Download Experimental Manipulation of a Desert Rodent Community: Food

Experimental Manipulation of a Desert Rodent Community: Food Addition and Species
Removal
Author(s): James H. Brown and James C. Munger
Source: Ecology, Vol. 66, No. 5 (Oct., 1985), pp. 1545-1563
Published by: Ecological Society of America
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Ecology, 66(5), 1985, pp. 1545-1563
© 1985 by the Ecological Society of America
EXPERIMENTAL
MANIPULATION
OF A DESERT RODENT COMMUNITY:
FOOD ADDITION AND SPECIES REMOVAL1
JAMES
H.
BROWN
AND
JAMES
C.
MUNGER2
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721 USA
Abstract. Since 1977 we have been conductingexperimentsin which we add supplementalseeds
or remove certaincombinationsof species of seed-eatingrodents and ants from 0.25-ha plots in the
ChihuahuanDesert of southeasternArizona. These experimentsevaluate the extent to which food
availability and interspecificcompetition influence rodent populations. Monitoringwith live traps
revealedthat:(1) the addition of seed at the rate of 96 kg plot-' yr-' resultedin an increaseddensity
of the largestgranivorousrodentspecies (Dipodomysspectabilis),decreasesin the densities of the two
next-to-largestspecies (D. merriamiand D. ordii),and no detectablechangesin the densities of other
rodents;(2) the removal of D. spectabilis,as well as other experimentallyinduced changes in the
abundanceof this species, resultedin reciprocalshifts in the densities of the two congenericspecies,
D. merriamiand D. ordii,and no significantchangesin densitiesof otherrodents;and (3) the removal
of all three Dipodomysspeciesresultedin largeincreasesin densityof fourof the five speciesof smaller
seed-eatingrodents,but had no effect on two species of insectivorousrodents.Taken together,these
resultsindicatethat limited food resourcesand interspecificcompetitionplay majorroles in regulating
the density of rodent populations and determiningthe organizationof desert rodent communities.
However,the responsesof the rodent populationsto our manipulationswere unexpectedlycomplex;
they includedlong time lags, asymmetricalinteractions,and little compensationin energyconsumption. This indicateshow much remainsto be learnedabout the processesthat determinethe structure
and function of even this relativelysimple and well-studiedcommunity.
Key words: community; competition; desert; Dipodomys; experiment; food limitation; granivory;
population; rodent; seeds.
INTRODUCTION
A fundamental question of population and community ecology is what determines the absolute and
relative abundances of species within local regions. Local population density is a consequence of the survival,
reproduction, and dispersal of individuals. These processes are affected by the capacity to tolerate the physical environment, the availability of essential resources, and interactions with other individuals of the
same and different species. One problem with assessing
the roles of these environmental factors in limiting
population density is that often they are not independent of each other. Thus, for example, both fluctuations
in climate and the presence of competing species can
affect the availability of resources, and both climate
and parasite infections can change requirements for
resources. In foraging to meet these varying resource
requirements, individuals may differ in their risk of
predation.
The independent and interacting effects of such limiting factors can be studied by controlled field experiments in which some variables are held constant while
others are manipulated systematically. We used such
experiments to analyze the effects of two factors, food
availability and the presence of other rodent species,
on the population densities and community organization of desert rodents, and we discuss the possible
I Manuscriptreceived 20 October 1983; revised 20 June
1984; accepted31 August 1984.
2
Present address:Departmentof Zoology, University of
Wisconsin, Madison, Wisconsin 53706 USA.
relationships between these factors and climatic variation and predation.
Communities of North American desert rodents may
be comprised of as many as 16 species, of which about
half are usually primarily granivorous (Table 1). Most
ecological studies of desert rodents have focused on
these seed-eaters, because they provide an excellent
system for assessing the effects of food limitation and
interspecific competition on a guild of ecologically similar species (e.g., see Brown et al. 1979b and references
therein, Munger and Brown 1981, Thompson 1982a,
b, Munger et al. 1983, Price and Brown 1983, Kotler
1984, Brown 1984). All of these species feed primarily
on the seeds of annual plants, a particulate resource
that is produced in pulses following infrequent and
unpredictable precipitation. Although seeds appear to
be harvested (or at least to disappear from the soil
surface) rapidly following flushes of seed production,
they can persist for many months or years in the soil
and in the stored caches of rodents. Potential competition for these food resources occurs not only among
rodent species, some of which differ substantially in
morphology, physiology, and behavior, but also between rodents and other kinds of desert granivores such
as birds and insects (Brown and Davidson 1977, Brown
et al. 1979b).
One advantage of the desert rodent system is that it
lends itself to experimental manipulations of such potentially important factors as availability of food
(Abramsky 1978, Hay and Fuller 1981), predation risk
(Thompson 1982b, Kotler 1984), habitat structure
JAMESH. BROWN AND JAMESC. MUNGER
1546
TABLE 1.
Ecology, Vol. 66, No. 5
Some characteristicsof the 16 species of rodentscapturedon our study site.
Species
Family
Dipodomysspectabilis
Dipodomysordii
Dipodomysmerriami
Perognathuspenicillatus
Perognathusflavus
Reithrodontomysmegalotis
Reithrodontomys
fulvescens
Peromyscusmaniculatus
Heteromyidae
Heteromyidae
Heteromyidae
Heteromyidae
Heteromyidae
Cricetidae
Cricetidae
Cricetidae
Peromyscuseremicus
Cricetidae
Onychomysleucogaster
Onychomystorridus
Neotoma albigula
Sigmodonhispidus
Spermophilusspilosoma
Ammospermophilusharrisi
Thomomysbottae
Cricetidae
Cricetidae
Cricetidae
Cricetidae
Sciuridae
Sciuridae
Geomyidae
Body
mass
Diet
Seasonalactivity (g)
active all year 125.0
granivorous
47.0
active all year
granivorous
active all year
40.8
granivorous
hibernates
15.4
granivorous
7.2
hibernates
granivorous
active all year
10.4
granivorous
active all year
13.2
granivorous
21.7
granivorousor active all year
omnivorous
21.6
granivorousor aestivates?
omnivorous
insectivorous
active all year
32.6
insectivorous
active all year
24.9
folivorous
active all year 173.5
folivorous
active all year 109.5
folivorous
hibernates
92.7
omnivorous
active all year 107.6
herbivorous
active all year 118.2
Total
* Based on captureson the control plots with the gates closed.
(Rosenzweig 1973, Price 1978, Thompson 1982b), and
interspecific competition (Schroder and Rosenzweig
1975, Brown and Davidson 1977, Price 1978, Munger
and Brown 1981, Abramsky and Sellah 1982). We tested
the hypothesis that food is a limiting resource by adding seeds to experimental plots. We also tested the
hypothesis that these species compete by experimentally removing certain combinations of species from
other plots. We assessed the effects of these manipulations by comparing the population densities, energy
consumption, and life histories of rodents on the experimental and control plots.
