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Microhabitat as a Template
for the Organization of a
Desert Rodent Community1
Michael A. Bowers2and Christine A.
Flanagan3
It is generally believed that species
have different fitnesses in different
habitats, that most communities are
comprised of sufficient habitat variation over which fitness differentials
can be expressed, and that species
select habitats that maximize their
fitness (e.g., Levins 1962, Schoener
1971).The manner and degree to
which species respond to the habitat
template involves elements of selection in its purest form (i.e., choice),
relegation, and correlation.
At the community level rarely do
species occupy habitats in an ideal or
cost-free fashion. By occupying space
or using resources in a habitat specific manner organisms alter habitat
suitability and thereby change the
basis over which habitats are selected
(Fretwell and Lucas 1970).Species
that use limited resources in an efficient manner or are behaviorally
dominant can monopolize the choicest habitats and relegate, directly or
indirectly, subordinate or competitively inferior species to secondary
'Paper presented at symposium, Management of Amphibians, Reptiles, and
Small Mammals in North America. (Flagstaff,AZ,July 19-21, 1988.)
2MichaelA. Bowers is Assistant Professor
in the Department of Environmental Sciences and Research Coordinator at the
Blandy Experimental Farm, University of Virginia, Clark Hall, Charloffesville, VA 22903.
3ChristineA. Hanagan is Assistant Curator of the Orland E. WhiteArboretum, University of Virginia, P.0.Box 1 75, Boyce, VA
22620.
Abstract.-We used 20 0.25-hafenced plots to
experimentally study microhabitat use by 1 1 desert
rodent species in southeastern Arizona. Removal of
the largest granivore , Dipodomys spectabifis,
produced the most pervasive shifts in the use of
microhabitats while adding food or removing ants
produced few responses. These results support the
idea that this community is organized around
competitive interactions involving aggression,
preemption, and relegation.
habitats (Colwell and Fuentes 1973,
Bowers et al. 1987). If the capture
success rates of predatory species
varies among habitats this can also
affect the absolute and relative fitness of prey species and their distribu tion among habitats (Kotler 1984,
Bowers 1988).
Marked patterns of habitat occupancy and segregation are often cited
as evidence that ecological communities are structured. The general pattern is that some (if not most) species
in a community utilize habitats differently from random and differently
than if each species occurred by itself. Observational and manipulative
experiments have shown that dynamical proper ties of populations
(including patterns of growth, demographics, and interaction) often become expressed as spatial phenomena, thereby establishing a connection between habitat occupancy and
population dynamics (see Connor
and Bowers 1987).
Many communities are comprised
of an array of microhabitats which
represent discrete, exploitable resources which occur with sufficient
variability so as to be partitionable
among species. The availability and
distribution of microhabitats have
been shown to limit the growth and
density of many populations and,
thereby provide an ecologically relevant and readily identifiable context
over which species interactions and
population growth can be studied
(Price 1978, Rosenzweig 19811.
Desert rodents have long provided ecologists with a model system
for examining the role of microhabitat in structuring communities. The
basic pattern throughout the major
North American deserts is that locally co-occurring species characteristically forage in microhabitats that
are structurally distinctive with respect to perennial vegetation and soil
type (Rosenzweig and Winakur 1969,
Price 1978; for reviews see Brown et
al. 1979, Munger et al. 1983, Price
and Brown 1983).
Three mechanisms, alone or in
combination, apparently account for
the general pattern. First, because of
differences in body size, mode of 1ocomotion and behavior, rodents differ in their abilities to exploit particular distributions of food (i.e., seed)
resources that are created by structural features of the microhabitat
(Bowers 1982, Harris 1984, Price
1983, Reichman 1981).Second, rodents may differ in their ability to
escape visually oriented predators so
that the most susceptible rodents are
limited to the safest microhabitats
(i.e., under vegetative cover) while
more vagile rodents show more unrestricted use of alternate microsites
(Kotler 1984). Third, the ability of
some species to aggressively defend
areas from other rodents may be
high in some habitats and low in others resulting in habitat dependent
segregation involving domination/
relegation (Hutto '1978, Frye 1983,
Bowers et al. 1987).
Desert rodent populations are remarkable in their ability to respond
to short-term changes in the abundance and distribution of food resources; primarily seeds. Some of the
more marked responses involve
changes in use of microhabitats. For
example, enriching microhabitats
with supplemental seeds increases
the use of these by desert rodents
(Harris 1984, Kotler 1984, Price and
Waser 1985).Such shifts are particularly noteworthy for microhabitats
where the risk of being preyed upon
is high, and suggests that both energetic profits and predatory risk play
a role in determining which microsites are used (Hay and Fuller
1981, Price and Waser 1985, Bowers
1988). Food availability also can
change the manner in which some
rodent species interact: from competitive exploitative interactions under low levels of food to aggressive
interference interactions under high
levels of food (e.g., Congdon 1974).
