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F.'ci~iojii'.75(2). 1994. pp. 4 3 8 4 4 5
L 1994 by the Ecolog~cdlS o c ~ c t yof Amcnca
LONG-TERM EXPERIMENTAL STUDY OF A CHIHUAHUAN DESERT
RODENT COMMUNITY: 13 YEARS OF COMPETITION'
EDWARD
J HESKE,'JAMESH BROWN,AND SHAHROUKH
MISTRY
De11arrr)letzt o f Blo/ogj I nrrersrri o f \ert Zleuco -Ilbi(querque \el$ Mekrco 57131 C S,4
d4hstract. An experimental study of competition between kangaroo rats (Dipodornys
spp.) and other sympatric desert rodents using exclosures with "semipermeable" fences
has been continuously maintained at a site in the northern Chihuahuan Desert since 1977.
A new set of experimental manipulations begun in 1988 at the same site repeated this
study.
As reported previously for this community, exclusion of three species of Dipodotnys
from both original and new experimental plots resulted in greater abundances of five species
of small granivorous rodents (Chaetodipus penicillatus, Perognath~ts.flavus, Perornyscus
eremicus, P. rnaniculatus, Reithrodorztomys megalotis) on these plots relative to controls.
In contrast, there were no significant treatment effects on the abundances of insectivorous
grasshopper mice ( 0 n ~ ) c h o r n ~spp.).
) s The long time lag before the response by small granivores to Dipodotnys removal observed in the original experiment was not repeated in the
experiment begun in 1988.
Long-term (10 yr) exclusion of kangaroo rats from experimental plots has resulted in
changes in vegetative cover, particularly increased grassiness. on these plots relative to
controls. We used the repetition of the Dipodotnys exclusion experiment in 1988 to evaluate
the importance of this potential indirect effect of kangaroo rats on other rodents in this
community. By examining differences in rodent capture numbers on the original and new
sets of Dipodomys exclusion plots, we could identify four species (C. penicillat~ts,Perognathus jlavl~s, Perornyscus eremicus, P. marzicl~latus)whose responses to kangaroo rat
removal reflected direct competition from kangaroo rats, one species (R. megalotis) whose
response reflected both direct and indirect (via vegetation changes and habitat selection)
effects, and two species (Sigmodon hispidus, S. .fi~lviventer)whose responses reflected only
vegetation-mediated effects.
The continuous presence of competition between small granivores and kangaroo rats
over the 13-yr study despite large. species-specific fluctuations in abundances suggests that
competition is pervasive within this community.
Key words: Chrhuahuan Desert: cornmi(nitj~;competrtion: desert rodents; Dipodomys: experiments: indirect e#ecrs: long-terr)~sti(dj.; re~~lication.
INTRODUCTION
Studies of interspecific competition have played an
important role in the development of theoretical and
empirical community ecology (Salt 1983, Strong et al.
1984, Diamond and Case 1986). Most experimental
studies have concentrated on painvise interactions and
assumed that the mechanism involved was interference
or exploitative competition. In recent years, attention
has been attracted to interactions between species that
are mediated through a third species or trophic group
(Schmitt 1987, Wooton 1992, 1993); these interactions
are generally termed indirect interactions (reviewed in
Strauss 1991). At present, however, few studies have
evaluated the relative importance of direct vs. indirect
effects in structuring communities. This is for good
reason. There are several problems in detecting indirect
' Manuscript received 25 March 1993: revised 29 May 1993:
accepted 5 June 1993.
Present address: Illinois State Natural History Survey. 607
East Peabody Drive. Champaign. Illinois 6 1820 USA.
effects, and in assessing their full magnitude. First. unless all species (or at least all functional groups of organisms) are monitored, it is likely that indirect pathways will be overlooked, and their consequences will
be confused with the results of direct interactions. Second, long-term press experiments (Bender et al. 1984)
may be required for the consequences of perturbations
to play out over indirect pathways with long time lags
.