METHODS
Study site
The study was conducted on the Cave Creek Bajada
(a deposit of alluvial soil) 6.5 km east and 2 km north
of Portal, Cochise County, Arizona, at an elevation of
1330 m. The soil at this site is a fairly homogeneous
mixture of alluvial boulders mixed with and overlaid
by finer particles. The terrain is relatively flat except
where it is dissected by several temporary watercourses. The vegetation is primarily upper elevation Chihuahuan desert scrub, but the habitat structure varies
from open grassy areas to stands of widely spaced shrubs
(primarily Gutierrezia, Ephedra, Flourensia) to dense
stands of arborescent Acacia and Prosopis along the
usually dry watercourses. The entire study site, encompassing - 20 ha, has been enclosed since July 1977 with
a barbed-wire fence to exclude domestic livestock.
Experimental plots
Experiments were conducted on 24 plots, each 0.25
ha in area (50 m on a side). These plots were placed
Total
Population
number
density*
Biomass of cap(individtures
uals/ha)
(g/ha)
7.92
990.0
1207
0.64
30.1
231
19.84
809.5
1612
1.52
23.4
93
0.64
4.6
266
0.60
6.2
199
1
rare
insignificant
rare
57
insignificant
0.28
6.1
164
1.80
2.24
2.76
58.7
55.8
231
279
259
4
27
7
0
478.9
rare
insignificant
rare
insignificant
rare
insignificant
not
unknown
measured
>38.24
>2463.3
4637
to include the flattest areas of most homogeneous vegetation but to leave at least 25 m between adjacent plots
(Fig. 1). Twenty-three plots were established in July
1977. The final plot was added in July 1979.
All plots were fenced with 6-mm wire mesh. Fencing
90 cm wide was buried 20 cm in the ground and bent
outward 10 cm at the bottom to discourage rodents
from digging under. The remaining 60 cm of wire was
supported vertically by metal posts (13-mm steel reinforcing rod). A 15 cm wide vertical strip of aluminum
flashing was riveted to the top of the fence to prevent
rodents from climbing over. This fencing rendered all
plots potentially rodent-proof, but 16 holes (gates) of
varying sizes cut in the fences (4 gates equally spaced
along each side of each plot) allowed access of selected
rodent species to appropriate plots (see Experimental
Manipulations, below). The fencing uniformly excluded jackrabbits (Lepus californicus) from all plots, but
did not restrict access by cottontail rabbits (Sylvilagus
auduboni), which regularly jumped over the fences.
Experimental treatments were assigned to the plots
at random, with the three exceptions mentioned below.
There were two replicates of each of 12 treatments
(Table 2): 4 kinds of seed addition, 3 kinds of rodent
removal, 2 kinds of ant removal, 2 kinds of rodent and
ant removal, and 1 control. A 3-mo pretreatment census period began in July 1977. During this time, large
(3.7 x 5.7 cm) gates in the newly constructed fences
allowed free movement of all rodents into and out of
all plots. Experimental manipulations were initiated in
September 1977. With the exception of the experimental manipulations, every effort was made to treat
all plots identically, including subjecting them to the
same intensity of rodent trapping and human traffic
October 1985
MANIPULATIONOF A DESERTRODENT COMMUNITY
1547
(which was confined as much as possible to designated
east-west pathways along the permanent grid stakes in
each plot).
There were three exceptions to this schedule and to
random assignment of treatment to plots. One of the
two plots (Plot 5) initially designated for removal of
the ant species Pogonomyrmex rugosus was found to
contain no colonies of this species, and in July 1979,
Plot 12 (previously unassigned) was assigned to this
treatment. On the same date, Plot 5 was reassigned for
removal of the rodent species Dipodomys spectabilis
(a new experimental manipulation) and another plot
(Plot 24) was constructed to provide a second replicate
of this treatment.
Experimental manipulations
Seed addition experiments. -Eight 0.25-ha plots were
assigned to four seed addition treatments: (1) large size,
constant rate; (2) small size, constant rate; (3) mixed
sizes, constant rate; and (4) mixed sizes, pulsed. In all
cases we added seed to each plot at a rate of 96 kg/yr.
This should have approximately doubled the availability of seed biomass, because our estimates of native
seed production are 400 kg ha-' *yr-'. From September 1977 to August 1980 the supplemental seed was
milo (Sorghum vulgare Pers.), but when we found that
granivores, especially ants, do not avidly take this
species, we switched in September 1980 to millet (Panicum miliaceum L.). "Large" seeds were added whole
(Xmass = 6 mg for millet), whereas "small" seeds were
cracked (X mass _ 1 mg). A "mixed" addition was
simply an equal mixture of whole and cracked seeds.
In the "constant rate" additions, 8 kg of seed were
supplied once per month, whereas in the "pulsed"
treatment the entire yearly allotment of 96 kg was added
in 2-6 equal installments over the 2-mo period (September-October) corresponding to peak seed production by the summer annuals. Seeds were scattered by
hand over the entire area of each plot.
Dipodomys removal experiment.--Four plots were
assigned for removal of all Dipodomys species (D. spec-
FIG. 1. Aerial photographof the study site, showing the
natureof the vegetationand the locations of the 24 experimental plots, each 50 m on a side (0.25 ha in area). The
experimentaltreatmentin each of the numberedplots can be
determinedby referringto Table 2.
tabilis, D. merriami, and D. ordii; see Table 2). In
September 1977 the gates in the fences were reduced
in size to prevent passage by Dipodomys, and all individuals of this genus were removed as they were
captured in monthly censuses. The reduced gate size
(1.9 x 1.9 cm) effectively prevented colonization by
Dipodomys but allowed the free passage of five species
of small granivorous rodents (Perognathus [hereafter
abbreviated Pg.] penicillatus, Pg. flavus, Peromyscus
eremicus, P. maniculatus, and Reithrodontomys meg-
Outline of the 12 experimentaltreatments,including control. Note that some of the rodent and ant removal
experimentshave a factorialdesign, and duplicatetreatmentsare listed underboth headings.
TABLE 2.
Control
Treatment Plots
Unmanipu- 11, 14
lated
Seed addition
Treatment
Plots
constant
seeds,
6, 13
Large
rate
Small seeds, constant 2, 22
rate
Rodent removal
Treatment
Plots
5, 24
Dipodomysspectabilis
Mixed sizes, constant
rate
All Dipodomysspecies 3, 19
and Pogonomyrmex
rugosus
All seed-eating
7, 16
rodents
All seed-eating
10, 23
rodentsand ants
9, 20
Mixed sizes, temporal 1, 18
pulse
All Dipodomysspecies
15, 21
Ant removal
Treatment
Plots
Pogonomyrmexrugosus 8, 12
Pogonomyrmexrugosus 3, 19
and all Dipodomys
species
All seed-eatingants
4, 17
All seed-eatingants
and rodents
10, 23
1548
JAMESH. BROWN AND JAMESC. MUNGER
alotis), as well as two insectivorous species (Onychomys leucogaster and 0. torridus). We placed wire-mesh
baffles (15 x 15 cm) perpendicular to the fences on
either side at the locations of the small gates to enable
the rodents to find the gates easily and to move freely
both into and out of the plots (well-worn runways attested to the fact that rodents had no difficulty in finding the much larger gates on nonremoval plots, and
therefore baffles were not used on these plots). Two of
the Dipodomys-removal plots, as well as two others
(see Table 2), were assigned for the removal of the large
harvester ant, Pogonomyrmex (hereafter abbreviated
Po.) rugosus, as part of a 2 x 2 factorial experiment.