In complex communities microhabitat use originates with preferences of individual species for certain
microhabitats, but these basic responses may become altered, directly
or indirectly, by interactions with
other species. Moreover, at the community level it is not clear how
changes in the resource base are
manifest in patterns of spatial usage.
Some important questions are: Does
interspecific competition become
more or less important with increasing food availability? Does the mode
of competition change? How does
food availability change the relative
roles of preference and relegation in
determining habitat occupancy?
Thus, detailing the interplay between
population and community-level responses to changes in resource
availability should reveal much
about the processes influencing microhabita t use and, thereby, the factors responsible for the organization
of these communities.
In this paper we describe patterns
of microhabitat use of 11Chihuahuan Desert rodents over a span of
more than eight years. We experimentally manipulated both species
composition and food supply and
measured resulting shifts in microhabitat use. By detailing shifts in
microhabitat use in response to our
manipulations we were able to identify the most important interactions
among species, estimate their relative
strengths, and say something about
the mode of interaction promoting
the shifts.
Our results suggest that the organization of this community revolves more around differences in
the ability of species to occupy and
defend certain key microhabi ta ts
than changes in food availability.
Study Site and Methods
The present paper details changes in
microhabitat use in response to longterm experimental manipulation of
rodent composition and food supply.
Our study site was located at an elevation of 1330 m in a relatively
homogeneous desert shrub habitat
on the Cave Creek Bajada 6.5 km east
and 2 km north of Portal, in Arizona,
USA. Manipulations were performed
in twenty 0.25-ha plots. Each plot
was fenced with 0.64-cm mesh hardware cloth, extending 0.7-m above
and buried 0.2-m below ground. In
addition to an unmanipulated fenced
control (see below), the remaining
treatments consisted of two general
classes: treatments where one or
more rodent species were removed,
potentially changing both food
availability and the potential for direct behavioral interactions; and food
alteration treatments where supplemental millet seeds were added at a
rate of 96 kg per year or seed-eating
ants were removed. Experimental
treatments were assigned to plots at
random.
Fourteen rodent species of which
11 were commonly captured, inhabited the study site, all except those
mentioned above had equal access to
all plots (fig. 1). Because of problems
in consistently identifymg the two
Onychomys species (as either 0,torridus or 0. leucogaster) we group
these together under the designation,
Onychomys spp.
Sixteen equally-spaced gates in
each plot allowed the selective exclusion of rodent species above a threshold body size while allowing all
other species access. Access gates
varied in size among the treatments.
Large gates (3.7 x 5.7-cm) allowed all
rodent species free access to control
(2 plots), ant removal (4 plots), and
the seed addition plots (8plots; see
below); medium-sized gates (2.6 x
3.0-cm) were used to exclude only
the largest granivore, Dipsdornys
spectabilis (2 plots); and small gates
(1.9 x 1.9-cm) were used to exclude
all Dipodomys species (4 plots). The
seed addition treatments included
six plots where supplemental seeds
were applied in 12 monthly applications (hereafter referred to as "constant seed additions"); two plots received the total allotment of seeds in
three applications during the fall
(September-November; referred to as
"pulsed seed additions"). Seeds were
uniformly scattered by hand over
each plot.
It was estimated from productivity measurements at the site that the
addition of 96 kg of seeds per year
should have approximately doubled
the total biomass of seeds produced
annually (our estimate of seed production was ca. 400 kg/ha/yr). The
constant seed additions included two
plots where whole millet (Panicurn
rniliaceam) was added (mean seed
mass = 6 mg); two plots where
cracked millet was added (mean
mass = 1 mg); and two plots where
an equal mixture of whole and
cracked millet was added. The
pulsed seed treatment was designed
to represent a doubling of the seed
production of summer annual plants,
a particularly important food source
for the rodents in this community
(Davidson et al. 1985). Brown and
Munger (1985) found no differences
in responses of rodents to addition of
seeds of different size, so the four
constant seed addition treatments
will be lumped together here (6
plots).
Rodents were censused monthly
during the week of the new moon
(moonlight has been shown to effect
the microhabitats used by desert rodents; Bowers 1988) using live traps
placed in each plot in 7 x 7 grids with
6.5-rn between trap stations. Traps
were baited with millet and opened
for one night per month with plot
gates closed so that only plot residents would be captured. For more
details concerning the experimental
design, see Bowers et al. 1987, Brown
and Munger (19851, and Brown et al.
(1986).
Following the lead of many previous studies on desert rodent communities we used the percent cover of
perennial plants to characterize the
microhabitat at each of the 980 trap
stations. Percent cover within a 2-m
radius of each trap station was measured by ocular estimation using reference disks of known percent coverage. Cover was measured in 1978,
1981, and 1983. There was no significant changes in perennial cover over
this five year period (Mann-Whitney
U-test; P > 0.051, so we used data
from 1983 to characterize microhabitats. Table 1 summarizes vegetation
cover data over the entire study site.