(Brown et al. 1986, Brown and Heske 1 9 9 0 ~ )Finally,
the magnitude of indirect pathways may fluctuate over
time, because each indirect pathway involves at least
one intervening species that may be influenced by extrinsic environmental variation.
The granivore-dominated desert rodent communities of southwestern North America have served as a
model system for the study of competition and community structure (Brown et al. 1986, Reichman 1990).
Studies of these rodents have not only produced experimental evidence that interspecific competition occurs. but have also provided many insights into the
mechanisms of resource partitioning and competitive
March 1994
C O M P E T I T I O N IN DESERT RODENTS
439
interactions. These mechanisms are reflected in non- per mice are also similar in size to many of the small
random spacing of morphological traits that affect re- granivores, and we assume that they are similarly sussource use. such as body size and incisor width (Brown ceptible to predation by large snakes that might be
1973, Simberloff and Boecklin 198 1, Bowers and Brown present on control plots but differentially excluded from
1982, Dayan and Simberloff, in press): direct aggressive plots with small gates. Finally, grasshopper mice are
interference (Frye 1983, Bowers et al. 1987); differ- aggressive and readily attack kangaroo rats when placed
ential use of microhabitats (Brown and Lieberman 1973, together with them in small arenas (J. H. Brown, perRosenzweig 1973. Price 1978. Wondolleck 1978, sonal observation); they are therefore not likely to be
Thompson 1982a, Bowers et al. 1987): differential re- aggressively excluded from study plots by kangaroo
sponses to correlates of predation risk (Thompson rats (see also Rebar and Conley 1983). Thus, a lack of
1982b, Kotler 1984, Brown 1989): and differential re- response by the two species of grasshopper mice to the
sponses to temporal environmental variation (Kotler kangaroo rat removal would lend further support to
and Brown 1988, Brown 1989).
the interpretation that a positive response by the five
species of small granivores is the result of competitive
A long-term experimental study of interactions
among desert granivores and between these seed-eaters release.
and the ephemeral plants that provide their primary
We also used the repetition of the Dipodornys refood was initiated in 1977 by J. H. Brown, D. W. moval treatment 10 yr after the original experiment to
Davidson, and their colleagues (Brown et al. 1986). assess the relative contributions of direct competition
Thus far, these experiments have documented several (aggressive interactions and exploitation of food reeffects of granivorous rodents or ants on the abun- sources) and indirect interactions (responses to kandances and species diversity of desert plants (Davidson garoo rat mediated vegetation changes) on the distriet al. 1985, Brown et al. 1986, Brown and Heske 1990a, bution of captures of rodent species at our study site
Samson et al. 1992. Heske et al., in press). diffuse com- by comparing data for the original kangaroo rat repetition among granivorous ants (Davidson 1985), and moval plots, where grass cover has increased dramatan unexpected indirect mutualism between granivo- ically (Brown and Heske 1990a, Heske et al.. in press)
rous rodents and ants (Davidson et al. 1984, Brown et and the new kangaroo rat removal plots, where these
al. 1986) and between rodents and birds (Thompson vegetation changes have not yet occurred. We preet al. 199 1). Initial results of an experiment to detect dicted that (1) small granivore/omnivore species charcompetition among granivorous rodents were reported acteristic of desert scrub habitat (Perognathus jlavus,
in Munger and Brown (1981): results of the first 5 yr C. penicillatus, Peromyscus eremicus, P. maniculatus)
were reported more comprehensively in Brown and would respond only to the direct competitive effect
Munger (1 985). Numbers of five species of small gra- (show approximately equal abundances on original and
nivorous and omnivorous rodents (Chaetodipus pen- new kangaroo rat removal plots, with both greater than
Peromyscus eremicus, P. on their respective control plots), (2) small granivore/
icillatus, Perognathusjla~~us,
maniculatus, Reithrodontornys megalotis) increased omnivore species more typically associated with grasssignificantly on plots where three species of kangaroo land habitat (R. megalotis) would respond to both dirats (Dipodomys spectabilis, D. ordii, D. merriatni) had rect competition and indirect pathways mediated
been removed, but only after a long time lag.