Consequently, results on four experimental plots could
be compared to those on four "control" plots to analyze
for the effects of Dipodomys removal with the effect of
ant removal held constant.
D. spectabilis removal experiment. -Similar procedures were used to exclude only D. spectabilis from
two plots. Gates and baffles were placed as described
above, except that the gates were large enough (2.6 x
3.0 cm) to allow the free passage of D. merriami and
D. ordii as well as the small rodent species. Removal
of D. spectabilis began in July 1979 on Plot 5 and in
February 1980 on Plot 24.
Ant removal experiments. -Four plots were assigned
for removal of all granivorous ant species and four were
designated for selective removal of Po. rugosus. Removal and continued exclusion of ants was accomplished by the use of poisoned bait (Myrex through
1980 and AMDRO thereafter), which was applied beginning in September 1977. Studies of toxicity to mammals and our experimental results suggest that neither
poison had any significant effect on the rodent populations. On plots from which all seed-eating ants were
to be removed, bait was both broadcast and applied
to individual colonies. On Po. rugosus removal plots,
bait was applied only to colonies of this species. Colonies of Po. rugosus and Po. desertorum that persisted
after poisoning were asphyxiated by first pouring 250
mL of gasoline down the entrance hole, then sealing
the entrance. (As described above, there was a change
in the assignment of one Po. rugosus removal plot.)
On two of the ant removal plots, rodent removals were
also carried out.
Measurement of responses
We used a monthly trapping regime to assess changes
in the densities and total biomass of rodent species and
in the life history attributes of individual rodents in
response to our experimental manipulations. Trapping
was conducted on all 24 experimental plots during a
period of two or three successive nights at approximately monthly intervals, at a time corresponding as
much as possible to the time of the new moon. During
each monthly trapping period, each plot was trapped
for a single night with 49 Sherman live traps (23 x
8 x 9 cm) baited with mixed birdseed or millet and
Ecology, Vol. 66, No. 5
placed at permanent grid stakes spaced at 6.25-m intervals. The standard procedure was to close the gates
through the fences on the night of trapping to insure
that only individuals residing on the plots were captured. However, during three of the monthly trapping
periods (March 1980, April 1981, and October 1982)
the plots were trapped with the gates open in order to
capture both residents and those individuals that regularly foraged on the plots but had their home burrows
outside.
All rodents captured were individually marked for
subsequent identification. The three smallest species
(Pg. penicillatus, Pg. flavus, and R. megalotis) were
marked by toe clipping; all other species were marked
with monel fingerling tags attached to the ears. Whenever an individual was captured it was weighed and
checked to determine reproductive condition. The latter was scored by classifying males as either having
fully scrotal testes, showing evidence of recently descended testes (distended scrotum but abdominal
testes), or being reproductively inactive. Females were
scored as being either in estrus (swollen vaginal orifice, with or without vaginal plug), pregnant (embryos
palpable), lactating (nipples reddish and enlarged), or
reproductively inactive.
From these data on captured individuals, five life
history attributes were assessed for each species on each
plot: average adult body mass, percent of population
exhibiting reproductive activity, and two measures of
residence status. Average adult body mass of a species
was calculated as the average mass of individuals that
exceeded a threshold mass for their species and sex;
the threshold used was the lowest mass at which the
majority of individuals of a given species and sex
showed reproductive activity. Rate of energy consumption was calculated using the number of individuals, the average individual body mass (M, in kilograms), and the allometric equation E = 753M0-67,
where E is the individual rate of energy consumption
(in kilojoules per day) (King 1974). Percent reproductive was defined, for males, as the percentage of individuals above the adult-mass threshold with scrotal or
recently descended testes, and, for females, the percentage of adult individuals either in estrus, pregnant,
or lactating. The first measure of residence status was
average residence time of individuals on a plot, which
was defined as the average time between the first and
last captures of each individual of a given species captured on that plot. This measure provides an estimate
of minimum survival time of an individual on a permanent home range. The second measure, percent residents on a plot, was calculated as the number of individuals that were captured more than once on that
plot divided by the total number of individuals of that
species captured on the plot.
The experimental manipulations and trapping program are ongoing. For purposes of the present paper,
however, we shall in general limit our consideration to
MANIPULATIONOF A DESERTRODENT COMMUNITY
October 1985
1549
= Small Seedeaters
= Dipodomys
l.
merriami + D. ordii
etbi
= D. spectabilis
0
'I,
0
0.
CL
V)
0
I0.
V)
L
z
C
NON-SEEDEATERS
NNSEE3.E0NNEEE
z
Onychomys spp.
R=
=Neotoma albigula
LL
2u
2.0-
S-
YEAR
TREATMENT
C
I§
1
3 4 5
Control
1 2
41
Small Seed Constant
4
5
Large Seed Constant
1 l21 3 14
Mixed Seed Constant
5
Mixed Seed Pulse
FIG.2. Effectsof the various seed addition treatmentson the mean population densities of seed-eatingand non-seedeating rodents. Data are shown by treatment(four seed addition manipulationsplus control), two plots per treatment,and
by year (five years;year 1 = 1977-1978). Note that as a group, seed-eatingrodents did not change in density over the 5 yr
in responseto supplementalseed, althoughD. spectabilisincreasedand D. merriamiand D. ordii decreasedon most experimental plots but not on the controls.
data for the 5-yr period from June 1977 to June 1982.
In analyzing the effects of trapping with the gates open,
however, we also consider captures for the 3-mo period
September-November 1982.
Statistical analyses
Despite the large spatial scale and long temporal
duration of these experiments, replication of the particular treatments was limited. This created problems
for statistical analysis. Nevertheless, we have tried to
be statistically rigorous in our treatment of the data.
Because the number of replicates for each test was small
we have used nonparametric analysis (specifically, the
Mann-Whitney Utest; Siegel 1956) wherever possible.
In those cases where the number of replicates was so
small as to preclude any possibility of significance with
nonparametric tests, we have used parametric procedures (i.e., analysis of variance). Because a U test typ-
ically has less statistical power than an analysis of variance, our reliance on the former test could have led to
an increased frequency of Type II errors. This does not
appear to have occurred, however. For each of the 56
U tests presented in the Appendix, we also tested the
same data by an analysis of variance. For only two of
the tests was there a significant difference; in both instances the U test gave the smaller probability value
(see Appendix).
To analyze for the effect of experimental treatment
on the four life history parameters, we compared results for experimental plots (where variables had been
manipulated) with those for control plots (where the
same variables had been held constant). To determine
the effect on densities and biomass, we used the magnitude of the change on each plot from the period
before manipulation to the period after manipulation.