Fence installation was completed
in June, 1977; premanipulative trapping was conducted from July-Seg
tember, 1977; and the manipulations
were initiated in October, 1977. We
restrict our analyses to include postmanipulation data compiled from
October 1977 to December 1984 and
to only those 20 plots to which rodents had access.
Analyses were designed to answer
two questions: first, what are the patterns of species associations occurring at the community level; and sec-
Bioodamys
spaclrbIIIs
Dlpodomys
m8rrhnl
Ant r e m o v a l
( 4 plots)
539
787
Seed-pulse
( 2 plots)
278
390
Seed-constant
(6 plots)
821
1005
Dipodomysremoval
( 4 plots)
0
0
8 . spectabilk-
0
465
Dipodomys
ordil
Porognathus Perognrthus
Prnlcillatus fhvuS
Peramyscus
m#nlculatus
Control
( 2 plots)
removal
( 2 plots)
Figure 1 .-Rodent species on study site (including their body sizes) along with their capture
frequencies in each of the experimental treatments. Included are the number of plots in
each treatment.
ond, what role does microhabitat
play in the distribution of individual
species. In this study patterns of association (including the association
of rodent species with each other and
with structural microhabitats) are
analyzed at the level of individual
trap stations (980 total). Hence, we
Poromyscus dontomys
magslotis
oremlcus
Weetama
elbi~ulo
Onychomyr
SPP.
were interested in measuring responses of rodents to microhabitat
variation occurring at a scale of a meter or two. However, we acknowledge that habitats may also be selected at larger spatial scales (Morris
1987). For example, rodents may also
select areas on the basis of rnicrohabitat composites (e.g., at the
level of the home range) which might
be best examined by considering
structural microhabitats over trap
station aggregates. However, there is
reason to believe that even if selection does occur at these larger scales
it is still oriented towards excluding
or including certain key microhabitats. Hence, we were confident our
analyses would detect patterns at
both scales.
Indices of species association were
calculated by using the frequency
that species were captured at the
same trap station using trap data for
the eight year period. This involved
several steps: (i) tabulating the proportion of trap stations where each
species was captured over the eight
year study; (ii) tallying the number of
trap stations where each pair of species co-occurred; and (iii) comparing
the observed frequency of co-cap
tures to that expected if species captures were distributed independently
and randomly among trap stations.
The expected frequency of species
co-capture was calculated by multiplying together the proportion of stations capturing species individually
to generate a probability of joint occurrence. A modified chi-square statistic, including the sign of association, was then used as an index of
association: i.e., a measure of the difference between the observed and
expected values. The null hypothesis
was that there would be an equal
number of positive and negative associations with less than 5% of the
association values being statistically
significant at a P = 0.05.
The analysis described above can
also be used to examine the association of all species in the community
at individual trap stations. Specifi-
cally, instead of asking how frequently species pairs associate we
can use the maximum likelihood estimation technique to estimate how
many trap stations should have captured O,1,2, . . n species (where n is
the number of species in the community) over the eight year period. As
in the above analysis, this uses the
proportion of stations capturing each
species, multiplies these together in
all possible combinations that might
produce co-captures of from 0 to n
species, and sums these probabilities
for each number of possible co-cap
tures to give an expected distribution
over the population of trap stations.
The null expectation here is that species captures are independently and
randomly distributed among trap
stations.
Analyses were also performed to
examine the individualistic responses
of species to variation in microhabitat and, particularly, how these
change when manipulations are applied at the level of the entire community. We used percent cover by
perennial plants at trap stations as a
general descriptor of microhabitat
type. Our goal was not to use a series
of variables to explain the largest
amount of variation in microhabitats
where species were captured but
rather we were interested in identifying a major resource axis over which
both species distributions and community-level responses could be analyzed. Past work justified using cover
as such a variable (Brown et al. 1979,
Munger et al. 1983, Price and Brown
1983). Our scheme of categorizing
microhabitats was simple: trap stations were grouped into those with
greater-than-median and those with
less-than-median cover. This was
performed separately for stations in
each of the six treatments. Hence,
each microhabitat category was represented by an equal number of trap
stations in each treatment type. The
null hypothesis for analyzing the trap
data was if rodents use microhabitats
randomly, and without regard to
vegetative cover, they should be
trapped in equal frequencies at stations in the two microhabitat categories. Avoidance or preference for microhabitats would be indicated by a
disproportionate number of captures
in one or the other category.
We were also interested in examining (1) the microhabitat affinities of
species in the different treatments,
and (2) shifts in types of microhabitats used by the same species over
the different seasons of the year and
over the six experimental treatments.
In the first case we used the Fisher
Exact Probability procedure in a twotailed test of the null hypothesis that
captures in the two microhabitats did
not differ from a 1:l ratio (Siege1
1956); in the second we subjected the
proportion of species' captures in the
two microhabitats to a 2-way
ANBVA where season and treatment
represented treatment factors.
Results
Results are based on 8,019 captures
of the 11 most common rodent species. Figure 1 lists the frequency of
capture for each species in the six
treatments summed over the eight
year study period.
