AN ABSTRACT OF THE THESIS OF
Heidi L. Brunkal for the degree of Master of Science in Wildlife Science, presented on
November 25, 1996.
Title: Over-winter Demography of the Gray-Tailed Vole (Microtus canicaudus) in
Fragmented and Continuous Ha
Redacted for privacy
Abstract approved:
W. Daniel E
Large scale disruption of natural habitats worldwide has led to concern over the
effects of habitat fragmentation on wildlife populations. Small scale experiments may be
a useful tool for discovering effects of fragmentation over larger landscape scales. I
sought to explore the potential for using voles as an experimental model system, at a
small scale, to discover mechanisms that may affect other species at different spatial
scales. I compared over-winter demography of gray-tailed voles, Microtus canicaudus, in
two experimental landscapes, consisting of fragmented and continuous habitat, to assess
the effects of habitat fragmentation. I chose winter as the time frame of the experiment
because it poses harsh conditions for voles and because seasonal bottlenecks may affect
population persistence. Population size, population growth rates, reproduction,
recruitment, survival and movements, were monitored using mark-recapture methods in
8, 0.2-ha enclosures planted with alfalfa. The habitat within the enclosures was
manipulated into 2 configurations of equal area, 1 large continuous patch (625 m2), and a
mosaic of 25 small patches (each 25 m2), prior to the introduction of 12 pairs of
animals/enclosure. I hypothesized that population size and growth rates, reproduction,
recruitment, and survival would be greater for vole populations in continuous habitats
than for populations in fragmented habitats. Additionally, I hypothesized that movements
would be more restricted within fragmented habitat because the voles would perceive the
area between habitat patches as a barrier.
I did not detect significant differences between vole populations in continuous and
fragmented treatments. However, populations residing in fragmented habitat showed
higher variability over the study period. Populations in both treatments decreased
throughout the winter period and all became extinct by the end of the study.
Reproduction occurred only during the fall period, and there were no significant
differences between treatments. Movements were not different between treatments, or
between male and female voles, but movements did increase over time. Survival appeared
to be higher for male voles in continuous habitat than in fragmented habitat, but female
vole survival was similar between treatments. Survival was influenced by weather
conditions, and predation. These results contrast with a previous experiment during the
summer season, and indicate that seasonal bottlenecks may be important to consider
when studying habitat fragmentation. Extinction of populations in both treatments
demonstrates that small populations are extremely vulnerable to both environmental and
demographic stochastic events.
Over-winter Demography of the Gray-Tailed Vole (Microtus canicaudus) in Fragmented
and Continuous Habitats
by
Heidi L. Brunkal
A THESIS
submitted to
Oregon State University
In partial fulfillment of
the requirements for the
degree of
Master of Science
Completed November 25, 1996
Commencement June 1997
Master of Science thesis of Heidi L. Brunkal presented on November 25. 1996.
Approved:
Redacted for privacy
eries and WilRe fe
Major Professor, representing
Redacted for privacy
Head of Department o
isheriest
da
cte
d
for
pri
d Wildlife va
cy
Redacted for privacy
Dean of Gradua 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
Heidi L. Brunkal, Author
ACKNOWLEDGMENT
This research was conducted as one of several experiments designed to investigate
the effects of habitat fragmentation on both demography and social structure of the gray-
tailed vole. I would like to thank my major professor, Dan Edge, for his assistance,
suggestions, and patience throughout my graduate education. I thank Jerry Wolff for his
contributions to the design of this research project. My colleague, Eric Schauber was
invaluable to me for help during the data analysis and provided much inspiration and
reassurance. Because this was an over-winter study, the field work was often in very wet
and cold conditions which were unpleasant and uncomfortable. I thank both Tom
Manning and Jenna App for critical assistance in coordination and completion of the data
collection and field work. Reed Noss and Gay Bradshaw provided critical comments on
the scale and scope of inference of this project. Weather data were provided by the
Oregon Climate Service, Oregon State University, Corvallis, Oregon. For personal,
emotional support with respect to completion of this thesis, I would like to express my
appreciation to D. Rosenberg, S. De Stefano, C. Brauderick, R. Olsen, R. Bjork, D.
Anderson, D. Twombly, 0. Schumacher and Clyde.
TABLE OF CONTENTS
INTRODUCTION
1
STUDY AREA
5
METHODS
Study Animal
Habitat Characteristics
Trapping Procedure
Data Analysis
9
9
9
10
RESULTS
Population Size, Growth, and Density
Reproduction and Recruitment
Movements
Survival
Habitat Characteristics
Mass Change
17
17
18
21
21
23
25
DISCUSSION
26
LITERATURE CITED
34
11
ii
LIST OF FIGURES
Figure
Page
1.
Daily maximum and minimum temperatures (C) and weekly precipitation (cm),
at Hyslop Crop Science Field Laboratory, Benton County, Oregon, 27
September-31 March 1995.
6
2.
Habitat fragmentation treatments used for experiment on over-winter demography
of gray-tailed vole populations, Hyslop Crop Science Field Laboratory, Benton
County, Oregon, 27 September 1994-31 March 1995.
7
3.
Mean (± SE) population size (a) and population growth rate (b) for gray-tailed
vole populations in continuous and fragmented habitat autumn and winter,
Hyslop Crop Science Field Laboratory, Benton County, Oregon, 27 September
1994-31 March 1995.
19
4.
Cumulative number of gray-tailed vole recruits (mean ± SE) for populations
in continuous and fragmented habitat during autumn, at Hyslop Crop Science
Field Laboratory, Benton County, Oregon, 27 September 1994-21 December
1994
20
5.
Maximum distance moved (mean ± SE) by male (top) and female (bottom) graytailed voles in continuous and fragmented habitat, at Hyslop Crop Science Field
Laboratory, Benton County, Oregon, 27 September 1994-31 March 1995.
22
6.
Gray-tailed vole survival probabilities (± SE) in continuous and fragmented
habitat at Hyslop Crop Science Field Laboratory, Benton County, Oregon, 27
September 1994-31 March 1995.
iii
24
PREFACE
Current concern over the large scale disruption of natural habitats worldwide has
led many scientists to develop research questions regarding the effects of habitat
fragmentation. Knowledge of patterns and processes across landscapes is necessary for
careful planning of land and resource use. However, direct experimentation and
hypothesis testing is difficult when conducting studies at the landscape level because
large-scale manipulation of habitats is often impractical or unethical (Turner 1989,
Hanski 1994). Conducting small scale experiments may be one way to discover
mechanisms and processes influencing populations at larger landscape scales.
Controlled experiments on species amenable to manipulative treatments may
serve as experimental model systems (EMS) for wildlife species that are less amenable to
experimentation (Ims and Stenseth 1989, Wiens and Milne 1989, Ims et al. 1993).
Advantages of using an EMS at a small scale include: (1) both population and individual
responses can be studied closely, (2) observations can be made with a level of detail that
may be difficult to attain at a broader scale, (3) larger sample sizes are available to
provide a more accurate representation of the phenomena under investigation, and (4)
treatments may be replicated with relative ease (Weins and Milne 1989, Ims et al. 1993).
However, disadvantages include: (1) species that have small space requirements may not
be comparable to those that have much larger area requirements, (2) species that can be
studied in small scale manipulated habitats may not be sensitive to habitat fragmentation,
and (3) results obtained from simplified experimental systems may not transfer to more
iv
complex landscape and ecosystem scales (Addicott et. al. 1987, Lord and Norton 1990).