This helped to control for any chance differences in
Ecology, Vol. 66, No. 5
JAMES H. BROWN AND JAMES C. MUNGER
1550
600~7
500-
400-
300-
"I
^1
11-1
"I^
11-
."
-
~
.
5~
1-,.
7Sc=5-~
200-
O
100-
I
I
YEAR
"I
>0 TREATMENT
ci
zz
0
NON-SEEDEATERS
(_
= Onychomys
LJ
z
LJ
spp.
= Neotoma albigula
Fl
TREATMENT
Control
Small Seed Constant
uiL
LI.LLihi.
Large Seed Constantl
Mixed Seed Constant
Mixed Seed
Pulse
FIG. 3. Effects of the various seed addition treatments on the mean energy consumption of seed-eating and non-seedeating rodents. Data are plotted by treatment and year as in Fig. 2. Note that provision of supplemental seed resulted in little
if any increase in total seed-eating rodent biomass, although D. spectabilis increased at the expense of D. merriami and D.
ordii.
relevant variables between plots; such differences can
lead to misleading results when comparisons are made
among a small number of randomly assigned and
somewhat heterogeneous (in habitat and rodent population, in this case) plots. For these comparisons, the
results included the entire 1st yr
before-manipulation
of data (three pretreatment sampling periods and eight
posttreatment samples; July 1977 to June 1978) because there was no indication of any significant response to the manipulations
during this period and
because this larger data base permitted a more precise
characterization of the initial state of each plot than if
only the three pretreatment samples had been used.
By attempting to be rigorous and conservative in our
statistical analyses, we ran the risk of failure to detect
significant results that would have been revealed if replication had been greater or if less conservative tests
had been employed. For this reason we emphasize that
the results we report in the next section may not represent the only responses of rodents to our experimental manipulations, but they are certainly the most dramatic responses and the only ones we were able to
document with statistical confidence.
RESULTS
Over the entire period, July 1977 to June 1982, we
recorded 4637 captures of 15 rodent species in a total
of 68 159 trap-nights (Table 1). The low frequency of
captures insured that sufficient empty traps were alshould not
ways available so that trap competition
have influenced the results. In performing the following
analyses we frequently combined rodent species into
functional groups whose member species were likely
to respond similarly to our manipulations. Seed-eating
rodents included: (1) the kangaroo rat, Dipodomys
spectabilis, the largest granivorous species; (2) D. mer-
1551
MANIPULATIONOF A DESERTRODENT COMMUNITY
October 1985
a) Seed
addition
b) Control, ant removal,
D. spectabilis removal
plots
6-
plots
KEY
1981-1982
plot no.
5C)
1977-1978
c
4-
'
3-5
2-
--
0
1c
QL
0-
I
I
I
I
I
0
1
2
3
4
I
I
I
I
Density of D. spectabilis
(no./plot)
I
0
1
2
3
Density of D. spectabil/s
(no./plot)
FIG.4. Changesin the mean densitiesof D. merriamiand D. ordiirelativeto changesin the mean densityof D. spectabilis
in responseto various experimentalmanipulations.Each line representsthe changeson one plot between the 1st yr of the
study(1977-1978) and the last 2 yr (1980-1982). Treatmentsand plot numbersareexplainedin Table 2. Note the pronounced
tendency for reciprocaldensity shifts, with D. spectabilisincreasingat the expense of D. merriamiand D. ordii on seed
addition plots and the reversetrend on other plots, includingcontrol and D. spectabilisremoval plots.
riami and D. ordii, medium-sized kangaroo rats; and
(3) five species of small granivores, Perognathus penicillatus, Pg. flavus, Peromyscus maniculatus, P. eremicus, and Reithrodontomys megalotis. Non-seed-eating rodents included: (1) Onychomys leucogaster and
0. torridus, small insectivorous forms; and (2) Neotoma albigula, a large folivore.
Effects of seed addition
The primary responses to the availability of supplemental seeds were: (1) a substantial increase in the
density and energy consumption of the largest granivorous rodent species (D. spectabilis); (2) a significant
decrease in the total energy consumption of all other
seed-eating species; the latter effect can be attributed
to (3) a large decrease in the combined density and
energy consumption of the two medium-sized granivorous species (D. merriami and D. ordii) (Figs. 2 and
3, Appendix). These responses appeared to occur on
all of the seed addition treatments. The size of seed
particles provided and the temporal schedule of seed
addition had little apparent effect on the rodents. The
only exception was an apparently longer residence time
and a higher percentage of adult individuals in reproductive condition for D. spectabilis on the plots where
seeds were added in a seasonal pulse rather than evenly
throughout the year. None of the smaller rodent species
other than Dipodomys showed any significant response
to the seed addition treatments (Figs. 2 and 3).
On the eight plots to which seeds were added, D.
spectabilis increased (between year 1 and years 2-5) in
mean density from 0.97 to 1.61 individuals per plot
per period (a 66% increase) and in energy consumption
from 170 to 288 kJ plot- 'd-1 (69%) (Fig. 4). During
this same period D. spectabilis on control plots decreased in density from 1.33 to 0.98 individuals per
plot per period (26% decrease) and in energy consumption from 242 to 165 kJ plot- d- (32%). Effects
of seed addition were significant for both measures
(Mann-Whitney Utests: U = 1, P = .044 for both variables). The corresponding decreases in both density
and energy consumption of D. merriami and D. ordii,
in response to the addition of seeds, were even more
significant (U = 0, P = .022 for both variables): density decreased from 2.35 to 1.37 individuals per plot
per period (58%) and energy consumption decreased
from 211 to 126 kJ plot- -d-l (60%) on plots to which
seeds were added, while on control plots density increased from 2.54 to 2.65 individuals per plot per period (4%) and energy consumption increased from 228
to 244 kJ plot-
d-l
(7%).
We analyzed attributes of individual kangaroo rats
that may have caused or responded to these changes
in population density with increased food availability.
1552
JAMES H. BROWN AND JAMES C. MUNGER
Dipodomys
spectobilis
a D. ordii
merriami
Dipodomys
1400
Ecology, Vol. 66, No. 5
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October 1985
MANIPULATIONOF A DESERTRODENT COMMUNITY
Although none of the species exhibited a detectable
increase in reproductive success in response to additional seeds, mean body mass of D. spectabilis was
greater on seed addition plots than on controls (U =
0, P = .022; Appendix), a result that could be attributed either to increased growth of D. spectabilis or to
movement of large individuals onto enriched plots.
Conversely, D. merriami had a significantly greater
proportion of individuals captured only once (not recaptured) on the seed addition plots than on the controls (U = 0, P = .022). This apparent reduced ability
of D. merriami to maintain permanent home ranges
in the face of increased densities of D. spectabilis implies competition between these kangaroo rat species.