through vegetation changes (thus. should have even
The original kangaroo rat exclosure and control plots greater abundances on original kangaroo rat removal
have now been continuously maintained for over 13 plots than on the new ones). and (3) folivorous species
yr. In January 1988 a new set of rodent manipulations typical of grassland (cotton rats: Sigtnodon hispidus, S.
was begun on eight other plots that were initially used ji~lviventer)would respond only to the indirect, vegefor other manipulations. This new series of kangaroo tation-mediated pathway (and be abundant only on
rat exclosures and controls provided additional repli- original kangaroo rat removal, or at least grassy, plots).
cation of the original competition experiment in space,
on new plots, and repeated the experiment in time, a
decade later. Thus. this study is unique in both the
Study site and experimental treatments
length of time that the manipulations have been mainThe study was conducted on the Cave Creek Bajada
tained and monitored. and in its repetition at a much
(bajada = an alluvial fan), 6.5 km east and 2 km north
later time.
Following Brown and Munger (1985), we used num- of Portal. Cochise County. Arizona. USA, at an elebers of grasshopper mice (genus Onychotnys) on kan- vation of 1330 m. The habitat is transitional between
garoo rat removals and controls as an additional test arid grassland and upper elevation Chihuahuan Desert
of the competition hypothesis. Grasshopper mice are scrub (Brown 1982), and varies from open, sometimes
primarily insectivorous (although they do consume grassy patches to areas dominated by shrubs (primarily
some seeds, especially in winter when insect abundance Gutierrezia sarothrae, Flourensia cernua, Ephedra triis low), and thus are not likely to compete for food furcata, Lycium torrevi, and Prosopis glandulosa) to
with kangaroo rats during most of the year. Grasshop- dense stands of arborescent shrubs (primarily Acacia
440
EDWARD J. HESKE ET AL.
greggi, Acacia neoverrcosa, and P. glandulosa) along
the usually dry watercourses that dissect the study site
in several places. The soil is a mixture of alluvial boulders mixed with and overlain by finer particles. The
entire 20-ha study site has been enclosed since July
1977 with a barbed-wire fence to exclude domestic
livestock.
Within the livestock exclosure are 24 study plots,
each 50 x 50 m (0.25 ha) in area and surrounded by
a fence of 6-mm wire mesh topped with 15 cm of
aluminum flashing (Munger and Brown 198 1, Brown
and Munger 1985). All plots were potentially rodent
proof, but holes (gates) of different sizes provide access
to selected plots by rodents of different species. Sixteen
gates are equally spaced (four per side) at ground level
around these plots: large gates (3.7 x 5.7 cm) allow
access by all rodent species, whereas small gates (1.9
x 1.9 cm) exclude the larger kangaroo rats but allow
access by several species of smaller rodents. To facilitate the location and use of the small gates by rodents,
wire-mesh baffles (15 x 15 cm) are placed perpendicular to the fences on either side at gate sites. Baffles
were not needed at the large gates. because well-worn
runways leading through most of these gates on nonremoval plots indicated that they are easily found and
readily used by rodents.
Plots were randomly assigned to various experimental treatments, and manipulations were initiated in
September 1977 following a 3-mo pretreatment census
period. Initial treatments included removal of some or
all rodent and ant species in a 2 x 2 factorial design,
or addition of millet seeds (see Brown and Munger
1985 for plot assignments and details of the manipulations). An additional treatment. removal of only the
largest species of kangaroo rat (Dipodornys spectabilis)
and its continued exclusion via medium-sized (2.6 x
3.0 cm) gates. was begun in July 1979 on one plot. and
replicated in February 1980 on a second. Results'of
the seed additions were discussed in Brown and Munger (1985) and will not be considered here. Ant removals did not affect rodent numbers at this site (Davidson et al. 1984, Brown and Munger 1985). Because
the factorial design of the experimental treatments allows us to focus attention just on the manipulations of
the rodent community, ant removals will also not be
considered further. We follow Brown and Munger
(1985) in using four plots (two with all Dipodotnys
excluded, and two with both Dipodonz),~and Pogonornyrrnes rugosus harvester ants removed) as the original kangaroo rat exclusion treatment, and four plots
(two unmanipulated and two with Pogono~nyrmexrl*gosus harvester ants removed) as the original controls.