Community-Wide Patterns of
Microhabitat Use
What are the patterns of species association at the level of the entire community? In answering this we considered the frequency that species were
captured at the same trap station. We
performed two tests. We first calculated species associations for all possible pairings of the 11species occurring in plots with intact rodent assemblages (i.e., those 14 plots with
large gates) resulting in a total of 45
values of species association. Plotting
all association values show that most
species in this community are captured at the same station much less
frequently than predicted by chance
(fig. 2; the null hypothesis is that
there would be an equal number of
positive and negative associations
and that only 5% of these would be
statistically significant at P < 0.05).
The deviation from what is expected
is particularly striking considering
that 27 of the association values exceeded the cutoff value for significance (3.84 for p ~ 0 . 0 5and d.f.=l)
and all of these were in the direction
of negative species associations; there
was not a single significant positive
association. This suggests a high
level of organization revolves around
the spatial segregation of species.
Among those factors that could be
responsible for this marked segregation are unique habitat preferences of
species. These could work alone or in
conjunction with habitat segregation
that is mediated through interactions
with other rodent species. The design
of our experiment allows a further
examination of the role of species interactions in producing the pattern.
Specifically,our experiment includes
treatments with an intact rodent assemblage (14 plots; 686 stations) as
well as treatments where either D.
spectabilis (2 plots; 98 stations) or all
Dipodomys (4 plots; 196 stations)
were selectively removed and excluded. Because previous studies
have shown Dipodomys (and
especially D. spectabilis) to be behaviorally dominant over many of the
species they co-occur with (Blaustein
and Riser 1974, Frye 1983, Bowers et
al. 1987) there is reason to think that
by their removal the patterns of association of the remaining species may
change. To evaluate this possibility
we restricted the analyses to include
just those eight non-Dipodomys species that occurred in all three treatments (number of painvise association values for this group = 21). The
degree to which these species were
associated with each other at trap
stations in each of the three treatments was calculated as before, and
then compared across the three treatments (fig. 3). The results show that
removing either all Dipodomys or just
D. spectabilis significantly a1ters the
degree to which the remaining species are spatially segregated (X2 =
17.33, df = 2; P < 0.000). While the
trend is clearly towards more positive and fewer negative associations
when competitors are removed, most
of the species are still negatively associated with each other.
The previous analysis can be extended from the two-species case to
one considering the association of all
11 species. Specifically, instead of
asking how frequently species pairs
associate we can use the maximum
likelihood estimation technique to
estimate how many trap stations
should have captured O,1,2 . . . 11
species over the eight year period.
Comparing the actual number of species captured per station with that
expected (fig. 4) shows that the observed distribution is shifted to the
left of that expected (significantly different at P < 0.05 using KolmogorovSmirnov one sample test), that there
are significant differences in the
mode of species co-captured per station (expected=4;observed=3), and
16
14
12
Species Associations
10
8
6
4
2
n1
-40
-30
-20
-10
0
10
Chi Square
20
30
40
Figure 2.-Estimates of species associationsfor plots with intact rodent assemblages (i.e.,
those with large gates). Association values represent modified chi-squares (with the sign of
association) and where calculated according to whether species were captured at the
same trap station more or less frequently than expected by chance. See text for more detail.
Intact
Dipodomys
Removal
0 0. s.
Removal
-
I
positive
negative
Associations
Figure 3.-Histogram of the number of positive and negative species associations for nonDipodomys species broken into three treatment categories: (i) treatments with intact rodent
assemblages; (ii) D. specfabilis removal plots; and (iii) Dijwdomys removal plots.
that there are large differences in the
proportion of stations capturing two
species (ca. 5% for the expected compared to 23% for the observed). The
main result is that trap stations captured fewer species than expected if
species captures were random, which
further evidence that species in this
community are spatially segregated.
Use of Space by Individual
Species: The Role of Cover
In this section we are interested in
the individualistic responses of species to microhabitat variation and,
particularly, how these change when
manipulations are applied at the
level of the entire community.
There was marked variability both
within and between species in the
usage of microhabitats (table 2 and
figs. 5 and 6). On control plots Pero-
myscus eremicus, Neo toma albigula,
Reithrodontomys megalotis, and Dipodomys merriami (in all treatments but
the D. spectabilis removals) all
showed positive associations for trap
stations with greater-than-median
cover.
Treatment
Expected
# species per S t a t i o n
Figure 4.-Histogram of expected and observed number of species captured at individual
trap stations.
Figure 5.-Distribution of captures in
greater-than and less-than median cover
for the five hetsromyidspecies listed according to treatment and seuson. Capture
data is graphed relative to what the null
hypothesis predicts (i.e., an equal number
of captures in both microhabitat types; the
zero line). Preference for higher-than-median sites is represented by positive values;
less-than-mediancover by negafive values. Bars within treatment categories indicate season: from left to right Spring
(March-May), Summer (June-August), Fall
(September-November),Winter (December-February). Treatment designation is as
follows: "-DS", Dipodomysspectabilk removal; "C",control; "SC",constant seed
addition; '-Aw, ant removal; "-Dm,D i m omys removal; "SP", pulsed seed additions.