Additional insights into this interaction are afforded
by the results of trapping with the gates in the fences
open. Because individuals with home burrows off the
plots moved onto the plots to forage, we found that
more individuals of all Dipodomys species were captured when the gates were left open than in the preceding and following trapping periods with the gates
closed (Fig. 5). However, the increase was to 2.09 times
as many D. spectabilis and 1.85 times as many D.
merriami and D. ordii on the seed addition plots as on
the controls (U = 0, P = .022 for both groups). The
net result was that when the gates were open, 3.36 times
as many individuals of D. spectabilis foraged on seed
addition as on control plots (U = 0, P = .022), whereas
D. merriami and D. ordii activity on the seed addition
plots increased only to the approximate level on control
plots (actually it was 1.21 times the control level, but
U = 5, P = .267). Clearly individuals of all the kangaroo rat species were attracted onto the plots that
received the supplemental seeds, but only D. spectabilis
was able to increase the density of permanent residents;
the increase in D. spectabilis apparently inhibited the
establishment of its smaller congeners.
Effects ofD. spectabilis
When preliminary results of the seed addition experiments suggested that D. spectabilis increased at the
expense of D. merriami and D. ordii, we initiated an
experiment in which D. spectabilis was removed from
two plots. Such a manipulation was expected to yield
interesting results for two reasons. On the one hand,
in terms of total food consumption D. spectabilis is
one of the two most important rodent species in the
community; it accounted for 53.0% of energy con-
1553
sumption by granivorous rodents on the control plots.
Thus, removal of D. spectabilis should have made
available large quantities of seeds for consumption by
other seedeaters. We had already observed (Munger
and Brown 1981) and now confirmed (see Effects of
Dipodomys Species, below) that small granivorous rodents increased several-fold in density following the
removal of all three Dipodomys species, and much of
this response could potentially be attributed to removal
of D. spectabilis, because of its large energy consumption. On the other hand, D. spectabilis is much more
similar in morphology (including body size), physiology, and behavior to its congeners, D. merriami and
D. ordii, than to any other seed-eating rodents on the
study site. On this basis, D. spectabilis might be expected to have a larger competitive effect on the other
Dipodomys species than on the granivorous rodents in
other genera.
The removal of D. spectabilis from two plots was
begun z 2 yr after the other experiments had been initiated, and no effects can yet be demonstrated with
statistical confidence because of the small number of
replicates per treatment. Clearly there was no noticeable effect during the 1st yr (1979-1980). During the
following 2 yr (1980-1982), combined average densities of D. merriami and D. ordii increased by a factor
of 2.89 to 3.14 individuals per plot where D. spectabilis
had been removed. However, they also increased by a
factor of 1.62 to 2.66 individuals per plot on the control
plots. Removal of D. spectabilis had no significant effect on any of the granivorous rodent species in other
genera.
Much more statistical power can be used to evaluate
the effects of D. spectabilis on other rodents by considering the data for other plots. Densities of D. spectabilis changed substantially in response to other manipulations, and we examined the correlation between
these changes and the response of the populations of
other rodent species. Such an analysis provides strong
evidence for a significant competitive interaction between D. spectabilis and the other two kangaroo rat
species. Fig. 4 shows that in general D. spectabilis increased and D. merriami and D. ordii decreased when
seeds were added, whereas the opposite trend occurred
on the other plots where all three Dipodomys species
were present and also on the two plots where D. spectabilis was removed. These overall reciprocal density
shifts are highly significant (Fisher's exact test, P =
FIG.5. Resultsof trappingin the indicatedplots with the gates in the fences open, comparedwith resultsof trappingwith
the gates closed in the previous and followingtrappingperiods. O control and ant removal plots, 0 seed addition plots, A
Dipodomysspectabilisremoval plots, and D Dipodomysspp. removal plots. Treatmentsand plot numbersare explained in
Table 2. Note that all of these functionalgroupsexcept the small seedeatershad highercapturesin all cases with gates open
than with gates closed (points above dashed line indicatingequal energyuse). Also, the seed-eatingDipodomysspecies, but
not the insectivorousOnychomysspecies, showedgreaterincreaseson plots where seeds had been added than on controlsor
where ants had been removed.
JAMESH. BROWN AND JAMESC. MUNGER
1554
Dip o do mys
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Ecology, Vol. 66, No. 5
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1982
FIG.6. Changesover time in the densities of each of the three functionalgroupsof rodents on four experimentalplots
from which all three Dipodomys species were removed beginning in October 1977, compared to the densities on four control
plots. Each point represents the mean of four plots.
.0055). Although interpretation of these results is complicated by the fact that other variables besides the
density of D. spectabilis differed among plots, the results are consistent in suggesting that the various manipulations affected the densities of D. spectabilis, which
in turn had direct negative effects on populations of D.
merriami and D. ordii.
Although our results do not show that D. spectabilis
by itself has significant effects on the small granivorous
rodents in other genera, all of the trends suggest that
there may be some competitive interaction. Densities
of small granivores increased by a factor of 4.97 to 0.83
individuals per plot on the two plots from which D.
spectabilis had been removed, compared to an increase
of 2.05 times to 0.57 individuals per plot on control
plots with D. spectabilis present. An analysis that included these four plots and all other plots with D.
spectabilis present revealed a weak trend toward reciprocal density shifts (Fisher's exact test, P = .16). Interestingly, both of these trends run counter to what
would be predicted if D. spectabilis had an indirect
positive effect (through its negative effect on the medium-sized kangaroo rat species) on the small granivores. Clearly, more data are required to determine
whether D. spectabilis has significant interaction with
the granivorous rodents other than its congeners.
Effects of Dipodomys species
We removed all three species of Dipodomys from
four plots and monitored the populations of the small
rodents on these plots and on four control plots to test
for competition among rodent species. As expected
under the hypothesis that competition for food is important in this community, small seed-eating rodents,
but not small nongranivorous species, increased in
density in response to this manipulation. This result
was well established within 3 yr and was reported briefly elsewhere (Munger and Brown 1981). Here we include two additional years of data and present a more
detailed analysis.
The results continue to support the competition hypothesis. During the 3-mo pretreatment period and for
an additional 8-9 mo after Dipodomys was removed,
there were no significant differences in the densities of
small rodents between the removal and control plots;
in fact, densities of small seed-eating rodents averaged
2.17 times as high on the control plots (Fig. 6). Beginning in mid-1978, however, numbers of small granivorous rodents increased on Dipodomys removal plots,
which from then on consistently maintained densities
that averaged 2.8-4.5 times as great as those on control
plots. During this period there was only one experimental plot in only one year (Plot 21 in 1980-1981)
October 1985
MANIPULATIONOF A DESERTRODENT COMMUNITY
that supported a lower density of small seed-eaters than
any control plot. For all of the small granivorous species
considered collectively, these results are highly significant (U = 0, P = .014). As shown in Table 3, none of
the small rodents responded to the treatments during
the 1st yr, but then four of the five small granivores
(but neither of the nongranivores) showed significant
increases in the absence of Dipodomys: Pg. flavus, R.
megalotis, P. maniculatus, and P. eremicus. Only Pg.
penicillatus showed no significant response, but this
species occurred at low densities and exhibited a very
patchy distribution among plots. We note parenthetically that P. eremicus, an excellent climber that sometimes scaled the "rodent-proof' fences, was also captured 2.7 times more frequently on the four plots from
which all rodents had been removed than on the four
control plots (U = 2.5, P = .08). The dramatic and
consistent increase of small seed-eating rodents in the
absence of Dipodomys supports the competition hypothesis.