However, if interpreted with caution, results from EMS studies can provide a tool useful
for scientific inquiry which provides information that remains unaddressed by computer
simulation models and larger, observational, landscape-level studies.
My experiment used gray-tailed voles (Microtus canicaudus) as an EMS in order
to reveal processes and mechanisms affecting population dynamics in fragmented
landscapes. Several aspects of gray-tailed vole ecology demonstrate their suitability as an
EMS. Voles have intrinsic value as a small mammal species, considerable existing data
on congeners for comparative or predictive purposes, almost worldwide distribution,
small size and low-vagility, populations which can be easily maintained on relatively
small plots, and habitat which can be manipulated into any desired mosaic. Additionally,
aspects of gray-tailed vole biology are comparable to other vertebrate species. For
example, females are territorial, they have a polygynous mating system, males and
females use space differently, and dispersal is male-biased (Ims et al. 1993, Wolff et al.
1994).
Gray-tailed voles are a common grassland species of Oregon's Willamette Valley.
Their preferred habitats in the valley are grassland and agricultural fields which are
frequently disturbed through cultivation or by fire. Because this species has evolved
within such ephemeral habitats, it is likely well adapted to disturbance (Verts and
Carraway 1987), and therefore may be less responsive to fragmentation than other
species. However, little is known about how gray-tailed vole populations respond to
human induced habitat disturbance (Verts and Carraway 1987). Edge et al. (1995)
reported that vole populations experienced negative impacts from mechanical mowing of
their habitat. Thus, the ability to experimentally fragment the habitat of this species and
closely monitor response may reveal important information related to habitat
fragmentation effects. Testing landscape level questions with smaller, experimental
systems, such as this, may become an important aspect of modeling or testing
management plans for conservation of other species. Limitations of conclusions drawn
from small scale experiments must be recognized for them to be a valuable conservation
tool.
vi
OVER-WINTER DEMOGRAPHY OF THE GRAY-TAILED VOLE (MICROTUS
CANICAUDUS) IN FRAGMENTED AND CONTINUOUS HABITATS
INTRODUCTION
The current unprecedented loss and fragmentation of natural habitats through
human activity is the most serious threat to biodiversity (Wilcox and Murphy 1985, Soule
1986). Rapid and severe declines in wildlife populations have been directly attributed to
habitat loss. However, effects of habitat fragmentation on wildlife populations have been
slower to appear and more difficult to discern (Morrison et al. 1992). Traditionally,
ecotones between habitat types created through habitat modification were considered
beneficial to wildlife (Leopold 1933). Recently however, large scale disruption of
contiguous habitats has been shown to adversely affect species that require large,
contiguous habitat areas (Harris 1988). Understanding the consequences of loss and
fragmentation of natural habitats is essential for maintaining viable populations of
wildlife species and preserving biodiversity (Morrison et al. 1992, Robinson et al. 1992).
Maintaining viable populations of wildlife species requires sufficient resources
and adequate environmental conditions for foraging, cover, reproduction and dispersal of
animals at a range of temporal and spatial scales commensurate with their life-history
patterns and processes (Morrison et al. 1992). The amount and spatial arrangement of
available habitats influence how species may use an area, and how that area may be
maintained for viable populations of a species. Habitat fragmentation reduces the total
amount of suitable habitat for a species in a landscape and apportions the remaining
habitat into smaller patches. The remaining patches of suitable habitat are often isolated
2
within a matrix of unsuitable or inhospitable habitat types (Forman and Godron 1981,
Wilcove et al. 1986, Saunders et al. 1991). Additionally, remnant habitat patches have a
larger proportion their area influenced by the adjacent matrix, described as "edge" habitat
(Harris 1988, Yahner 1988).
Currently, most of what is known about habitat fragmentation effects has been
derived from observational studies of populations in previously fragmented environments
(Gottfried 1979, Middleton and Merriam 1981, Henderson et. al. 1985, Verboom and van
Apeldoorn 1990, van Apeldoorn et al. 1992). These studies provide data regarding the
patterns and dynamics of patch occupancy. However, it is difficult to make inferences
regarding the behavioral and demographic mechanisms that produce the observed
patterns because these relationships may be merely correlational and contain confounding
factors (Hanski 1994). Often only observational data can be collected because large-scale
experimentation, requisite for determination of responses to habitat fragmentation, would
be unethical or impractical (Hanski 1994, except see Bierregaard 1992). Recent
approaches testing predictions about population response to fragmentation have used
small scale experimental designs and attempted to control patch size (Gaines et al. 1992,
Robinson et al. 1992), connectivity (LaPolla and Barrett 1993), and amount of edge
(Harper et al. 1993). These approaches allow for hypothesis testing insight into
mechanisms that may underlie the pattern and dynamics of populations in fragmented
environments.
In summer 1994, Wolff et al. (1997) conducted an experiment that monitored
demographic and behavioral responses of gray-tailed voles (Microtus canicaudus) to
3
habitat loss and fragmentation. The study tested two hypotheses: (1) habitat loss and
fragmentation would negatively impact gray-tailed vole demography, and (2)
fragmentation would cause voles to restrict their movements and reduce their home range
size. Their results indicated that at the time of fragmentation, vole populations were
sufficiently flexible to accommodate a 70% reduction in habitat. Population density
estimates were greater in fragmented habitats, than in continuous habitats of equal area,
or control enclosures. Peak densities were 2,880 animals/ha in fragmented habitats, as
opposed to 545 animals/ha in control areas. In fragmented habitat voles reduced
frequency and distance moved, and animals exhibited a home range size reduced by
>50%. However, these results may have been confounded by other factors such as
seasonal effects, or effects resulting from high-density populations. Habitat
fragmentation effects may become more discernable when resources are scarce rather
than abundant. Therefore, I examined the demography of gray-tailed vole populations
over-winter in both continuous and fragmented habitat.
Specifically, my central objective was to conduct a replicated field experiment to
compare the over-winter demography of gray-tailed voles in continuous and fragmented
habitats. Winter poses harsh conditions for voles because the vegetation that provides
food and cover for voles is greatly reduced during this season. Lack of cover may
increase predation pressure. Hawks, owls, coyotes (Canis latrans), weasels (Mustela
spp.), and feral cats (Felis domesticus) were all present in the experimental area. In
addition, wet and cold climatic conditions may create stresses not present during other
seasons. No experimental studies have examined the effects of fragmentation during
4
non-breeding periods. Yet, resource availability during seasonal "bottlenecks" may be an
important factor determining size of the potential breeding population the following
season, and may consequently affect population persistence.
First, I hypothesized that habitat fragmentation would adversely affect vole
population density and growth, recruitment, and reproductive activity. Secondly, I
hypothesized that individual movement patterns would be more restricted in fragmented
habitat than in continuous habitat, and that this difference would be more pronounced for
male voles, which have larger home ranges than females. Finally, I hypothesized that
survival rates would be higher for animals in continuous habitat than in fragmented
habitat, and that this difference would be sex-specific, with female voles exhibiting
higher survival rates than males. I expected movement across the matrix area to expose
animals to potential predation and reduce survival rate. Also, higher edge to area ratio in
the fragmented habitat may subject voles in those patches to microhabitat conditions
more extreme than those in continuous habitat.
