their first pregnancy than juvenile female recruits in the
control populations. This is not surprising considering the unnatural
"stress" of being transported to a new environment in which young
females had to establish a breeding territory, burrow system, and nest
site among unfamiliar competitors. Yet even with this unnatural "forced"
dispersal, the survival rate of translocated young females was 93% and
did not differ from the 97% survival of young females in control
populations. Females first caught at _1.5 g and introduced into
treatment enclosures moved a mean of 17.0 m between introduction and
first capture at maturity, and these animals survived as well as recruits
in control populations that moved only 5.4 m and were not forced to
disperse. Female gray-tailed voles, like other Microtus species, are
assumed to defend territories aggressively (Wolff 1985, 1993b, Wolff et al.
1994). Thus, the delay in first reproduction of introduced females may
be attributable to competition with established adult females during
periods of high population densities. However, considering the purported
high costs of dispersal at relatively high densities (e.g., Hestbeck 1982,
Anderson 1989, Wolff 1993a), I was surprised by the lack of biologically
24
significant costs to immigration into unfamiliar populations by young
females.
The percentage of females successfully nursing a litter did not
differ between control and treatment populations (60% and 62%
respectively). Infanticide committed by strange females has been
proposed as a mechanism reducing juvenile survival in vole populations
(e.g., Wolff 1993b, 1995; Lambin 1994b). Although my measurement of
infanticide is indirect, it suggests that preweaning mortality did not
occur differentially when kin groups were disrupted. This finding
contrasts with suggestions made by Lambin and Yoccoz (1998) that the
differential degree of juvenile survival in kin versus non-kin populations
in Townsend's voles may be due to the presence of immigrant females in
their non-kin treatments.
In similar studies that compared populations composed of kin and
non-kin, no differences in population size or measures of fitness were
found between control and treatment populations of meadow voles
(Boonstra and Hogg 1988) or prairie voles (Sera and Gaines 1994). In an
experiment with bank voles, Ylonen et al. (1990) found higher rates of
population growth in kin populations. Ylonen et al. (1990) attributed
these conflicting results to the difference in the importance of social
interactions in population regulation between Microtus and Clethrionomys
species. In Microtus, females are more apt to share breeding space with
female relatives than are Clethrionomys. Alternatively, Wolff (1995)
suggested that a difference in the experimental design, namely that the
populations were composed of related males (in addition to the related
females), may account for the contradictory results. Wolff argued that
related males may be relatively amicable to each other and less apt to kill
each others' young. In the experiments conducted by Boonstra and Hogg
25
(1988) and Sera and Gaines (1994), the unrelated males could have been
killing infants in both the treatment and control populations (Wolff
1995).
Another confounding factor in the above studies is that after the
initial introductions, no manipulations were conducted and consequently
kin groups could have formed after the first litter was recruited. If initial
populations densities were relatively low such that space was available
for colonization, competition for territorial space would have been
minimal and consequently infanticide may not have occurred in either
treatment or control populations. My experimental design differed from
these studies in that I measured demographic and reproductive
parameters at low and high densities in populations in which kin groups
were prevented from forming for at least three generations. I did not rely
on the initial relatedness of the founding animals to define a "kin" or
"non-kin" population. Rather, I continually disrupted the kin structure
throughout the experiment, by removing all juvenile females as they were
caught and replacing them with juvenile females from unrelated
populations. This experimental design resembles more closely
experiments with Townsend's voles conducted by Lambin and Krebs
(1993) and Lambin and Yoccoz (1998) in which unenclosed populations
were manipulated to create kin and non-kin treatments. Lambin and
Krebs (1993) found higher female survival as well as higher weaning
success of the first spring litter on the kin treatments in spring. Lambin
and Yoccoz (1998) found a significant increase in preweaning survival in
kin treatments. Lambin and Yoccoz present an age-structured
demographic model that suggests that such differences in pre-weaning
survival may have a substantial impact on population growth rates.
However, neither experiment was designed to measure population-level
26
responses, consequently the influence of the observed fitness benefits to
individuals on demography is not known.