Additional evidence in support of this hypothesis
and of the proposition that the competition is primarily
for food came from monitoring densities of small nongranivorous rodents. Two species of primarily insectivorous rodents, Onychomys leucogaster and 0. torridus, passed freely through the small holes in the fences
of the Dipodomys removal plots. Jointly the densities
of these insectivorous species were not significantly
different on experimental and control plots (densities
were 26% greater on control plots, but U = 5, P = .43),
and neither species showed any difference when considered individually (Table 3). Taken together, these
data suggest that rodent species that eat significant
numbers of seeds increase substantially in density when
granivorous Dipodomys species are removed, but insectivorous rodents are unaffected. These results not
only reinforce the conclusion that granivorous rodents
compete for a limited food supply, they also help rule
out alternative explanations, such as that the increase
in small rodents was attributable to reduced losses to
predators (e.g., snakes) that were differentially excluded
from experimental and control plots by the differentsized holes in the fences.
The data on individual life history attributes showed
no significant differences between Dipodomys removal
and control plots that might indicate the mechanism
of the response of small seed-eating rodents to missing
competitors. We emphasize, however, that the number
of replicates was small and that there was considerable
variation among experimental plots. We suspect that
the increased density of small granivorous rodents on
Dipodomys removal plots can be attributed largely to
immigration.
Effects of ants
In contrast to an earlier study at another site where
seed-eating rodents were shown to increase in density
when granivorous ants were removed (Brown and Da-
1555
vidson 1977, Brown et al. 1979b), we noted virtually
no significant response of rodents to removal of either
Pogonomyrmex rugosus alone or all species of granivorous ants. The only exception was a significantly greater increase (F = 8.25, P < .05) in the combined densities of the small seed-eating rodent species on plots
where both Dipodomys and Po. rugosus had been removed than on plots where only Dipodomys was absent; this result was obtained only for the 2nd yr of the
study (1978-1979), which was also the 1st yr of the
response of the small granivorous rodents (Fig. 6). Although we do not want to attach too much importance
to this result, it is possible that the small granivorous
rodents initially responded to a greater availability of
seeds on plots where both Dipodomys and Po. rugosus
had been eliminated, but, because the other ant species
subsequently increased to compensate for the missing
Po. rugosus, this response was ephemeral.
Compensation in energy consumption
Although experimental provision of additional seeds
and removal of certain rodent species resulted in increased abundance of certain rodent species, it is of
interest to ask to what extent these increases compensated for the changes in food resource availability. The
degree of compensation was estimated from data on
the usable energy content of supplemental seeds (11 637
kJ/kg for millet; from values in Altman and Ditman
1968) and from allometric equations relating the average daily energy requirements of a small mammal to
its body mass (see Methods: Measurement of Responses). Results of these calculations are shown in
Table 4. Compensation was surprisingly slight: virtually none for the added seed, only - 10% for removal
of the three Dipodomys species, and perhaps as much
as 34% for the removal of D. spectabilis. We emphasize, however, that statistical confidence cannot be
placed in the last figure, because the response of the
remaining rodents (primarily the increase of D. merriami and D. ordii) to removal of D. spectabilis was
not statistically significant. Therefore we conclude that
although adding seed or removing competing species
made additional food resources available to the remaining rodent species, only a small fraction of these
additional energy resources were actually converted
into rodent biomass. Although certain species clearly
profited from enhanced food availability and increased
in density, these changes were inadequate to account
for most of the millet seeds that we provided or the
natural seeds that were made available by removing
competing rodent species.
DISCUSSION
Our experiments provide three lines of evidence that
interspecific interactions are important in determining
desert rodent densities and community organization.
1) Small seed-eating rodents increased in density
when three species of kangaroo rat were removed.
JAMESH. BROWN AND JAMESC. MUNGER
1556
Ecology, Vol. 66, No. 5
3. Density response of small seed-eating and non-seed-eatingrodents in a 2 x 2 complete factorial experiment
involving removal of the three large granivorousDipodomysspecies, as well as the large harvesterant Pogonomyrmex
rugosusduring 1977-1982.
TABLE
Plots with Dipodomysremoved
Po. rugosuspresent
Plot 3
Year -
1
Po. rugosusabsent
Plot 19
1
2-5
2-5
Plot 21
Plot 15
1
2-5
1
2-5
Rodent density (mean no. capturesper plot per census period)
Small seedeaters
Pg. flavus
Pg. penicillatus
P. maniculatus
P. eremicus
R. megalotis
Total
0.25
0.08
0
0
0
0.33
0.78
0.04
0.02
0.13
0.57
1.54
0
0
0
0.08
0.08
0.16
0.27
0
0.40
0.32
0.67
1.66
0
0
0
0
0
0
0.79
0.37
0.19
0.33
0.20
1.88
0.17
0
0
0
0
0.17
0.80
0.07
0.07
0.04
0.29
1.27
0.50
0.08
0.58
0.24
0.20
0.44
0
0
0
0.11
0.02
0.13
0
0
0
0.42
0.09
0.51
0.92
0.33
1.25
0.32
0.11
0.43
Small non-seedeaters
0. torridus
0. leucogaster
Total
* Control.
t Resultsof Mann-WhitneyU tests comparingthe fourDipodomys-removalplots and the fourplots with Dipodomyspresent,
with respectto averagedensity for year 1 (July 1977 throughJune 1978), averagedensity for years 2-5 (July 1978 through
June 1982), or the changein averagedensity betweenyear 1 and years 2-5. NS: not significant(P > .05).
2) The two medium-sized species of kangaroo rat
showed reciprocal density shifts to changes (both induced and natural) in density of the larger kangaroo
rat, D. spectabilis.
3) Use of plots by nonresidents of the two mediumsized species of kangaroo rat (as measured by increased
trapping success when trapping with the gates open)
was higher on plots where densities of D. spectabilis
were high than on plots where densities were low, which
indicates that although the smaller congeners could
trespass and do some foraging on D. spectabilis home
ranges, they were strongly inhibited from establishing
residence there.
In addition, our experiments, as well as other observations, indicate that these interactions are due, at
least in part, to food limitation and competition for
this scarce resource. This evidence includes:
1) densities of species of small rodents that are not
highly granivorous did not respond to the removal of
Dipodomys species;
2) the direction of the reciprocal density shifts between D. spectabilis and the two medium-sized Dipodomys species was determined primarily by seed
availability: D. spectabilis increased on seed addition
plots, D. merriami and D. ordii increased on all other
plots;
3) use of plots by nonresidents was much higher on
seed addition plots than on other plots; and
4) densities of large-seeded winter annual plants have
increased as much as several thousand times in response to the removal of rodents, indicating that predation by these granivores substantially reduces the
standing crop of their food resources (Brown et al., in
press).