In January 1988, six plots that had formerly been
seed additions and two plots that were ant removals
were reassigned in a 2 x 2 factorial, stratified-random
(treatments equally divided between north and south
sides of the study area) design as new replicates and
controls of the kangaroo rat and ant removal experi-
Ecology. Vol. 7 5 . No. 2
ment. Thus, a new set of four kangaroo rat removal
(two Dipodornys removal and two Dipodom.vs plus ant
removal) and four control (two unmanipulated and two
ant removal) treatments was established. Gate size was
adjusted on the plots selected for kangaroo rat exclusion, and removals were begun during the January rodent census.
Rodents were censused on all 24 plots approximately
once each month over a period of 2-3 consecutive
nights near the time of the new moon. Each plot was
live-trapped for one night by setting a single Sherman
live trap baited with either mixed bird seed or millet
at each of 49 permanent grid stakes spaced 6.25 m
apart. Gates were closed at the time traps were set to
insure that only individuals residing on the plots at the
time of each census were captured. Individuals were
marked either by toe-clipping (Chaetodipus, Perognathus, Reithrodonto~nysprior to 1987) or ear-tagging
with monel fingerling tags (all other species, Reithrodontotnys after 1987). Species, sex, mass, and reproductive condition were recorded for all captured animals before their release at the capture site.
Statistical analyses
We used repeated-measures analysis of variance
(rmANOVA; PROC ANOVA, SAS 1988) to test for
differences in numbers of captures of rodents of various
categories on experimental vs. control plots. For the
original set of four kangaroo rat removal and four control plots, a series of 155 census periods was used for
the analysis (September 1977-January 199 1). For the
new set of four kangaroo rat removal and four control
plots initiated in 1988, this series was divided into a
premanipulation series of 1 18 census periods (September 1977-January 1988), and a postmanipulation series of 37 periods (February 1988-January 199 1). There
is less statistical power when these shorter series are
used compared to results obtained from the full 155
periods. thus increasing the risk of a Type I1 statistical
error. However, this makes the test more conservative
when positive results are obtained. We used the combined densities of five species of small granivores on
experimental or control plots in these analyses because
the experimental design does not allow us to control
for possible interactions among these species, but we
also used rmANOVA to assess the responses of the
individual species.
To evaluate the relative influence of direct and indirect effects of kangaroo rat removal on numbers of
small granivores, we compared abundances, using
rmANOVA, of all small granivores and each species
individually on the original and new sets of experimental and control plots for the 3 yr following the start
of the new experiment (February 1988-January 199 1).
All analyses used the basic model statement CENSUS
TREATMENT CENSUS x TREATMENT. with
TREATMENT representing the blocking variable and
CENSUS representing the repeated measure. Signifi-
March 1994
COMPETITION I N DESERT RODENTS
cance levels of TREATMENT effects are presented in
Results.
30
25
44 1
1 D i p o d o m y s spp.
A
Control
I
o D ~ p u d u ~ n yremoval
s
4
The presence or absence of kangaroo rats was an
important factor affecting the abundance and distribution of small granivorous rodents on the experimental plots. Fig. IA illustrates that the exclosure fences were very successful at excluding kangaroo rats from
Dipodornys removal plots, while allowing them access
to control plots. Combined capture numbers of five
species of small granivores were significantly higher on
the four experimental plots from which Dipodo~nys
have been excluded since 1977 than on control plots
(rmANOVA. P = ,005, Fig. IB). In contrast, numbers
ofgrasshopper mice captures did not differ significantly
between original control vs. original Dipodo~nysremoval plots (rmANOVA, P = .59, Fig. IC).
30
-
Dlpodomys spp.
25 -
?