5
STUDY AREA
This experiment was conducted at Oregon State University's Hyslop Crop Science
Field Laboratory, approximately 10 km north of Corvallis, Oregon. The site has an
elevation of approximately 70 m, level topography and is surrounded by agricultural
fields. Weather at the site during the study period was characterized by high levels of
precipitation and cool temperatures. A total of 111.5 cm of precipitation was recorded at
the study site, with 14.7 cm of the total occurring as snow; 47.8 cm of the total (2.0 cm as
snow) occurred during the autumn period (27 Sept-21 Dec) and 63.7 cm (12.7 cm as
snow) occurred during the winter period (22 Dec-31 Mar). Temperatures ranged from 30
C to -2.2 C during autumn, and between 22.8 C and -9.4 C during the winter (Fig. 1).
These conditions represent typical winter weather in the Willamette Valley of Oregon.
Eight 0.2-ha (45 x 45 m) small mammal enclosures were used for this experiment.
Mammal enclosures were constructed of galvanized sheet metal extending approximately
1 m above the ground and 0.6-1.0 m below ground level to prevent escape or entry by
burrowing rodents. Each enclosure was planted with alfalfa (Medicago sativa) in spring
of 1991. Alfalfa in each enclosure covered 43 x 43 m, with a 1-m strip of bare ground
maintained along the inside of the fence. In 1994, four replicate enclosures were
randomly selected for each of two fragmentation treatments, each with equal area of
habitat (625
m2)(Fig. 2): one continuous 25 x 25-m habitat patch surrounded by a 10-m barren strip;
and 25 small (5 x 5 m or 25 m2 ) patches of habitat, each separated by 4 m of bare ground.
30
daily high
6
daily low
i
20
10
-10
20
rain
snow
15
III 111111111111111111111111
r-F1
,z,s,t,
Q.
c.e,
Figure 1. Daily maximum and minimum temperatures (C) and weekly precipitation (cm),
at Hyslop Crop Science Field Laboratory, Benton County, Oregon, 27 September-31
March 1995.
7
Fragmented
habitat
Continuous
habitat
Patch = 5 x 5 m
Patch = 25 x 25 m
Trap Station Interval = 4.3 m
Trap Station
interval = 3 m
Interpatch
distance = 4 m
Figure 2. Habitat fragmentation treatments used for experiment on over-winter
demography of gray-tailed vole populations, Hyslop Crop Science Field Laboratory,
Benton County, Oregon, 27 September 1994-31 March 1995. Black dots represent trap
stations; shaded areas represent alfalfa habitat.
8
Herbicide was applied to the untreated alfalfa habitat on 1 July 1994. To clear the
areas around and between the patches, the dead alfalfa was mowed, raked and removed
from the enclosures on 22 July 1994. This treatment removed two-thirds of the total area
covered by alfalfa in each enclosure, leaving a matrix of bare soil devoid of cover and
food, which is unsuitable vole habitat (Cole 1978, Getz 1985). Matrix areas were
maintained by biweekly mowing, until the alfalfa became dormant for the season. On 30
August 1994, prior to the initiation of the experiment, the areas of remaining alfalfa
habitat were mowed to a height of 25 cm in order to stimulate new growth during the
autumn.
Each of the small patches in the fragmented habitat was approximately one half
the size of an average female home range (.g = 56 m2) and one fourth the size of an
average male home range (1 = 94 m2), whereas the area of continuous habitat was
approximately equivalent to 11 female home ranges and 7 male home ranges (Wolff et al.
1994). The 4-m strip of bare ground between small patches was perceived as a bather by
the voles, and reduced vole movements during the summer experiment (Wolff et. al.
1997).
9
METHODS
Study Animal
The gray-tailed vole is a common grassland species of Oregon's Willamette
Valley, and is similar in appearance, behavior, and ecology to other Microtus species,
especially the closely related M. montanus (Wolff 1985, Verts and Carraway 1987).
Demographic, reproductive, and behavioral parameters of gray-tailed voles have been
monitored in field enclosures for several breeding seasons (Wolff et al. 1994, 1996; Edge
et al. 1995, 1996; Schauber et al. 1997). Gray-tailed voles have small space requirements
relative to most mammals, with male home ranges overlapping those of one or more
females (Wolff et al. 1994). Because these animals are small in size and have low
vagility, populations can be easily maintained on small plots. Also, the preferred habitat
of this vole (grassland and agricultural fields) can be manipulated into any desired
mosaic. Breeding occurs from March through November, modal litter size is four,
juveniles are weaned at 15-18 days, and females may start breeding when they reach 18 g
(18-20 days old)(Wolff et al. 1994).
Habitat Characteristics
I measured habitat characteristics 3-4 October 1994. I recorded alfalfa height
(cm), and estimated cover using a Daubinmire (1959) frame (0.1 m2). Three cover types,
green alfalfa, dead alfalfa stems, leaves and litter, and bare ground were recognized. I
recorded the percent area occupied by each cover type within the frame. The frame was
10
placed at five locations within each patch, one at the center and one at each of the four
cardinal directions, 2 m from the center frame. In the continuous habitat, 25 imaginary
patches were established in a 5 x 5 grid, and the same observations recorded. This totaled
125 observations of height and cover within each enclosure.
Trapping Procedure
Fragmented habitat enclosures had 100 trap stations set in a 10 x 10 array with 3
m spacing between stations within each patch, and 6 m between stations in adjacent
patches including the 4-m interpatch matrix. Each patch contained four traps, at least 1 m
from the patch edge in any direction. No traps were placed in the matrix areas, because I
was strictly interested in between patch movement, and I assumed that voles would not
use the matrix area as habitat. Continuous habitat enclosures had 56 trap stations: 36
stations in a 6 x 6 array within the large patch, with a 4.3-m spacing between stations; and
20 trap stations along the perimeter of the enclosure fence, at approximately 8-m spacing.
In fragmented habitat one Sherman live trap (7.5 x 9.5 x 25.5 cm) was placed at each
station, for a total of 100 traps. In continuous habitat, two Sherman traps were placed at
each of the 36 stations within the large patch, and one trap was placed at each of the
perimeter stations for a total of 92 total traps. Voles were trapped for three consecutive
days (defining the trap-period) every two weeks from 27 September 1994 (with the
exception of the week of 11 Oct) until 31 March 1995. Traps were baited with sunflower
seeds and oats, set in the morning, and checked in the evening during each trapday.
Traps were locked open, and pre-baited when not in use. Trapping effort was
11
concentrated during daylight hours because voles exhibit diurnal activity patterns during
the autumn (Drabeck 1994), and to minimize trap mortality during long, cold winter
nights.
During the week of 13-16 September 1994 all resident voles were trapped and
removed from the enclosures. These voles served as the population pool from which 12
pairs of adult (25-35 g) voles were released into each enclosure on 17 September 1994.
No vole was released into an enclosure from which it had been removed. Each vole had a
numbered aluminum ear tag in its right ear at the time of release. All voles subsequently
captured were ear-tagged. I recorded tag number, body mass, sex, reproductive
condition, and trap location for each capture, and animals were released where they were
captured. All newly tagged animals were considered recruits and I assumed that they
were born within the enclosures. Females were considered to be in reproductive
condition if they were lactating, pregnant, or had widely open pubic symphyses when
captured.
Data Analysis
I determined values for population size, density, population growth, survival rate
and movements for each enclosure and trap-period of the study. Values for reproductive
activity and recruitment were determined only for the autumn period because there was
no reproductive activity or recruitment in populations for any of the enclosures during the
winter period.