Those species associated with
more open microhabi tats included
the large kangaroo rat, Dipodomys
spectabilis, and the smallest species,
Perognathus ffavus.The remaining
species used the two microhabitats
more indiscriminantly with the exception that Peromyscus maniculatus
was captured more frequently in
high-cover microsites in the D. spectabilis removal treatment.
Figures 5 and 6 and table 2 show
our experiments were of the kind
and were of sufficient intensity to
promote community-wide changes in
the use of microhabitats by all species; only the Onychomys showed significant seasonal shifts in microhabitat use (captured more frequently in
higher-cover areas during the fall
than in the other seasons). Using the
control treatment as a reference point
showed that the majority of species
shifted their use of microhabitats on
plots where D. spectabilis was experimentally removed. These shifts, involving eight of the nine species
present, included an increase in the
use of microsites with less-than-median cover by D. merriami, P. pencillatus, P. ffavus,and N. albigula, and an
increase in the use of high-cover sites
by P. maniculatus, P.eremicus, R.
megalotis, and D. ordii.
The remaining manipulations registered fewer and less dramatic
shifts: i.e., increased use of open microhabitats by P. pencillatus and P.
maniculatus on constant seed addition plots; and shifts towards highercover microsites by R. megalotis and
P. pencillatus in ant removal and Dipodomys removal treatments, respectively.
The role of microhabitat in the organization of this community can be
further evaluated by comparing the
distribution of trap captures for all
species with what is available at trap
stations (fig. 7). The objective was to
determine whether certain types of
microhabitats are used by the rodent
community more frequently than
others. This analysis shows that the
distribution of captures in control, D.
spectabilis removal, and Dipodomys
removal plots all differ significantly
from that expected if the use of microhabitats was random with respect
to vegetative cover (KolmogorovSrnirnov two sample test; P < 0.05).
However, there are characteristic
ways these differ from expected. On
control plots there were fewer than
expected rodent captures in traps
having < 5% cover; on D. spectabilis
removal plots there were a greaterthan-expected number of captures
for this same cover category; and on
Dipodomys removal plots most rodents were captured at trap stations
with > 10 % cover.
Discussion
Our results identify species interactions as the principal factor producing structure in this community. It is
significant that, by adding supplemental seeds or removing ants, we
were able to change microhabitats
used by only a few of the species but
removing a large, potentially dominant competitor produced many
shifts. This suggests that the primary
mode of interaction, as it effects the
patterns of microhabitat use in this
community, involves the direct responses of rodent species to each
other rather than interactions mediated through the exploitation of food
resources, or the individualistic responses of rodents to particular microhabita t types.
The results point to the importance of one dominant species, D.
spectabilis, whose presence in the
community plays a disproportionate
role in determining which microhabitats are utilized by the other species,
and thus the organization of the community as a whole. Whenever it is
present, regardless of how much
food is available, it appears to relegate the majority of other rodent species to higher-than-median cover
habitats, thereby reducing the density of potential competitors in the
open habitats it prefers. A notable
exception is Perognathus flavus which
was captured in open sites along
with D. spectabilis. Because of its
small size (ca. 7 g) and low population density, P. flavus may have only
a negligible impact on the food resources that can be harvested by D.
spectablilis and, therefore, may not
compete directly with or be subjected
to its aggressive behavior. The importance of such size-ratio thresholds
in allowing species to coexist has
been discussed (Ebwers and Brown
1982). Defending open areas from
other rodents may be a mechanism
by which D. spectabilis is able to
preempt food resources for its exclusive use. Supporting evidence for this
comes from other research at our
study site where it was found that
Treatment
Figure 6.-Distribution of captures in the two
microhabitat categories for the six Cricetid
rodents listed by treatment and season.
See legend to figure 5 for more details.
experimental seeds placed in open
microhabitats remained largely unharvested when D. spectabilis was
present but quickly disappeared in
plots where it was removed (see
Bowers et al. 1987).
Our results also infer something
about the mechanism by which D.
1
spectabilis affects the use of space by
other rodent species in the community. Competition can be mediated
through two processes: (i) exploitative interactions where species interact through a shared resource base;
or (ii) contest interactions involving
aggressive dominance and relegation
CONTROL
rc-----i
----,
Lo,,,
REMOVAL
PERCENT COVER
Figure 7.-Distribution of trap captures (broken line; all species combined) and available
trap sites (sold line) relative to vegetative cover on (i) control; (it) 0. spectaMlis removal;
and (iii) Dipodomys removal plots.
to suboptimal areas and resources.