A
,
1 ' ' , I ' ' , I
'
I
Otlychomys spp.
,
I
' ' I , , , ,
'
'
,
I
' -
C
n
YEAR
0ocD
Small granivores
.
G
Control
B
I l ~ p o d o m y sremoval
FIG. 2. Captures of selected species of rodents o n four
control plots and four kangaroo rat exclusion plots where the
experimental treatments were initiated in January 1988. Data
are presented as 3-mo averages for clarity in presentation. (A)
Three species of kangaroo rats (Drpodotnj.~spectahllis. D.
merriarrzi. D. ordll). ( B ) Five species of small granivorous
rodents (Chaetodlpus penlcillarzis, Perognathzis Na~,zis,Perorrzysczis ererrzicus, Perotn~,sc'usm aniculatus. Reithrodontorrz~s
megalotrs). ( C ) Two species of grasshopper mouse (Onycllo112~'slezic'oga~ter.0 . torridus). Vertical dotted line indicates
period when kangaroo rats were removed from exclusion plots.
Prior to January 1988 there was no significant difference in the number of kangaroo rats captured on the
plots designated to become new sets of experimental
removals and controls (rmANOVA, P = .09), but the
modified gates and removal program were highly effective in excluding Dipodotnjs from experimental plots
after this time (rmANOVA, P = .01: Fig. 2A). Similarly. there was no significant difference in the number
of small granivores captured on plots designated as
Dipodornys
removals or controls up to January 1988
YEAR
(rmANOVA. P = .66), but a significant difference was
FIG. 1 . Captures of selected species of rodents on four
present during the postmanipulation period ( r m control plots and four kangaroo rat exclosures where experANOVA. P = ,009, Fig. 2B). Again, there was no sigimental treatments were initiated in September 1977. Data
are presented as 3-mo averages for clarity in presentation. (A) nificant difference in numbers of On)rhotn~,s
c aptured
Three species of kangaroo rats (Dlpodorrzys spectahilis. D.
on Dipodornys removal vs. control plots either before
rrzerrrami. D. ordii). ( B ) Five species of small granivorous
(rmANOVA. P = .22) or after the manipulation
rodents (Cllaetodipus penic'illatus, Perognathzis Na~,zis,Perorrz,vscus ererrzic'us. Perorrz~~sczis
maniczilarus. Reirhr~dontorrzj~s (rmANOVA, P = .35, Fig. 2C).
megalotis). ( C ) Two species of grasshopper mouse (OnychoNumbers of small granivores were much higher at
rrzj.s lezic'ogastcr, 0. torrrdus).
our study site in 1988-1990 than 1978-1980 (Figs. 1
E D W A R D J. HESKE ET AL.
442
1978-1980
1988-1990
Original
1988-1990
New
EXPERIMENT
FIG.3. Mean number of captures per census period of five
species of small granivorous rodents (species considered independently) on either the four control and four kangaroo rat
exclusion plots from the experiment initiated in September
1977 (original) o r the four control and four kangaroo rat exclusion plots initiated in J a n u a n 1988 (new) during the years
indicated. Note differences in scale of vertical axis. Significant
differences between original and new Dipodornys removal plots
in 1988-1990 indicate an indirect effect: 1978-1980 data for
original plots are included for comparative purposes only and
to illustrate the effect of competition on these plots in their
first 3 yr postmanipulation (see also Munger and Brown 198 1).
and 2). Small granivores were slow in responding to
the removal ofkangaroo rats in the original experiment
(Fig. 1B), and numbers of captures of small granivores
on kangaroo rat exclusion plots did not consistently
exceed those on control plots until well over a year
after the original manipulation. In contrast, a competition response was immediately obvious in the new
experiment (Fig. 2B), and numbers of captures of small
granivores were consistently greater on kangaroo rat
exclusion plots beginning with the month after the new
manipulation
Although the total number of small granivores captured in 1988-1 990 was slightly higher on the original
set of kangaroo rat exclosures than on the new set. the
difference was not significant (rmANOVA, P = .53).