12
I used program CAPTURE (Rexstad and Burnham 1992), under the closed
population model incorporating heterogeneous capture probabilities among animals, to
estimate population size and density (Chao 1988). This model was chosen because it
performed best during a trapping experiment, in the same field enclosures, in which
population sizes were estimated from nine known-size populations representing a range
of densities, from 30-90 animals/enclosure (Manning et al. 1995). In this experiment,
however, densities were often <30 animals/enclosure. For values >14 animals/enclosure,
CAPTURE performed well, producing population estimates with low variability, but
when populations declined to <14, population estimates generated by CAPTURE were
highly variable. I compared the values from CAPTURE with values generated from a
minimum number alive (MNA) analysis. MNA analysis counts individuals not caught
during a particular trap-period, as present within that week, if that individual is caught
during a subsequent trapping effort. MNA underestimated population size when
populations were >14 animals/enclosure, but performed well when population size was
<14 animals/enclosure. For each enclosure, I used the population estimates from
CAPTURE when estimates were >14, and I used MNA estimates when population sizes
were <14 animals/enclosure. Population sizes were transformed to the natural log for the
analysis. Because values were natural log transformed, when population size was zero in
an enclosure, I used 0.5 as the estimate for that enclosure. I calculated the rate of
population growth as the change in the natural log of population size between trap-
periods. Because both treatments had equal habitat area, I used population size for the
analysis, rather than density. I calculated 95% confidence intervals for the difference
13
between means of population size for each trap-period. I present confidence intervals for
trap-periods with the greatest and least difference between means to evaluate power of
statistical tests.
I used four measures of reproductive performance: (1) the proportion of adult
females in reproductive condition, (2) proportion of total voles captured that were
recruits, (3) the cumulative number of recruits produced over the breeding period, and (4)
the number of recruits per adult female. The number of recruits per adult female was
calculated using the number of newly tagged voles each trap period divided by the total
number of adult females in that enclosure four weeks earlier. The four-week time lag
allows offspring to reach trappable size (Wolff et al. 1994). Proportional values were
arcsin square-root transformed for analysis. The cumulative number of recruits and the
number of recruits per adult female were natural log transformed for analysis.
To determine effects of fragmentation treatments on movements, I examined the
mean maximum distance moved (MMDM) by voles during each trap period. MMDM
for each enclosure and sex was calculated as the average of the maximum straight-line
distances animals moved between capture locations within a trap-period (Wilson and
Anderson 1985). Values were generated from program CAPTURE (White et al. 1978)
and natural log transformed for analysis.
I estimated sex-specific survival rates using derivations of the Cormack-Jolly-
Seber mark-recapture methodology (Cormack 1964, Jolly 1965, Seber 1965). Programs
RELEASE (Burnham et al. 1987) and SURGE (Pradel and Lebreton 1991) were used for
survival modeling. The modeling philosophy espoused by Burnham et al. (1987) and
14
Lebreton et al. (1992) was adopted and the goodness-of-fit of each model and the number
of parameters required was evaluated. "Good" models are defined as those that fit the
data, characterized by a small numbers of parameters and reflect current understanding of
the species. Specific hypotheses can be tested by comparing goodness-of-fit among
competing models. The following approach was used: (1) populations within enclosures
were modeled separately with an emphasis on sex-specific differences, and (2) treatment
effects on survival were explicitly tested by comparing relative fit among models. The
most parsimonious models were identified using Akaike's Information Criterion (Akaike
1973; see also Lebreton et al. 1992:83-85). This approach has been used and is further
explained by Paradis et al. (1993) in estimating sex- and age-specific survival rates of the
Mediterranean vole (Microtus duodecimcostatus) in Europe.
I used the Statistical Analysis System (SAS Version 6.05; SAS Institute 1990) for
all other analyses. Population size and population growth rates were tested for treatment
differences using multivariate repeated measures analysis of variance. I used the mean
value for the four replicates in each treatment for these analyses. My analyses were
divided into two distinct time periods because there were insufficient degrees of freedom
to perform the repeated measures analysis on all 13 trap periods combined, and because
reproduction stopped in autumn. The first six trap-periods used in the analysis were
defined as autumn (27 Sep1994-21 Dec 1994); I defined the next seven trap-periods (22
Dec 1994-31 Mar 1995) as winter.
Using data from the autumn period, I tested for effects of fragmentation and time
on reproductive activity of females and recruitment. I used a multivariate repeated
15
measures analysis of variance to determine if these measures differed among treatments
during any trap period of the study. Additionally, I performed a repeated measures
analysis of variance on the cumulative number of recruits that entered the population
during the autumn period. Density estimates during autumn were well below those
achieved during the peak breeding season, summer, when mean density in continuous
habitat was 1,056 voles/ha and 2,880 voles/ha in fragmented habitat (Wolff et al. 1997).
Even at the high density levels recorded in summer, population size was not a significant
covariate in statistical analysis (Wolff et al. 1997). For the autumn reproductive data,
population density was assumed to be insufficiently high to produce density-dependent
effects, which could confound treatment effects. Additionally, the majority of the
reproductive data did not have a type-H covariance matrix structure that would allow for
a valid univariate whole-plot/split-plot analysis incorporating the use of density as a
covariate (Huynh and Feldt 1970).
I analyzed effects of fragmentation and time on MMDM using a univariate
analysis with fragmentation treatment as a whole-plot factor and time as a split-plot factor
(Huynh and Feldt 1970). Males and females were treated separately using the mean
number of captures per animal in each enclosure as a covariate. The movement data had
a type-H covariance matrix structure which allowed for a valid univariate wholeplot/split-plot analysis (Huynh and Feldt 1970) incorporating use of number of
captures/animal and population density as covariates. Population density was included as
a covariate because individual movement of small mammals can be density-dependent
(Wolff 1985). The analysis of MIVIDM was completed for the first 11 of the 13 trap-
16
periods. During the final two trap-periods, populations in both treatments had declined to
one individual/enclosure of either sex. Thus, when there was <1 individual/replicate
within a treatment, I excluded those data from the analysis.
I analyzed habitat characteristics by performing a series of 2-sided t-tests to assess
differences between continuous and fragmented habitat types. I compared the difference
in means for alfalfa height (cm), and percent cover of (1) green alfalfa, (2) dead alfalfa
stems, leaves and litter, and (3) bare ground, from the combined measures for the four
replicates in each treatment.
Finally, as a indirect measure of resource quality within the enclosures, I analyzed
the mass change of adult voles that were captured over >5 trap-periods, excluding
pregnant females. I used the mass of the animal when first captured, the mass of the
animal when it was last captured and the change in the two mass measurements for the
analysis. I used a t-test to assess the difference in mean mass change of animals in
continuous compared to fragmented habitat treatments.
17
RESULTS
I captured 299 voles 2,555 times during 33,792 trap-nights from 27 September
1994 through 31 March 1995.
Population Size, Growth, and Density
Vole populations declined for the first six weeks following release, but increased
slightly from 27 October to 22 November (Fig. 3a). Density estimates in continuous
habitat reached a mean maximum of 380 animals/ha (SE = 7.7); in fragmented habitat the
mean maximum density was 356 animals/ha (SE = 17.7). After 22 November all
populations declined throughout the remainder of the fall and winter, and became extinct
by 28 March. Population size in fragmented enclosures was more variable than in
continuous enclosures throughout the winter period. Although populations in fragmented
enclosures were lower than in continuous habitats during the first 10 weeks, I observed
no time by treatment interactions during autumn (F52= 1.179, P = 0.518), but means did
differ over time (F52 = 10.563, P = 0.089). During the winter period, I observed no time
(F61 = 11.479, P = 0.222), or interactive effects (F6,1 = 0.128, P = 0.969) on population
size. The greatest difference between the means for population size, 6.75 (95% C.I. -5.5
to 19), occurred during the third trap-period (8-10 Nov 1994), the smallest difference
between means, 0.125 (95% C.I. -0.34 to 0.59), occurred during the last trap-period
(28-31 Mar 1995).