We measured several life history parameters in an
attempt to discern the demographic mechanism that
was responsible for the density changes caused by our
manipulations. D. merriami had a lower percentage of
residents on seed addition plots, corresponding to its
lower densities there. This may indicate that a reduction in successful immigration onto seed addition plots
or an increase in emigration from these plots may have
led to decreased densities there. D. spectabilis had a
higher average adult body mass on seed addition plots;
the demographic consequence of such a result is unknown. Our failure to find further differences in reproduction or residency that could account for the other
changes in density (such as the increased populations
of small seed-eaters in response to removal of Dipodomys) indicated that identifying the mechanisms that
lead to a change in abundance is likely to be more
difficult than simply documenting the shifts in density.
This may be because very small adjustments in rates
of reproduction, survival, immigration, and emigration can lead to rather large differences in standing
densities.
Although we have demonstrated food limitation and
interspecific competition, we still know very little about
how these processes operate to influence the abundance
of species and the organization of the community. For
example, we do not know to what extent species compete by interference and exploitation, exactly how resources are used differentially among species so that
stable coexistence is maintained, or what roles antipredator strategies, life history traits, foraging behaviors, seed storage, and hibernation play in the interactions among species. It is important to work out these
mechanisms, because in order to interpret our results
MANIPULATIONOF A DESERTRODENT COMMUNITY
October 1985
TABLE3.
1557
Continued.
Plots with Dipodomyspresent
Po. rugosus absent
Po. rugosus present*
Plot 11
1
Plot 14
2-5
1
Plot 12
1
2-5
Plot 8
1
2-5
Significancet
2-5
1
2-5
Change
0.014
Rodent density (mean no. capturesper plot per census period
0.08
0.13
0.08
0.06
0.08
0
0.42
0.26
NS
0.014
0.33
0.39
0
0.02
0.25
0.21
0
0.02
NS
NS
NS
0
0
0
0.41
0
0.02
0.14
0.68
0
0
0
0.08
0
0.06
0.06
0.20
0
0
0
0.33
0.02
0.08
0.24
0.55
0
0
0
0.42
0
0.02
0
0.30
NS
NS
NS
NS
0.022
0.057
0.029
0.014
0.022
0.057
0.029
0.014
0.08
0
0.08
0.45
0.22
0.67
0.08
0.08
0.06
0.13
0.32
0.45
0
0
0
0.24
0.05
0.29
0.25
0
0.25
0.07
0.42
0.49
NS
NS
NS
NS
NS
NS
NS
NS
NS
in a general conceptual framework it is necessary to
know to what extent the observed processes of population regulation, interspecific interaction, and community organization depend on specific features of the
biology of these particular rodent species, and to what
extent these patterns and processes occur in other systems. Certainly interspecific competition appears to be
an important phenomenon in other kinds of rodents
(Grant 1969, 1971, 1972, Redfield et al. 1977) and
other groups of terrestrial vertebrates (e.g., Hairston
1980, 1981, Pacala and Roughgarden 1982).
The responses of rodents to our manipulations, additional responses of ants, plants, birds, and other organisms to these and similar experiments in desert ecosystems (e.g., Brown and Davidson 1977, Brown et al.
1979a, b, Inouye et al. 1980, Inouye 1981), and the
results of other experimental manipulations of communities (e.g., in the intertidal zone: Connell 1961,
Dayton 1971, Paine 1974, Lubchenco and Menge 1978,
Sousa 1979, Menge and Lubchenco 1981) suggest that
natural communities are organized by a complex web
of interspecific interactions that cannot adequately be
described or predicted by current ecological theory.
The problems of interpreting the results of field experiments with respect to the specific predictions of
mathematical models are beyond the scope of this paper, but see Schaffer (1981) and Bender et al. (1984).
Here we simply note that although existing models of
population regulation and interaction provide a basis
for interpreting the simple qualitative trends that are
caused by our manipulations, these models do not prepare us for the surprising complexity of several responses (including small degrees of compensation,
asymmetries, and long time lags) revealed by the rodent
populations.
First, consider the extent of compensation. Although
TABLE 4.
Energeticcompensationby desert rodents to supplementalseeds and to removal of selected rodent species. (For
details of calculation,see Methods:Measurementof Responses.)Note that rodent compensationfor the additional food
energymade availablenever exceeded 34%.
Experimentaltreatment
Removal of all 3
Energymade available
(kJ/d)*
Energeticresponse
(kJ/d)t
Seed addition
Removal of D. spectabilis
Dipodomys species
3060
201.4
439.7
91
33.2
49.4
(by all 8 species of
(by 5 species of small
(by 7 species of smaller
granivorousrodents)
granivorousrodents)
granivorousrodents)
Percentcompensation:
33.8
9.5
2.9
* For seed additiontreatments,calculatedas the metabolizableenergyin the addedmillet. For othertreatments,determined
by calculatinghow much the removed individualswould have consumed, based on their total biomass.
t Determinedby calculatingthe consumptionof the indicatedgroups,based on their measuredincreasein total biomass.
t For the rodent removal experiments,percentcompensationwas calculatedas: [(1977-1978 energy consumption minus
1978-1982 energyconsumptionfor the averageof the removal plots) minus (1977-1978 energyconsumption minus 19781982 energyconsumptionfor the averageof the control plots)] divided by (metabolizableenergy of added seeds or energy
consumptionof the rodents removed).
1558
JAMESH. BROWN AND JAMESC. MUNGER
manipulations that supplied additional food or altered
the densities of particular rodent species resulted in
substantial changes in densities of certain species, the
magnitudes of the compensatory responses in terms of
energy consumption were very small. This suggests that
processes other than straightforward competition for
food among rodent species must also play important
roles in determining the structure and function of this
community. Possibilities include: (a) intraspecific competition and aggression; (b) competition with other seedeating organisms, such as birds and ants, that might
also compensate to unknown degrees for seeds made
available by the manipulations; and (c) predation or
foraging constraints that might make it unprofitable
for certain rodent species to collect particular kinds of
seeds or to forage in certain microhabitats. For example, the failure of small seedeaters to compensate
for missing Dipodomys might be due in part to increased susceptibility of the small granivores to predation if they were to increase foraging in the open
microhabitats favored by the missing kangaroo rats
(see Rosenzweig 1973, Brown 1975, Price 1978, Hay
and Fuller 1981, Thompson 1982a, Price and Brown
1983, Kotler 1984).
Evidence for asymmetrical competition comes especially from the dependence of the outcome of interactions among kangaroo rat species on levels of food
availability. Addition of seed did not result in an increase in the density of all granivorous rodent species,
or even in an increase in some species and no significant
change in others. Instead, regardless of the size of seed
particles added and the temporal pattern of seed addition, the manipulation favored the largest granivorous rodent species, D. spectabilis, at the expense of its
medium-sized congeners, D. merriami and D. ordii.