For exploitation alone to account for
the patterns of microhabitat use, D.
spectabilis, through its foraging,
would have to significantly alter the
distribution of food (seed) resources
among the microhabitats in ways
that are ecologically significant for
the other species. This is unlikely for
several reasons. First, many of the
seeds utilized by the smaller species
appear to be too small to be econornically harvestable by D. spectatnlis (see
Bowers et al. 1987).Second, many of
the species showing significant microhabitat shifts were non-granivores
(i.e., Neotoma), and hence, should be
relatively insensitive to changes in
the resource base attributable to the
foraging of D. spectabilis. Third, adding seeds should have made food
more available to all species and reduced the degree to which D. spectabilis was able to alter the distribution
of food resources, so that shifts by
the other species would have been
expected in response to this treatment. Moreover, significant changes
in the distribution of food resources
were more likely to have been caused
by D. merriami that occurs at higher
densities than D. spectabilis. Our results show that adding supplemental
seeds or removing D.merriami produced fewer shifts than removing
just D. spectabilis.
As an alternative to exploitation,
competitors of large body size may
directly restrict the foraging activities
of smaller species through interference. Under an interference mode of
competition adding seeds may not
alter the intensity or outcome of the
interaction. Because most significant
shifts in microhabitat use occurred in
the D. spectabilis removal treatmentcoupled with the fact that adding
seeds had little effect on the patterns
of microhabitat-leads us to the conclusion that aggressive interference
by D. spectabilis is the mechanism
most consistent with our results.
Our study also indicates that the
majority of shifts in microhabitat use
originate with the D. spectabilis-D.
merriami interaction and, at the community level, this one interaction affects the microhabitat utilization of
the majority of rodent species
through a complex network of direct
and indirect interactions. Perhaps the
most striking shift (not in the magnitude of response but in the number
of individuals involved) was the increased use of open areas by the numerically dominant D. merriami
when D. spectabilis, which had formally used these sites was removed.
Mast other shifts by the smaller r e
dents, including the increased use of
open microhabi tats by Perognathus
flavus, Peromyscus maniculatus and
Reithrodontomys megalotis when all
Dipodomys were removed, suggest
that these species responded directly
to D. merriami and only indirectly to
D.spectabilis. Hence, there appears to
be a hierarchy of interactions. The
primary one is between the
behavioral ID. spectabilis) and
numerical ID. merriami) dominants
and it is this interaction around
which the community is organized.
Other studies have noted the potential for interference between desert
rodents (Blaustein and Riser 1974,
Hutto 1978, Rebar and Conley 19831,
especially between D. spectabilis and
D. merriami (Frye 19831, and our
study shows how this one interaction
can resound throughout the community to affect many other species.
A primary motivation for our
study-and most studies focusing on
the role of habitat-is that microhabitats represent a limited and exploitable resource and the manner in
which they are used directly impinges on population growth and
density. Many of the experimentally
induced microhabitat shifts we have
reported were accompanied by
changes in local species density
(Brown and Munger 1985, Brown et
al. 1986) that support the contention
that D.spectabilis controls the dynamics of this community through a combination of direct and indirect effects.
For example, increasing food levels
by adding seeds resulted in an in-
crease of D ,spectabilis and a decrease
in D. merriami densities. Removal of
D. spectabilis resulted in positive density compensation of D. merriami but
no changes in densities of the smaller
seed-eaters; removal of all Dipodomys, however, resulted in large density increases in several of the
smaller rodents. Taken together, the
microhabitat and density responses
to our manipulations indicate that
interference competition for certain
foraging sites not only determines
the spatial organization of this community but that it is directly involved
in the regulation of rodent densities.
There are several aspects that warrant further comment. First, our results show that when D. spectabilis is
present open sites are underutilized
by the community as a whole; when
D. spectabilis is removed the
remaining Dipodomys shift to use
these open sites; but when all Dipodomys are removed the remaining species are unable to fully utilize the vacated microhabitats (fig. 7). Hence,
there appears to be a limit to how far
the community can compensate for
the absence of certain species.
Among the possible explanations for
this might be that assemblages of
desert rodents have been associating
together for a sufficient time to have
lost the flexibility to respond to situations where one or more of the species are absent (Schroder and
Rosenzweig 1975).Another is that
quadrupedal species may have a limited ability to avoid predators in
open microhabitats and this limits
the degree to which they can compensate when the bipeds are removed. In either case the relaxation
of one factor (in this case the removal
of dominant competitors) appears to
be accompanied by the increased importance of others.
Second, the effects of interference
competition by D. spectabilis appear
to be effective in excluding interspecifics primarily in open areas although this dominant does occur in
greater-than-median cover habitats.
It may be that aggression is of lim-
ited value in bushy microsites where
subdominant species may readily
find refugia. As a result, I>. spectabilis
may be involved in two kinds of
interactions with each of its competitors; exploitatively for seeds in bushy
sites and through interference in
open microhabitats. As a result, the
highly asymmetrical interactions between the dominant/subordinates in
open sites may become more nearly
symmetrical in bushy sites where
premiums are on foraging efficiency.