18
Population growth rates were positive during only two intervals of the study,
between the second and third trap period, and between the third and fourth trap period in
both treatments (Fig. 3b). There were no differences in mean population growth rate over
time during the autumn period (F52 = 3.60, P = 0.232), however, growth rates did differ
over time during the winter period (F52 = 16.02, P = 0.060). I observed no time by
treatment interactions in population growth rates for autumn (F52= 0.322, P = 0.867) or
winter (F5a = 0.25, P = 0.921).
Reproduction and Recruitment
The proportion of female voles displaying reproductive activity averaged 0.31
(range 0.22-0.49) throughout the autumn for all enclosures. Female reproductive activity
did not differ over time (F52 = 3.437, P = 0.241) nor was there a time by treatment
interaction (F5a = 1.361, P = 0.475). The mean proportion of captures composed of
recruits/week averaged 0.14 (range = 0.02-0.21) for all the enclosures, and did not differ
through time (F52 = 4.912, P = 0.178) nor were there interactive effects (F52 = 0.201,
P = 0.936). The mean number of recruits/adult female/week was 0.46 (range 0.28-0.57).
No difference in recruits/adult female was apparent over time (F34= 3.673, P = 0.121),
nor were there interactive effects (F34= 0.654, P = 0.621). The cumulative number of
recruits increased over the autumn period (F52 = 13.00, P = 0.073); although continuous
habitat enclosures had a higher mean number of recruits overall (Fig. 4), there were no
time by treatment interactions (F52 = 0.155, P = 0.959). Variability in the cumulative
19
0.6
111111111(11
0.4
0.2
0.0
-0.2
-0.4
-0.6
-0.8
-1.0
-1.2
-1.4
I
I
I
A
ct,
4,-,
,
el.
I
c,
e
CD
I
i
I
I
I
c3
I
I
I
\(0
e,S
sz>
(z,
<(.2,
et,c4,2e
Figure 3. Mean (± SE) population size (a) and population growth rate (b) for gray-tailed
vole populations in continuous and fragmented habitat autumn and winter, Hyslop Crop
Science Field Laboratory, Benton County, Oregon, 27 September 1994-31 March 1995.
20
4%
0°
\4°
4(1,
'0°
0(a
Figure 4. Cumulative number of gray-tailed vole recruits (mean ± SE) for populations in
continuous and fragmented habitat during autumn, at Hyslop Crop Science Field
Laboratory, Benton County, Oregon, 27 September 1994-21 December 1994.
21
number increased over time and in general was greater in the fragmented habitat than in
the continuous habitat.
Movements
Mean maximum distance moved for voles over winter did not differ between
fragmented and continuous habitat (F14 = 0.406, P = 0.565), nor did MMDM differ
between male and female voles (F15= 0.454, P = 0.537). Movements of all voles
increased in both distance and variability from autumn through the winter (Fig. 5),
and this difference in MMDM was significant over time (F528= 6.687, P = 0.000). I
observed no two-way interactions between sex and fragmentation treatment (F15 = 0.014,
P = 0.912), between sex and time (F5,29 = 1.139, P = 0.363), nor between time and
fragmentation treatment (F528 = 0.630, P = 0.679). Finally, there was no three-way
interaction among sex, treatment and time (F529= 0.406, P = 0.841). Density and mean
number of captures/animal were included as covariates in all analyses of movements,
although neither covariate was significant (F14 = 0.414, P = 0.561; F14 = 0.078, P = 0.79,
respectively).
Survival
Initially, I modeled survival for male and female voles separately because I
suspected sex-specific differences in survival rates based on previous studies from gray-
tailed voles (Edge et al. 1995, 1996; Schauber et al. 1997; Wolff et al. 1997). However,
survival rates were only partially sex-specific. The final model of biweekly
22
0
I
I
c1,
coe9-
I
6
A
A
49.
061/4
4:-.
I
I
rt,(1/
4
N.°
0
0
V
I
Nc3
0eC,
I
I
Il<
Nc:
.c..
0.
bl
I
I
N
'b
lac
'Z'
key
N
I
6
(1,
ke0
Figure 5. Maximum distance moved (mean ± SE) by male (top) and female (bottom)
gray-tailed voles in continuous and fragmented habitat, at Hyslop Crop Science Field
Laboratory, Benton County, Oregon, 27 September 1994-31 March 1995.
23
survival (AIC = 1,543, 6 parameters)(Fig. 6) resulted in male survival differing between
habitat types; males in continuous habitat had slightly higher survival (0.73-0.88) than
males in fragmented habitat (0.58-0.88). Female vole survival rates were similar
between habitat types and were comparable to rates of males in fragmented habitats
(0.58-0.88). The 10 best models all had similar AIC values (range 1,542-1,544) and 6
parameters. The final model was chosen because it was more biologically informative;
changes in survival appeared to be weather related. Survival declined for all animals
during two periods, the first before and after 19 December 1994 and the second before
and after 16 February 1995. Survival rates for male voles in continuous habitat seemed
relatively stable and never declined below 0.73. The survival rates of males in
fragmented habitat fluctuated, rebounding from the first decline, but declining again and
remained at a depressed level (0.58) during the last three intervals of the study. Female
vole survival rates were lower for two intervals following the first major decline in
survival, rebounded, then declined again following 16 February 1995.
Habitat Characteristics
The mean height of the alfalfa was 23.3 cm (SE = 0.28, range 17-33) and did not
differ between treatments (t = 0.17, 6 df, P = 0.87). Twenty-seven percent of the total
cover was green alfalfa (range 14-47%) at the time the observations were recorded, and I
detected no difference between treatments (t = 0.48, 6 df, P = 0.65). Alfalfa litter and
dead stems composed an average of 65% of the cover (range 58-81%), and bare ground
comprised only 1% of the cover (range 0-4), neither of these variables were significantly
24
A
A`b
4)-%
c,`"
cp('
cI''
IP 1
n3'
4f*
re?
4
43
Figure 6. Gray-tailed vole survival probabilities (± SE) in continuous and fragmented
habitat at Hyslop Crop Science Field Laboratory, Benton County, Oregon, 27 September
1994-31 March 1995.
25
different between treatments (t = -0.27, 6 df, P = 0.80 and t = -1.21, 6 df, P = 0.27,
respectively).
Mass Change
Analysis of the mass change of adult voles, excluding pregnant females, resulted
in an average mass increase of 1.4 g (range 1.2-9 g) for all voles over the period of the
study. Voles in continuous habitat were slightly heavier at first capture than voles in
fragmented habitat (t = 2.24, 51 df, P = 0.03), however, on the last capture, voles in the
fragmented habitat were not different in mass from those in continuous habitat (t = -0.02,
49 df, P = 0.99). Voles in fragmented habitat increased mass, while mass of voles in
continuous habitat remained stable. Thus, the change in mass differed between treatments
(t = -2.48, 43 df, P = 0.02), but this was due to the greater gain in mass by voles in the
fragmented treatment.