My study was not designed to measure individual benefits
associated with being in kin groups, but if they existed they were not
detectable at the population level. I had large sample sizes within each
enclosure (see Appendix) and four replicates for each treatment, and still
found no demographic or reproductive differences between control and
treatment populations. The comparable number of females that
eventually became pregnant and the similar birth intervals for control
and treatment females suggests that once established, females were as
successful in the non-kin as in the kin populations. In fact, the
population with the most rapid growth rate and that reached the highest
density was a treatment enclosure. The experimental design represented
a worst-case scenario in that I disrupted 100% of female kin groups for 4
months. The habitat in the enclosures during summer consisted of tall
(-1 m), dense vegetation and predation probably was minimal. Avian
predators including Northern harriers, Circus cyaneus, red-tailed hawks,
Buteo jamaicenis, and American kestrels, Falco sparverius, were observed
occasionally in the study area, but probably had little effect on vole
mortality. A total of 107 (5-< = 27) juvenile female recruits were captured
in the control enclosures. Ninety-seven percent of juvenile female
recruits in the control enclosures attained sexual maturity and young
females remained within 5.4 m of their natal site, suggesting that kin
groups were forming to some extent in control populations.
Having kin as neighbors presumably is beneficial in some species
such as ground squirrels (Sherman 1981, Murie and Michener 1984) or
prairie dogs (Hoogland 1985) in which considerable interaction occurs
among neighbors, especially in predator vigilance and giving alarm calls.
27
Having related females as neighbors may also be beneficial for some
microtine rodents or in some situations, as shown for Townsend's voles
by Lambin and Krebs (1993) and Lambin and Yoccoz (1998). However, I
found no evidence that individual benefits contributed to population
growth rates in gray-tailed voles. Modal litter size in gray-tailed voles is
six, which is comparable to that of many other microtine rodents (Keller
1985). However, the number of pups born in wild Microtus populations
that ever reach the trappable population is typically less than three,
often one or two (Taitt and Krebs 1985, Schauber et al. 1997, this study).
Of those one or two weanlings, probably less than half will live long
enough to breed and half of those will be males. Thus, the probability of
female kin groups ever forming or persisting long enough to contribute to
population regulation may be quite small. "Random" mortality and other
stochastic events likely disrupt kin groups frequently enough at all
densities to preclude them from contributing to differential population
growth rates and regulation.
Other demographic processes may be influenced by kin-
structuring. For example, Kawata (1987) proposed that kin groups may
enable individuals to more successfully survive a spring decline. Kin
groups may provide advantages at certain periods during the lifetime of
gray-tailed voles. My study was not designed to measure any parameters
that would reflect advantages during breeding lulls such as in winter.
However, gray-tailed voles are short lived (approximately 6 months) and
the greatest growth and reproduction occurs during the summer
breeding season, thus it might be expected that the advantages kin
groups provide would be exhibited during the summer breeding season.
The Charnov and Finerty (1980) model of vole population dynamics
predicts that at low densities neighbors will be kin and will behave
28
amicably toward one another, and at high densities aggression will
increase due to greater dispersion and an influx of non-kin, causing
populations to decline. According to this model, fitness benefits
associated with kin groups should be greater in populations at low
densities, when neighbors would more likely be kin, than at high
densities. However, some researchers have proposed just the opposite,
that at high densities individuals are more likely to be kin than non-kin,
and that kin groups would provide fitness advantages which in turn
would create a positive feedback on population growth (Lambin and
Krebs 1991, Wolff 1995). Under this scenario, greater fitness benefits
would be expected at high than at low densities. In an experiment
designed to test the level of relatedness in meadow vole populations at
differing densities, Pugh and Tamarin (1990) did not find a consistently
high level of relatedness among adult residents at low density, nor a
consistent reduction in relatedness among neighbors as density
increased, as the Charnov and Finerty (1980) model would predict. My
experiment monitored gray-tailed vole populations from relatively low to
relatively high densities, and failed to find any time-by-treatment
interactions in population size or growth rate, or reproductive and
recruitment rates. I suggest that the differing densities of the
populations did not result in changes in social behavior perceptible at
the population-level, as would be predicted by either of the above
scenarios.