Third, the existence of strong, aggressive interactions among species
increases the potential for indirect
and high-order interactions that involve species that overlap very little
in resource utilization. For example,
the large herbivore, Neotoma albigula
was as likely to shift its microhabitat
use as the granivorous species. However, it is interesting to note that although the non-granivores shifted
microhabitat use when granivorous
species were removed, significant
density changes were limited to just
other granivores (Brown and Munger
1985). Hence, while interference may
play a role in determining use of microhabitats by rodents in several foraging guilds, its effects appear to be
most significant for ecologically similar species.
The goal of experimental programs is to hold most variables constant while manipulating others, and
then to measure for shifts in response
variables. In this paper we have used
patterns of microhabitat use in control plots as a reference point for
interpreting our experimental results.
The assumption in doing this is that
the degree to which the community
responds to a particular manipulation provides an estimate of its importance in producing the basic pattern. In our particular case we
wanted to know how the baseline
patterns of microhabitat use (i.e.,
those in control plots) change when
supplemental food is added or species are removed. While some of our
patterns are easy to interpret, others
are very complex and appear to in-
volve a hierarchy of responses that
operate over different scales in time
and space. The existence of such a
dynamic and diverse set of responses
shows the limitations of most twospecies models of interspecific interactions upon which past theories of
community organization have largely
been based; they also call into question the value of studies seeking to
understand the mechanistic processes that determine community
composition through comparative,
nonexperimental methods.
Implications for Management
While the spatial association of small
mammals with particular microhabitats has been rigorously and repeatedly documented, and the patterns
suggest almost a universal role of
microhabi ta t in "structuring" small
mammal communities, the processes
responsible for producing these associations are poorly understood (Price
and Brown 1983, Bowers 1986).To
successfully manage/manipulate
such communities there is a clear
need to better understand the processes that determine which microhabitats are used and which are
not. Towards this end we identify
two particularly relevant areas for
our discussion: (1)the scales in time
and space over which microhabitat
use occurs; and (2) the roles of correla tion, and selection/relegation in the
occupancy of microhabitats.
Vagile organisms, e.g. small mammals, can potentially respond to features of the habitat at several different scales. At the macro-end of the
habitat spectrum animals choose areas in which to establish home
ranges. Microhabitat selection, in
contrast, usually involves the use/
disuse of small areas within the
home range. There are also temporal
differences in schedules of usage:
macrohabitat selection occurs over a
much longer timescale (weeksmonths) while microhabitat use occurs more immediately (seconds-
minutes). While it was assumed for
years that macrohabitat selection occurred through the selection of composite microhabitats, recent work on
small mammals suggests that the two
may be largely separate (Morris
1987).
Most factors that are demonstrably important to the structure of
small mammal communities, i.e., primary productivity, plant species and
foliage height diversity, vegetation
cover, substrate type, competitor diversity and abundance, and predatory pressure, vary more between
macrohabitats than among microhabitats within particular locales.
For example, primary productivity
and plant cover are determined by
plant species composition and general conditions for growth that vary
over large environmental gradients
at the macrohabitat scale. These large
scale gradients influence patterns of
microhabitat use by determining
which rodent species are present,
their densities, the distribution and
abundance of food resources, and the
types of microhabitats that are available for selection. As a consequence,
the composition, densities and demographical behavior of small mammal
populations and communities may
more closely reflect habitat variability at the macro-rather than the micro-scale. On the other hand, microhabitat usage is a phenomena involving choices of individuals. Microhabitats that, by definition, vary
over scales smaller than individual
home ranges, have significance for
the survivorship or reproduction of
foraging individuals, but may have
little relevance when integrated over
the population as a whole.
Most experimental studies examining the role of microhabitat in
structuring small mammal communities tend to confound micro- and
macrohabitat effects. Typically, manipulations (e.g., food addition, species removal, tailoring of vegetation)
are applied at the level of the rnacrohabitat with microhabitat usage by
individuals measured as a response
variable. The research reported here
suffers from such a confounding.
Other field experiments that examine
the allocation of foraging time among
patches restrict manipulations to the
level of microhabitats (Kotler 1984,
Price and Waser 19851, and are not
confused by responses of entire
populations. Clearly, the time has
come to utilize the information we
now have to design comprehensive
studies that distinguish between micro- and macrohabitat selection: i.e,
studies that manipulate certain microhabitats on a scale over which
populations might respond.
Correctly gauging the scale over
which species respond to the environmental mosaic is critical to the
successful management of that species. Programs aimed at managing
species by manipulating microhabitats may or may not be successful
depending on the scale at which the
manipulation is applied. If the goal is
to manage populations then rnacrohabitat may be the correct context
for the program. This is not to suggest that microhabitat is an inappropria te context for management programs. What it does suggest is that
management oriented programs
should be directed towards populations rather than the behavior of individuals. In many cases this may involve changing the focus from the
micro to macro level.