26
DISCUSSION
The over-winter demography of vole populations residing in fragmented habitat
did not differ substantially from populations in continuous habitat. Under both habitat
conditions, populations experienced declines in size and experienced negative growth
rates, limited reproduction, and minimal recruitment. The most dramatic result of my
experiment was the extinction of all populations in both habitat conditions. The proposed
hypotheses, namely that habitat fragmentation would adversely affect population
demography, was generally unsupported by this study. However, variation in the data
was greater under the fragmented habitat treatment than under the continuous habitat
treatment. Results from the over-winter period contrast with those from the previous
experiment conducted during summer in which fragmentation resulted in an increase in
vole densities and decreased movements (Wolff et al. 1997). Taken together, these
results suggest that winter may be a vulnerable period for gray-tailed voles, and that
seasonal bottlenecks may be a critical factor affecting the ability of populations to persist
through time.
Extinctions of all populations in this experiment demonstrates the vulnerability of
small populations. I began this experiment with 12 pairs of animals, or 24 individuals,
per enclosure to establish experimental populations. I anticipated that this initial
introduction would be sufficient because previous experiments (Edge et al. 1995, 1996;
Schauber et al. 1997; Wolff et al. 1997) during the spring and summer in the same
enclosures used only six pairs of animals per enclosure to establish sizable populations
27
(range 29-305 animals/enclosure) that always persisted over-winter (J. Wolff, pers.
comm.). Populations in both treatments experienced some growth during the autumn, but
during the winter, growth rates were consistently negative for all populations. The initial
growth in autumn was insufficient to allow population persistence through the winter in
either habitat, and was unable to produce populations large enough to contribute to
reestablishment during early spring. Small populations are subject to high rates of
extinction through stochastic events (Shaffer 1981). Populations in this experiment
remained small throughout the study, and were vulnerable to both demographic and
environmental stochasticity. Richter-Dyn and Goel (1972) suggest that a population size
of 10-15 individuals is a threshold size below which extinction due to demographic
stochasticity is likely. Additionally, environmental stocasticity, cold winter weather and
predators, probably contributed to extinction. Apparently, the populations in this
experiment fell below a level that would have allowed them to persist despite stochastic
influences.
Measures of reproductive performance illustrate the influence of demographic
factors on the populations in this study. Reproduction during the autumn was lower than
anticipated. Wolff et al. (1994) reported that 78-92% of female gray-tailed voles were in
reproductive condition from May through October, and that breeding activity occurred
from March to December, with a lull in January and February. During the autumn period
of this study only 31% of females were reproductive, and breeding ceased in early
December and never resumed during the rest of the study period (through the end of
March). Recruitment was also low, the modal litter size for gray-tailed voles in the field
28
is 4.4 (Wolff et al. 1994), yet an average of only 0.46 recruits per adult female per week
entered the population in either treatment. Recruitment in both treatments was
insufficient for population persistence, resulting in eventual extinction.
Individual behavior and activity patterns of voles probably further increased the
vulnerability of populations in this experiment. Vole movements demonstrated an
unexpected pattern, voles in the fragmented habitat did not restrict their movements to
specific patches and did not appear to perceive the bare ground between fragments as a
barrier. Wolff et al. (1997)reported that voles responded to fragmentation by restricting
movements, with an apparent perception of the areas between fragments of habitat as
barriers. Voles in fragmented habitat did not restrict their movements, instead voles in
both habitat types showed a pattern of increasing distance moved throughout the study.
This pattern of movement may reflect the breakdown of territoriality with the cessation of
breeding (Wolff 1985). Increased social tolerance among individuals during the nonbreeding season may have allowed expansion of home ranges and increased movements
(Madison and Mc Shea 1987). Alternatively, scarce and widely dispersed resources may
have induced voles to move greater distances over time in order to procure necessary
resources (Diffendorfer et al. 1995). Longer, wide-ranging movements by voles may
have increased their exposure to predation and reduced survival rates.
Survival rates appeared to be influenced by predation and weather conditions.
Residing in fragmented habitat seemed to depress survival rates for male voles, but did
not effect female vole survival rates. Pronounced declines in survival for all voles in this
experiment generally followed periods of harsh winter weather conditions, including
29
below-freezing temperatures and snowfall. Halle (1995) suggests that voles may increase
their activity level in response to cold temperatures, because energy demands increase as
temperatures decline. Madison (1985) reported that voles increased movements on days
following snowfall. Exposure to extreme cold may be a major source of risk to small
mammals in winter because they may not be able to meet increased energy demands
(Anderson 1986). Further, increased activity, due to metabolic needs for food, combined
with little cover, may create a situation in which predators can affect vole survival and
persistence over the winter (Pearson 1985). Snow-covered surfaces may increase the risk
of predation as well (Anderson 1986), because predators can easily detect voles both on
and under the snow surface. Although I am unable to determine from my study whether
declines in survival rates reflected direct exposure to weather, or to predation, seasonal
conditions significantly effected vole survival rates regardless of the habitat treatment.
Habitat characteristics could be another aspect contributing to eventual population
extinctions. Graminoid and herbaceous vegetation serves as both the major food source
and as the primary cover for most species of Microtus (Getz 1985). Species occupying
habitats in which green vegetation is seasonally absent or reduced in quantity feed on
dead plant material, seeds, and roots (Getz 1985). Mass of voles in both treatments
increased over the winter period, suggesting that there was not a shortage in available
food in either habitat condition. Cover may have been a more critical component of
habitat for voles during winter for at least two reasons. First, during winter voles shift
their activity to a diurnal pattern (Drabeck 1994) and consequently, are exposed to diurnal
raptor predation (Madison 1985). Furthermore, Reynolds and Gorman (1994) reported
30
that despite intense levels of predation by raptors, voles continued to exhibit diurnal
activity. I found no differences in cover between continuous and fragmented habitat.
The average vegetation height at the beginning of this experiment was 24 cm in the
continuous treatment, and 23 cm in the fragmented treatment, both dramatically less than
summer vegetation, which was >1 m tall. Furthermore, following senescence of the
alfalfa, foraging by voles probably continued to reduce the amount of cover available
inside the enclosures (Pearson 1985). I have no direct measure of predation at the field
site. However, in two searches of the enclosures, raptor castings containing 10 ear tags
from my experimental animals were found (J. Peterson, unpubl. data). Further, a shorttailed weasel (Mustela ermina) was captured in a trap inside one of my experimental
enclosures during the study, and on two occasions feral cats (Felis domesticus) were
chased from inside of the enclosures. Pearson (1985) indicates that such predator
assemblages will continue to kill voles, even when vole populations are low. My
observations provide no evidence, however, that vole populations in fragmented habitat
were more vulnerable to predation than those in continuous habitat, as predicted.
Secondly, vegetative cover moderates the microclimate (humidity and
temperature) within the habitat, which may reduce physiological stress on voles (Getz
1985). Although voles can reduce their activity in response to cold weather, voles
maintain high metabolic rates and do not hibernate during the winter (Madison 1985).
Many species of Microtus are hypothesized to aggregate in winter in order to obtain
thermoregulatory benefits of group nesting (Madison 1984). Little is known about the
winter ecology of the gray-tailed vole (Wolff et al. 1994), and it is unknown whether this
31
vole depends upon group nesting to conserve energy. Madison and Mc Shea (1987)
conclude that even average winter conditions could cause wide-spread mortality due to
hypothermia when voles nest alone. Again, the present data do not support the
hypothesis that voles in fragmented habitat experienced more extreme microhabitat
conditions that those in continuous habitat.