When each species was examined individually, however. the most grassland-preferring of the five small
granivore species. Reithrodontornj-s megalotis, did show
significantly more captures on the original than on the
new kangaroo rat exclusion plots (rmANOVA, P = .04.
Ecologl. Vol. 75. No. 2
Fig. 3E). R. mrgalotis was about twice as abundant on
new kangaroo rat exclusion plots as on controls, but 3
times as abundant on the original kangaroo rat exclusion plots as on controls. The other four species of
small granivores all were more abundant on both sets
of kangaroo rat exclusions than controls as predicted
by the competition hypothesis (rmANOVA, all P values < .05). but differences between the new and original
exclusion plots were not significant (Fig. 3A-D). In
contrast. cotton rats, Sigmodon hispidus and S . ,fu/vrscens, were captured only on the four original kangaroo
rat exclusion plots and on two each of the original and
new control plots. All captures of cotton rats occurred
in grassy areas on these plots, although not all plots
with grassy areas yielded captures of cotton rats (E. J.
Heske, personal observation). Because grasses were
patchily distributed at our site, Sigmodon were captured on four out of eight control plots as well as all
four original kangaroo rat exclusion plots. but none of
the new kangaroo rat exclusion plots. Thus, cotton rats
were captured significantly more often on the original
than on the new kangaroo rat exclusion plots during
this period (68 vs. 0 captures; rmANOVA, P = .05),
whereas numbers of captures on original and new control plots were not significantly different (25 vs. 18
captures; rmANOVA, P = .73).
Our data clearly show that interspecific competition
with kangaroo rats affected the abundance and local
distribution of five species of small granivorous rodents
at our study site. Numbers of small granivores averaged twofold higher on the set of experimental plots
from which kangaroo rats had been continuously excluded since 1977 than on control plots (see also Brown
and Munger 1985). This response was observed again
when a second set of kangaroo rat exclosures and controls was initiated in 1988. There was no difference
between removal and control plots in the numbers of
insectivorous grasshopper mice in either the original
or new kangaroo rat removal experiments.
One difference between results from the original experimental treatments begun in 1977 and the new treatments begun in 1988 is the presence of a long time lag
in the former. In the original experiment, there was a
delay of 1 yr before any differences between small
granivore numbers on kangaroo rat exclusion and control plots were detected. In the new experiment, a response to the removal of kangaroo rats was apparent
immediately.
Brown and Munger (1985) suggested that the long
time lag before the response by small granivores to the
original kangaroo rat removals might be due either to
the fact that seed crops are episodic and at least some
species appear to rely heavily on seeds stored in caches.
or to the fact that reproduction is episodic and dispersal
may occur primarily by juveniles. Thus. a new seed
crop or new cohort of rodents might have been required
-
March 1994
COMPETITION IN DESERT RODENTS
before population responses to the manipulation would
occur. However, the original manipulations were also
started following an extended severe drought, when the
small granivorous rodents were at low density. The
new series was started when the abundance of small
granivores was at a record high, in part because it followed an El Niiio year of high precipitation and seed
production (Brown and Heske 1990b). We now believe
that the delayed responses to the original manipulations occurred because at that time there were simply
not many individuals of the small granivore species to
detect and move into the favorable habitat patches
created by removing kangaroo rats. The extended
drought during and preceding this period may also
have reduced resources to low levels throughout the
area, so that differences in resource abundance between
kangaroo rat exclosures and controls were not as detectable as in 1988. This difference underscores the
value of repeating ecological studies under as many
different conditions as possible. Our 1988 findings
demonstrate that a long time lag before a response is
not a general property of this system.
After the initial time lag in 1977-1 978. the response
of small granivores to the removal of competing kangaroo rats was highly consistent over 13 yr of monitoring. There was no indication that competition on14
occurred during "ecological crunches" when resources
were scarce (Wiens 1977). Rather. a negative influence
of kangaroo rats on the abundance and local distribution of small granivores appears to be a strikingly
consistent feature of the rodent community at our site
in spite of much year-to-year variation in precipitation.
primary production, and population densities of rodent
~nanuscript).
species (J. H. Brown et al.. ~tnp~tblished
This relative constancy of competition poses an apparent paradox when we consider patterns of community dynamics at our site (Brown and Heske 1990h).