My third hypothesis, that juvenile males would disperse farther
and mature less rapidly in populations in which their sisters were
present in the natal sight than in populations in which their sisters had
been removed, was not supported by my results. I detected no difference
in the distance dispersed by young males in control (R = 17.6 m) and
29
treatment (R = 16.8 m) populations. In that the treatment did not remove
the mothers of juvenile males, who may also affect juvenile male
dispersal, this response should be interpreted with caution. The time to
sexual maturation for juvenile males, measured either in number of
weeks or as weight gain per week, did not differ between control and
treatment populations. Survival of male recruits first caught at <30 g was
not affected by the disruption of kin groups (-- = 85% in control and )7( =
84% in treatment populations). In that male survival in gray-tailed voles
is probably a factor of male-male competition, and my manipulation did
not intentionally affect this parameter, I did not expect a difference in
juvenile male survival between control and treatment populations.
Only a few studies have been conducted to test for the stimulus
that precipitates dispersal of juvenile males. Wolff (1992) found that
juvenile dispersal in white-footed mice, Peromyscus leucopus, was
stimulated by the presence of opposite-sex parents. When a parent was
removed, the opposite-sex offspring would remain in or near the natal
site. However, when the opposite-sex parent was present, the juvenile
emigrated. In contrast, Jacquot and Vessey (1995) found that the
presence or absence of mothers in white-footed mice at time of juvenile
male dispersal was not related to dispersal distance. In addition, males
with more sisters dispersed farther than males with fewer sisters,
indicating that interactions with siblings may be more important than
interactions with the mother in determining dispersal distances. In
white-tailed deer, Odocoileus virginianus, removal of the mother caused
young males to remain in their natal site, whereas when the mother was
not removed, their sons emigrated (Holzenbein and Marchinton 1992).
In ground squirrels, all juvenile males emigrate from their natal site
regardless of the presence or absence of their mothers (Holekamp and
30
Sherman 1989). Holekamp and Sherman (1989) concluded that juvenile
male dispersal in ground squirrels is "hard-wired" and is not necessarily
stimulated by a social environment. In ground squirrels, females are
philopatric, and thus resident neighboring females would have been
related at some level. Consequently, male dispersal in ground squirrels
likely still functions to decrease the chances of inbreeding. My study was
not designed to test directly the stimulus for male dispersal, but my
findings suggest that the presence of sisters was not in itself sufficient to
affect emigration of brothers from the natal site. Emigration of young
males could be stimulated by the presence of their mothers, by a
combination of mothers and sisters, or dispersing from the natal site
may be an inherent behavior.
31
SUMMARY AND CONCLUSIONS
1. The objective of my research was to determine if kin-structuring in
populations of gray-tailed voles affected population growth rates and size,
reproduction, juvenile recruitment, and pregnancy and lactation rates. I
compared four treatment populations in which kin groups were deterred
from forming, with four control populations that I did not manipulate.
2. I found no differences in demographic or reproductive parameters
between the control and treatment populations, with the exception of a
delayed time to first pregnancy for the treatment females.
3. My experimental design differed from previous experiments that have
sought to test the effects of relatedness on demographic and fitness
parameters by comparing populations of related and unrelated voles, in
that I continually disrupted the kin structure of the treatment
populations throughout a summer breeding season. Additionally, my
analysis focused on population-level effects and thus contrasts with
other studies that have demonstrated individual-level benefits to
microtines in kin groups.
4. The results from this study refute the assumptions of the Charnov
and Finerty (1980) model of population dynamics relative to social
behavior. Because kin groups did not provide fitness benefits at the
population-level, I conclude that the degree of relatedness of individuals
does not contribute significantly to population-level vole dynamics.
5. My study provides evidence that young male voles are not affected by
the presence or absence of their sisters, either in distance moved from
the natal site or in time to sexual maturation. Further research is
required to determine the proximate (and ultimate) causes of juvenile
male dispersal in microtines.