The scale of fragmentation established between the two experimental treatments
may have been inappropriate to answer questions regarding the effects of habitat
fragmentation. A previous summer experiment indicated that voles perceived the
fragmented habitat treatment as a collection of patches, and that the total amount of
habitat was able to support viable populations (Wolff et al. 1997). However, over-winter
treatment conditions may not have been perceived as different by voles, and the amount
of habitat may have been too small to maintain population viability. The fragmentation
treatment was initially established at the individual level (Addicott et al. 1987), defined
by the summer home range of gray-tailed voles (Wolff et al. 1994), and may not represent
the home range of voles throughout an annual cycle. Home range size of Microtus
species often increase in the winter because of seasonal changes in resource availability
and spacing behavior (Madison and McShea 1987). Such temporal changes in habitat use
can influence how spatial characteristics of habitat are perceived (Addicott et al. 1987).
The extinction of populations in both treatments suggests that total habitat available may
have been too small, and that populations of voles may have been responding to habitat
loss, regardless of fragmentation pattern (Andren 1994). These results do not describe
definitive effects of habitat fragmentation between treatments, but they do demonstrate
32
that populations or sub-populations that occupy small, isolated areas are faced with high
rates of extinction (Gilpin and Soule 1986).
Alternatively, because the animals were artificially enclosed, they may have been
unable to locate suitable refugia (from weather or predation) within the confines of the
enclosures. However, in previous experiments in the same enclosures vole populations
persisted over-winter, suggesting that at least some areas of refugia exist within the
enclosures (J. Wolff, pers. comm.). However, fragmentation may often remove critical
areas of microhabitat that may be used only during certain times and for specific
purposes. It is critical to understand the entire life-history of an organism in order to
determine how removing and changing spatial arrangement of habitat on the landscape
will influence a population (Diffendorfer et al. 1995).
Although this study was of short duration, it focused on a vulnerable and critical
period for gray-tailed voles (Madison 1984). My over-winter results contrast markedly
with results from a study performed during the summer breeding season (Wolff et al.
1997). Even species that seem well adapted to disturbance, such as the gray-tailed vole,
may become sensitive to fragmentation due to temporal variation. Seasonal fluctuations
in environmental conditions and species requirements may create annual population
bottlenecks, which short-term studies may overlook. Population persistence will depend
on viability through such bottlenecks. This study, when contrasted with the results of
Wolff et al. (1997), lends support to the suggestion that habitat fragmentation research
should encompass several seasons and be conducted over the long-term (Andren 1994).
33
Small scale studies, such as mine, provide a way to directly test hypotheses
regarding habitat fragmentation. However, caution should be used when generalizing
results from a small scale to a larger scale (Murphy 1989). In order to apply results from
a small scale experiment to a larger scale, detailed understanding of species life-histories
and differences in the scale at which they use the landscape is critical (Diffendorfer et al.
1995). The idiosyncratic nature of many species and high levels of natural variability
may preclude direct application of theoretical or practical models to many real-world
situations (Shaffer 1981). Small scale studies, therefore, are probably more useful as tools
for constructing models or testing theories, rather than for making direct predictions or
generalizations to larger scales. In this respect, small-scale experimental studies provide
a link between theory, computer simulation models, and large-scale empirical research,
and may serve to improve scientific inquiry at all levels in diverse fields of research.
34
LITERATURE CITED
Addicott, J. F., J. M. Aho, M. F. Antolin, D. K. Padilla, J. S. Richardson, and D. A.
Soluk. 1987. Ecological neighborhoods: scaling environmental patterns. Oikos
49:340-346.
Akaike, H. 1973. Information theory and an extension of the maximum likelihood
principle. Pages 267-281 in B. N. Petran and F. Csaki, eds. International
Symposium on Information Theory, Second Edition. Akademiai Kiaki, Budapest,
Hungary.
Anderson, P. K. 1986. Foraging range in mice and voles: the role of risk. Canadian
Journal of Zoology 64:2645-2653.
Andren, H. 1994. Effects of habitat fragmentation on birds and mammals in landscapes
with different proportions of suitable habitat: a review. Oikos 71:355-366.
Bierregaard, R. 0., T. E. Lovejoy, V. Kapos, A. A. dos Santos, and R. W. Hutchings.
1992. The biological dynamics of tropical rainforest fragments. Bioscience
42:859-865.
Burnham, K. P., D. R. Anderson, G. C. White, C. Brownie, and K. H. Pollock. 1987.
Design and analysis methods for fish survival experiments based on releaserecapture. American Fisheries Society Monograph 5:1-437.
Chao, S. 1988. Estimating animal abundance with capture frequency data. Journal of
Wildlife Management 52:295-300.
Cole, F. R. 1978. A movement barrier useful in population studies of small mammals.
The American Midland Naturalist 100:480-482.
Cormack, R. M. 1964. Estimates of survival from the sighting of marked animals.
Biometrika 51:429-438.
35
Daubinmire, R. F. 1959. A canopy-coverage method of vegetational analysis. Northwest
Science 33:43-64.
Diffendorfer, J. E., M. S. Gaines, and R. D. Holt. 1995. Habitat fragmentation and
movements of three small mammals (Sigmodon, Microtus, and Peromyscus).
Ecology 76:827-839.
Drabeck, C. M. 1994. Summer and autumn temporal activity of the montane vole
(Microtus montanus) in the field. Northwest Science 68:178-184.
Edge, W. D., R. L. Carey, J. 0. Wolff, L. M. Ganio, and T. Manning. 1996. Effects of
Guthion 2S® on Microtus canicaudus: a risk assessment validation. Journal of
Applied Ecology 33:269-278.
Edge, W. D., J. 0. Wolff, and R. L. Carey. 1995. Density-dependent responses of graytailed voles to mowing. Journal of Wildlife Management 59:245-251.
Forman, R. T. T., and M. Godron. 1981. Patches and structural components for a
landscape ecology. Bioscience 31:733-739.
Gaines, M. S., G. R. Robinson, J. E. Diffendorfer, R. D. Holt, and M. L. Johnson. 1992.
The effects of habitat fragmentation on small mammal populations. Pages
875-885 in D. R. McCullough and R. G. Barrett, eds. Wildlife 2001: Populations.
Elsevier Science Publishers Ltd. Essex, England.
Getz, L. L. 1985. Habitats. Pages 286-309 in R. H. Tamarin, ed. Biology of New World
Microtus. American Society of Mammalogists Special Publication 8,
Gilpin, M. E., and M. E. Soule. 1986. Minimum viable populations: processes of species
extinction. Pages 19-34 in M. E. Soule, ed. Conservation biology: the science of
scarcity and diversity. Sinauer Press, Sunderland, Massachusetts.
Gottfried, B. M. 1979. Small mammal populations in woodlot islands. The American
Midland Naturalist 102:105-112.
36
Halle, S. 1995. Effect of extrinsic factors on activity of root voles, Microtus oeconomus.
Journal of Mammology 76:88-99.
Hanski, I. 1994. Patch occupancy dynamics in fragmented landscapes. Trends in
Ecology and Evolution 9:131-135.
Harper, S. J., E. K. Bollinger, and G. W. Barrett. 1993. Effects of habitat patch shape on
population dynamics of meadow voles (Microtus pennsylvanicus). Journal of
Mamma logy 74:1045-1055.
Harris, L. D. 1988. Edge effects and the conservation of biotic diversity. Conservation
Biology 2:300-332.