On the one hand, kangaroo rats have a consistent negative impact on the local distribution of the small
granivores (Munger and Brown 198 1, Brown and Munger 1985, this study). On the other hand, species in this
community tend to exhibit highly individualistic patterns of population dynamics. the relative proportions
of species in the community have varied over time in
a manner not explainable by a simplistic competition
model. and many species that we have demonstrated
or suspect to be competing strongly show positively
correlated temporal variation in abundance (Brown and
Heske 1990h). How d o we reconcile the apparently
deterministic outcome of competition with the observed Gleasonian independence of species in this
community?
One solution may be to consider the processes that
govern population dynamics. The long-term temporal
fluctuations in rodent abundance reflect the influence
of environmental conditions within the local regron
(that includes a much larger area than just our study
area) on the birth and death rates of the pop~t1ation.s
443
of the different species. We observe highly individualistic, species-specific patterns of temporal variation
in abundance. both seasonally and year to year (Brown
and Zeng 1989, Brown and Heske 1990b). While we
have not yet identified all of the environmental variables causing these fluctuations, the available evidence
suggests that they reflect the interaction between the
unique resource requirements and environmental tolerances of each species and the temporal variation in
weather, food supply, vegetative cover, predators, and
so on. Thus. it is not surprising that species that tend
to have positively correlated population dynamics are
often ones that compete strongly; the requirements for
similar conditions and resources that cause similar
population fluctuations also tend to cause these species
to compete intensely.
In contrast, the differential responses of the small
granivores to the presence or absence of kangaroo rats
reflect the influence of smallpatches of habitat (patches
within our study site created by our experimental manipulations) on the habitat selection and movements
of individual rodents (see also Brown and Munger
1985). The experimental study plots at our site are
relatively small (0.25 ha). and individuals of the small
granivore species were often captured on more than
one plot. Therefore, differences in small granivore
abundance among plots apparently reflected primarily
habitat selection by individual rodents. Such smallscale habitat selection has been demonstrated in other
studies of desert rodents (e.g.. Rosen~weig 1973,
M'Closkey 1978, Price 1978. Wondolleck 1978). Other
studies have demonstrated that use of the shrub/open
space mosaic of microhabitats by small granivores is
affected by the presence of kangaroo rats (Price 1978,
Bowers et al. 1987). Our data indicate that small granivores also select habitat patches on a slightly larger
scale, i.e., study plots with or without kangaroo rats.
Regardless of the other variables that are driving the
population dynamics of the rodents in the community.
patches of habitat that are similar in every respect except for the absence of kangaroo rats are always more
favorable for small granivores to reside and forage in.
The scale(s) at which interactions between individuals
become translated into the dynamics of populations
and metapopulations rather than just patch selection
by a few individuals is an important area for future
research.
The long-term maintenance and monitoring of our
experiments, along with the repetition of the kangaroo
rat exclusion treatment 10 yr after initiation of the
original experiment, provide a unique opportunity to
evaluate the importance of an indirect mechanism by
which the absence of kangaroo rats can influence the
distribution of small granivores in this rodent community. Exclusion of kangaroo rats from study plots
at our site produced dramatic changes in the relative
abundances of several species of ephemeral plants (Davidson et al. 1985, Brown et al. 1986. Samson et al.
444
E D W A R D J. HESKE ET AL.
1992) and later caused major changes in vegetative
cover, particularly that of certain grasses (Brown and
Heske 1990a, Heske et al.. in press). Because these
differences in grass cover took many years to develop.
we can use differences between capture numbers of
small granivores on the original long-term kangaroo
rat exclosures and the new kangaroo rat exclosures
where such vegetation changes have not yet had time
to take place to measure the additional influence of
these vegetation changes on the abundance and distribution of several rodent species.