32
6. Kin groups may provide fitness benefits in some rodents, such as
ground squirrels or prairie dogs, or under some conditions for microtine
rodents. However, my findings indicate that kin groups do not appear to
provide demographic or reproductive benefits at the population-level in
gray-tailed voles, and that further research may be needed to understand
the role of kin groups in microtine rodents.
33
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40
APPENDIX
41
APPENDIX. Summary data, sample sizes, means and standard
errors for each of four control and four treatment enclosures
used for one-way ANOVAs for each response variable.
Females
Controls
Parameter Enclosure No.
Treatments
N
x
Enclosure No.
N
x
Proportion of females lactating within 12 days of parturition
18
19
15
14
12
21
11
Total animals
Mean
52
1
0.53
0.50
0.83
0.55
2
6
14
20
10
16
13
13
52
0.60
0.077
SE
0.51
0.50
0.81
0.55
0.62
0.097
Proportion of recruited and introduced females that survived
until maturity
1
24
18
14
19
29
21
10
Total animals
Mean
77
0.92
1.00
0.97
1.00
2
25
6
12
12
16
14
20
65
0.97
0.020
SE
0.88
0.92
1.00
0.94
0.93
0.025
Proportion of recruited and introduced females that eventually
became pregnant
1
18
19
21
Total animals
Mean
SE
7
5
9
5
0.86
0.80
1.00
1.00
26
2
6
14
20
8
5
6
8
0.88
1.00
1.00
0.88
27
0.91
0.051
0.94
0.036
42
Appendix, Continued
Females, Continued
Controls
Parameter Enclosure No.
Treatments
N
R
Enclosure No.
N
T(
Distance moved (m) between first capture and maturity
by juvenile females first caught at <15 g
18
19
21
4
4
4
2
Total animals
14
1
11.5
5.5
4.6
0.0
Mean
SE
2
3
6
4
4
14
20
5
16
5.4
2.35
15.8
19.6
22.2
10.4
17.0
2.57
Weeks to first pregnancy for female recruits <30 g at introduction
that eventually became pregnant
1
3.13
2.20
3.70
3.56
16
10
18
19
21
20
Total animals
55
9
Mean
SE
2
14
6
14
11
11
11
20
4.00
4.18
4.00
4.55
47
3.13
0.330
4.18
0.130
Intervals between births (in weeks)
1
18
19
21
Total animals
Mean
SE
4
4
8
5
21
4.00
4.04
6.75
5.53
2
6
6
5
5
7
14
20
4.90
2.57
3.80
3.07
23
5.08
0.661
3.59
0.506
43
Appendix, Continued
Males
Controls
Parameter Enclosure No.
Treatments
Enclosure No.
N
N
Distance moved (m) between first capture and maturity
by juvenile males first caught at <15 g
1
1
18
19
21
2
Total animals
Mean
4
2
9
18.0
17.9
13.2
14
21.5
20
2
6
8
5
3
15.7
17.4
12.5
4
20
21.7
17.6
SE
16.8
1.91
1.71
Weight gain between first capture and maturity by male recruits
first caught at <30 g
1
11
18
19
21
15
13
12
51
Total animals
Mean
SE
11.55
13.67
14.19
13.21
2
26
6
5
14
12
20
20
63
13.15
0.572
10.90
15.10
13.38
14.65
13.51
0.941
Weeks to sexual maturity for male recruits first caught at <30 g
1
11
18
19
21
15
13
12
51
Total animals
Mean
SE
2.00
2.27
2.46
2.17
2.22
0.096
2
26
6
5
14
12
20
20
63
2.38
2.80
2.33
2.40
2.48
0.108
44
APPENDIX, Continued
Males, Continued
Controls
Parameter Enclosure No.
N
Treatments
x
Enclosure No.
N
x
Proportion of juvenile male recruits that survived until maturity
1
11
18
19
21
8
16
13
Total animals
48
Mean
SE
0.91
1.00
0.94
1.00
0.96
0.023
2
6
14
28
20
22
75
8
17
0.89
0.75
0.76
1.00
0.85
0.059