Our second point for discussion
involves habitat correlation versus
selection/relegation. Habitat usage is
determined by the habitats available,
the tolerances/preferences of organisms for these habitats, and the
among-habitat variability in fitness.
Clearly, there must be some variability in the structure of the habitat in
order for selection to occur. Habitats
that are relatively homogeneous at
the smaller scales may not exhibit
habitat associations even by highly
selective species. Conversely, showing that a habitat has a significant
degree of microhabitat variability
does not imply that organisms have
the ability or inclination to respond
to that variability. In order to apply
the patterns of microhabitat use from
one site to predict what is occurring
at another requires an understanding
of the biological factors underlying
microhabitat use. Achieving this has
proved difficult because of several
problems. First, it is clear from a
growing body of experimental work
(including the present study) that
habitat association does not necessarily imply habitat selection. Because
microhabitats are rarely discrete,
usually grade from one type to another, and involve a suite of factors
that either characterize or are correlated with specific microhabitats, it is
rare that habitat occupancy can be
tied to a single factor. As a result it is
difficult to conclude that an animal is
selecting a habitat per se, some feature of that habitat, or some factor
that is only correlated with that microhabitat. As a complicating factor
habitat selection probably reflects
integrated responses of organisms to
maximize fitness relative to several
largely independent processes. For
example, animals might select microhabitats so as to minimize predatory risk, or food encounter rates, or
to jointly maximize food intake while
minimizing predatory risk (Bowers
1987).
Second, the present results and
those of others (Price 1978,
MfCloskey 1978, Wondolleck 1978,
Bowers et al. 1987) show that microhabitat provides a template over
which species interactions and competitive hierarchies become expressed. The pattern is one of selection/ relegation-the competitive
dominant selecting its preferred microhabitat and through exploitative
or interference competition relegating other species to less preferred
sites. The more ecologically similar
two species-and hence, the greater
the intensity of competition between
them-the greater the potential role
of interspecific competition in determining microhabitat usage.
Competitive interactions represent
dynamical processes impinging on
microhabitat association and usage.
Seasonal or year-to-year fluxes in resource availability or changes in the
distribution of resources among microhabitats can a1ter the economical
basis underlying competitive interactions, and thereby promote shifts in
microhabitat usage. For example,
Congdon (1974) found during periods of low resource availability that
the large D.deserti and the smaller,
D. rnerriarni, coexisted in the same
microhabitats but that the former became aggressive and excluded the
latter from these sites when food levels increased. Similarly, Frye (1983)
found that D. spectabilis excluded D.
rnerriarni from areas around its burrows just in the fall when seeds from
summer annuals were abundant.
Competitively based selection/
relegation has the effect of increasing
usage of secondary habitats while
decreasing usage of the most preferred ones. The result is that competition promotes the segregation of
species among microhabitats and the
degree to which the community is
spatially organized. Thus it is no accident that the most striking patterns
of microhabitat use and segregation
are in communities that are highly
competitive (Connor and Bowers
1987). As the present study has demonstrated even one strong interaction
involving just two species (in this
case the behavioral and numerical
dominants) can affect microhabitat
usage by all species in the community through direct and indirect pathways of interaction.
Care must be taken when examining the spatial organization of communities where competition might be
occurring. Efforts to understand microhabitat utilization through reconstitution studies that measure individual species preferences for microhabitats, then combines these in a
general model of microhabitat associa tion, will miss higher-order competitive effects that may be the main
determinants of microhabitat use.
Further, since competition can be indeterminate, work over complex
pathways, and operate over widely
varying scales in time and space it is
doubtful that any one model can be
used to predict microhabitat use over
all communities. As a first step towards using microhabitat utilization
as a tool for management programs
we need to know which communities
are interactive (i.e., structured
around selection/relegation
schemes), which are non-interactive,
and something about ecological attributes of each. It may be that in
some communities microhabitat is
the correct context for management
programs while in other communities the focus should be on species
interactions. Species removal experiments such as the one described here
provide a straightforward test of
these models.
What we are suggesting here is
that microhabitat use be viewed as a
manifestation of process and that
these processes provide the basis for
management. We feel that the most
important question is not which
habitats are being used by a particular species but why it is using that
microhabitat and not others. Recent
work has shown that the pathways
by which species interact at the level
of ecological communities can be
very complex and that similar patterns of microhabitat usage need not
share a common sequence of causation (see papers in Diamond and
Case 1986).
Without knowing something
about which processes are locally important it is risky to extrapolate findings from one site in managing another. For example, Bowers (1986)
found in rarefaction studies of the
same three species rodent community that microhabitat use at one site
was affected by interspecific competition but not at two others. Such results underscore the fact that microhabitat use involves multidimensional responses of organisms to
their environment. Understanding
the basics of such relationships
should be the goal of community
ecologists and managers alike.
Acknowledgments
We thank J.H. Brown and D.B. Thompson for help in the field and for
discussion. J.H. Brown and R.T.
M'Closkey provided critical reviews
of the manuscript.
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