The relative importance of direct and indirect effects
of kangaroo rats on the local distribution of rodents
varied among species in a way predictable by their
general habitat associations. Four out of five species
of small granivores were not significantly more abundant on the original kangaroo rat exclusion plots than
on the new exclusion plots. These are species typical
of desert scrub, or. in the case of Pero~nyscusmaniculatus, not strongly associated with either desert scrub
or grassland. The effect of kangaroo rats on these species appears to be primarily through direct competition. by some combination of aggressive behavioral
interactions (Frye 1983) and resource depletion. R.
megalotis, the one of the five species most typically
associated with grasslands, however. was captured significantly more often on the original than on the new
kangaroo rat exclosures. This difference reflects an additional contribution of an indirect effect of the longterm changes in vegetation induced by the absence of
kangaroo rats and the differential selection of grassy
habitats by Reithrodonto~nys(Brown and Heske 1 9 9 0 ~ ) .
The distribution of harvest mice at our site was therefore affected by kangaroo rats through both direct competition and indirect pathways.
Two other species. Sigmodon hispidus and S. ,fulviventer, responded only to characteristics of the vegetation (Brown and Heske 1 9 9 0 ~ ) and
.
hence only to
indirect effects. Cotton rats are as large or larger than
kangaroo rats, primarily folivorous, and grassland specialists. Therefore, we expect that they are not intimidated behaviorally by Dipodo~nys,d o not compete
significantly with kangaroo rats for food, and prefer
habitats with high grass cover. Captures of both Sigtnodon spp. and R. tnegalotis are significantly correlated with grass cover on study plots at our site (Brown
and Heske 1 9 9 0 ~ )whereas
.
captures of the other common species of rodents at our site are not (E. J. Heske
et al.. unpublisheddata). Further. cotton rats have only
become regular inhabitants of our study site since 1987;
only seven captures of Sigmodon were made in the
preceding 10 yr even though they are regularly found
in other grassy sites within the San Simon Valley (E.
J. Heske. unpublished data). As expected. cotton rats
were significantly more abundant on the original than
on the new kangaroo rat exclosures. There was no consistent treatment effect in the distribution of cotton
rats other than that explainable by their positive cor-
Ecology. Vol. 75. No. 2
relation with grass cover, indicating that direct interactions between cotton rats and kangaroo rats were
minimal
The relati\e importance of direct vs. indirect effects
on community structure is unknown, and w ~ l probablq
l
be found to \arq among taxa and systems. One of the
mechanisms that we have considered a direct effect
(exploitative competition) could, in fact, technically be
considered an indirect effect because it also involves
other organisms (the seeds that the rodents consume).
Our distinction between direct and indirect pathways
is really between competitive mechanisms and noncompetitive mechanisms involving other kinds of organisms. Our approach of repeating an experiment in
time is a useful way to assess the nature and importance
of indirect effects because interactions involving indirect pathways are expected to play out with longer
time lags than direct interactions (Bender et al. 1984).
The indirect effect of kangaroo rats on other rodents
via changes in grass cover was not apparent until 10
yr after kangaroo rat removal was begun. Obviously,
it would not have been detected by the typical shortterm experiment. For this reason, indirect effects are
probably more widespread and important than is currently appreciated.
This paper results from the combined efforts of many researchers working at the Portal study site over the years. In
particular. M. Bowers. D. W. Davidson. B. Harney. J. Munger. W . Spencer, and D. Thompson made important contributions to this study. from its conception and initiation through
the collection of much of the data discussed herein. M. V.
Price. S. K. Robinson. R . E. Warner. and two anonymous
reviewers made helpful suggestions on earlier versions of the
manuscript. Research at this site has been supported by National Science Foundation Grants, most recently BSR8718139.
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You have printed the following article:
Long-Term Experimental Study of a Chihuahuan Desert Rodent Community: 13 Years of
Competition
Edward J. Heske; James H. Brown; Shahroukh Mistry
Ecology, Vol. 75, No. 2. (Mar., 1994), pp. 438-445.
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