Henderson, M. T., G. Merriam, and J. Wegner. 1985. Patchy environments and species
survival: chipmunks in an agricultural mosaic. Biological Conservation
31:95-105.
Huynh, H., and L. S. Fe ldt 1970. Conditions under which mean square ratios in repeated
measurements designs have exact F-distributions. Journal of the American
Statistical Association 65:1582-1589.
Ims, R. A., and N. C. Stenseth. 1989. Divided the fruit flies fall. Nature 342:21-22.
Ims, R. A., J. Rolstad, and P. Wegge. 1993. Predicting space use responses to habitat
fragmentation: can voles Microtus oeconomus serve as an experimental model
system (EMS) for capercaillie grouse Tetrao urogallus in boreal forest?
Biological Conservation 63:261-268.
Jolly, G. M. 1965. Explicit estimates from capture-recapture data with both death and
immigration-stochastic model. Biometrika 52:225-247.
LaPolla, V. N., and G. W. Barrett. 1993. Effects of corridor width and presence on the
population dynamics of the meadow vole (Microtus pennsylvanicus). Landscape
Ecology 8:25-37.
37
Lebreton, J. D., K. P. Burnham, J. Clobert, and D. R. Anderson 1992. Modeling survival
and testing biological hypotheses using marked animals: a unified approach with
case studies. Ecological Monographs 62:67-118.
Leopold, A. 1933. Game management. Charles Scribner's Sons. New York.
Lord, J. M., and D. A. Norton. 1990. Scale and the spatial concept of fragmentation.
Conservation Biology 4:197-202.
Madison, D. M. 1984. Group nesting and its ecological and evolutionary significance in
overwintering microtine rodents. Pages 267-274 in J. Merritt, ed. Winter ecology
of small mammals. Carnegie Museum of Natural History Special Publication 10.
Madison, D. M. 1985. Activity rhythms and spacing. Pages 373-419 in R. H. Tamarin,
ed. Biology of New World Microtus. American Society of Mammalogists
Special Publication 8.
Madison, D. M., and W. J. Mc Shea. 1987. Seasonal changes in reproductive tolerance,
spacing and social organization in meadow voles: a microtine model. American
Zoologist 27:899-908.
Manning, T., W. D. Edge, and J. 0. Wolff. 1995. Evaluating population size estimators:
an empirical approach. Journal of Mammalogy 76:1149-1158.
Middleton, J., and G. Merriam. 1981. Woodland mice in a farmland mosaic. Journal of
Applied Ecology 18:703-710.
Morrison, M. L., B. G. Marcot, and R. W. Mannar'. 1992. Wildlife-habitat relationships.
The University of Wisconsin Press, Madison, Wisconsin.
Murphy, D. D. 1989. Conservation and confusion: wrong species, wrong scale, wrong
conclusions. Conservation Biology 3:82-84.
38
Paradis, E., G. Guedon, and R. Pradel, 1993. Estimation of sex- and age-related survival
rates of a microtine population. Journal of Wildlife Management 57:158-163.
Pearson, 0. P. 1985. Predation. Pages 535-566 in R. H. Tamarin, ed. Biology of New
World Microtus. American Society of Mammalogists Special Publication 8.
Pradel, R. J., and J. D. Lebreton. 1991. User's manual for program SURGE, version 4.1.
Mimeographed document, C.E.P.E./C.N.R.S. BP 5051, 34033 Montpellier cedex,
France.
Rexstad, E., and K. P. Burnham. 1992. User's guide for interactive program CAPTURE.
Colorado Cooperative Fish and Wildlife Research Unit, Colorado State
University, Fort Collins.
Reynolds, P., and M. L. Gorman. 1994. Seasonal variation in the activity patterns of the
Orkeny vole (Microtus arvalis orcadensis). Journal of Zoology, London 233:
605-616.
Richter-Dyn, N., and N. S. Goel. 1972. On the extinction of a colonizing species.
Theoretical Population Biology 3:406-433.
Robinson, G. R., R. D. Holt, M. S. Gains, S. P. Hamburg, M. L. Johnson, H. S. Fitch, and
E. A. Martinko. 1992. Diverse and contrasting effects of habitat fragmentation.
Science 257:524-526.
SAS Institute, Inc. 1990. SAS/STAT User's guide version 6, Fourth Edition. SAS
Institute Inc. Cary, North Carolina, 534 pp.
Saunders, D. A., R. Hobbs, and C. Margules. 1991. Biological consequences of
ecosystem fragmentation-a review. Conservation Biology 5:18-32.
Schauber, E. M., W. D. Edge, and J. 0. Wolff. 1997. Insecticide effects on small
mammals: influence of vegetation structure and diet. Ecological Applications
7:136-150.
39
Seber, G. A. F. 1965. A note on the multiple recapture census. Biometrika 52:249-259.
Shaffer, M. L. 1981. Minimum population sizes for species conservation. Bioscience
31:131-134.
Soule, M. E., Editor. 1986. Conservation biology: the science of scarcity and diversity.
Sinauer Press, Sunderland, Massachusetts.
Turner, M. G. 1989. Landscape ecology: the effect of pattern on process. Annual
Review of Ecology and Systematics 20:71-197.
van Apeldoorn, R. C., W. T. Oostenbrink, A. van Winden, and F. F. van der Zee. 1992.
Effects of habitat fragmentation on the bank vole, Clethrionomys glareolus, in an
agricultural landscape. Oikos 65:265-274.
Verboom B., and R. C. van Apeldoorn. 1990. Effects of habitat fragmentation on the red
squirrel, Sciurus vulgaris L. Landscape Ecology 4: 171-176.
Verts, B. J., and L. Carraway. 1987. Microtus canicaudus. Mammalian Species 267:1-4.
White, G. C., K. P. Burnham, D. L. Otis, and D. R. Anderson. 1978. User's manual for
program CAPTURE. Utah State University Press, Logan, Utah.
Wiens, J. A., and B. T. Milne. 1989. Scaling of 'landscapes' in landscape ecology, or,
landscape ecology from a beetle's perspective. Landscape Ecology 3:87-96.
Wilcove, D. S., C. H. McLellan, and A. P. Dobson. 1986. Habitat fragmentation in the
temperate zone. Pages 237-256 in M. E. Soule, ed. Conservation biology.
Sinauer Associates, Inc. Sunderland, Massachusetts.
Wilcox, B. A., and D. D. Murphy. 1985. Conservation strategy: the effects of
fragmentation on extinction. American Naturalist 125:879-887.
40
Wilson, K. R., and D. R. Anderson. 1985. Evaluation of two density estimators of small
mammal population size. Journal of Mamma logy 66:13-21.
Wolff, J. 0.1985. Behavior. Pages 340-372 in R. H. Tamarin, ed. Biology of New
World Microtus. American Society of Mammalogists Special Publication 8.
Wolff, J. 0., W. D. Edge, and R. Bentley. 1994. Reproductive and behavioral biology of
the gray-tailed vole. Journal of Mamma logy 75:873-879.
Wolff, J. 0., T. Manning, S. M. Meyers, and R. Bentley. 1996. Population ecology of the
gray-tailed vole, Microtus canicaudus. Northwest Science 70:334-340.
Wolff, J. 0., E. M. Schauber, and W. D. Edge. 1997. Effects of habitat fragmentation on
the social dynamics of gray-tailed voles. Conservation Biology. In press.
Yahner, R. H. 1988. Changes in wildlife communities near edges. Conservation Biology
2:333-339.