This is consistent with reports that D. spectabilis is
restricted to highly productive regions of deserts and
arid grasslands, whereas D. merriami and D. ordii have
wide distributions that include much less productive
habitats (Rosenzweig and Winakur 1969, Brown 1975,
Frye 1983). It is also consistent with evidence that D.
spectabilis is behaviorally dominant and aggressively
excludes small kangaroo rats (Frye 1983, M. A. Bowers
et al., personal observation). Although our experiments
provide no additional direct evidence on the mechanism, it seems reasonable that the asymmetry is due
in large part to the size difference between the kangaroo
rats. It is more likely that increased densities of D.
spectabilis (in response to increased seed availability)
caused the decrease in the densities of D. merriami and
D. ordii, than that the converse is true. Unfortunately,
because of the difficulty of designing fences that would
allow free access of D. spectabilis while excluding the
medium-sized kangaroo rats, it will be difficult to obtain direct experimental evidence to test this hypothesis.
Similarly complex patterns are apparent in the response of the small seed-eating rodents to our manip-
Ecology, Vol. 66, No. 5
ulations. These species showed no significant response
to either seed addition or D. spectabilis removal, but
they increased several-fold when all three Dipodomys
species were removed. This suggests that the kangaroo
rats, especially the medium-sized species D. merriami
and D. ordii, have a strong competitive effect on the
small granivorous rodents over a wide range of potential availability of seeds. On the other hand, had we
been able to perform the reciprocal experiment and
remove the small granivores, it is unlikely that we would
have been able to detect any competitive effect on Dipodomys. Such noncomplementary results can be expected whenever coexisting species differ greatly in individual body mass (which can result in asymmetrical
interactions based on aggression or differential foraging
efficiency), population density, or both (as in the present study). Such differences can greatly complicate the
interpretation of removal experiments to test for competition. For example, Abramsky and Sellah (1982)
removed the smaller of two granivorous rodent species
from a sand dune in Israel and found little evidence
for competition, but it is questionable whether the expected response would have been of a detectable magnitude, especially given the lack of replication and short
duration of their experiment.
In all of our experiments we observed time lags of
several months to a year before we noted any changes
in the rodent populations, and several years were required to obtain statistically significant results (see also
Hairston 1980). This observation also seems to have
important implications for other field experiments in
which supplemental food is provided or selected species
are removed. Clearly the absence of an immediate response cannot be taken to indicate the lack of food
limitation or competition. It is noteworthy, however,
that other experimental studies of desert rodents that
have failed to obtain any evidence of competition have
been conducted for less than a year (e.g., Schroeder and
Rosenzweig 1975, Abramsky and Sellah 1982). It remains unclear why we observed such long delayed responses to our manipulations. Production of desert
seed crops and rodent reproduction both occur in temporal pulses associated with favorable conditions (adequate precipitation). Because at least some species of
desert rodents (especially D. spectabilis) store seeds in
caches and disperse primarily as juveniles, it is perhaps
not surprising that availability of a new seed crop or
of dispersing young rodents may be required for local
populations to respond completely to altered conditions of food availability and density of competitors.
This does not necessarily mean that periods of significant competition are infrequent, as Wiens (1977) has
suggested. If this were the case, one would expect to
see significant differences in the rodent populations
among our experimental treatments only during such
rare instances. But we observed that once the rodents
had responded to the manipulations, the relative magnitudes of the differences in densities and biomass of
October 1985
MANIPULATIONOF A DESERTRODENT COMMUNITY
species between experimental and control plots remained surprisingly constant (e.g., Figs. 2 and 6).
Both the low degree of compensation and the long
time lags can probably be attributed at least in part to
two complicating factors that are common to many
communities: competitive interactions with distantly
related organisms, and indirect effects of granivores
mediated through their impact as predators on seedproducing plants. Preliminary results of ongoing experiments suggest that both are important in this system. Although much of the food made available by
adding exogenous seeds or removing competing rodent
species is not converted into rodent biomass, this seed
does not persist for long in the environment. Preliminary data suggest that at this study site as elsewhere
(e.g., Brown and Davidson 1977, Brown et al. 1979a,
b) granivorous birds and ants consume many of the
seeds that otherwise would be available to rodents.
Also, rodents (and probably the other granivores as
well) have significant long-term effects on the availability of different kinds of seeds because their selective
predation on certain seed species importantly influences the composition of the plant community (e.g.,
Inouye et al. 1980, Inouye 1981).
Another factor that may be extremely important in
this community is the impact of rodent predators. We
emphasize that although our experiments demonstrate
that limited food resources and interspecific competition play major roles in the organization of the rodent
community, this does not mean that predation is not
also important. Indeed, our study site supports many
predators (including coyotes, hawks, owls, and snakes),
and we have little evidence to suggest that rodents die
of starvation. We suspect that most individuals are
killed by predators (and we have witnessed a few incidents). Probably food supply, interspecific competition, and predation interact to limit rodent populations. Competition among species decreases an already
limited food supply and causes individual rodents to
spend more time foraging and to forage in more exposed microhabitats, thereby increasing their susceptibility and losses to predators. Other processes, such
as parasitism, may also be important, but these are
even less well understood (Munger et al. 1983).
Variation in the physical environment obviously also
plays a major role in regulating the population size and
determining the community structure of desert rodents. Although this has not been a focus of our experiments, the effects of climate are apparent in our
data. The substantial increase in the average densities
of both kangaroo rats and small granivorous rodents
in the winter of 1981-1982 (Fig. 6) appears to have
been a direct consequence of exceptionally heavy precipitation and high seed production in the preceding
months. These temporal fluctuations are consistent with
data showing correlations between precipitation, seed
production, and granivorous desert rodent population
density and species diversity over geographic gradients
1559
in southwestern North America (Brown 1975). This
provides an example of how physical and biotic factors
(climate and prey availability) can interact to limit population densities and affect community organization.
Experimental manipulations are very much in vogue
in contemporary ecology. Although we believe the
present study provides another example of the valuable
insights that can be obtained from replicated, controlled experiments conducted in the field, we caution
against the uncritical acceptance of experimental results as an accurate representation of the patterns and
processes that occur in unmanipulated systems. In this
regard, we mention several limitations of our procedures that should be considered before extrapolating
our results to make inferences about natural communities.
1) The spatial and temporal scales of our manipulations were arbitrarily limited. Our experimental plots
were tiny islands in a vast sea of unmanipulated desert.
Would we have observed the same kinds or magnitudes
of density changes if we had been able to treat much
larger areas, or do the responses we recorded simply
reflect the choice of small patches of favorable habitat
by individuals whose populations are regulated largely
by other processes operating on a much larger spatial
scale?
2) Although we tried to minimize or control for artifacts associated with the use of fences to limit immigration onto the plots, several possible effects remained. Perhaps the most serious was the differential
exclusion of rodent predators, especially large snakes,
which could pass through the large gates but not the
small ones. To some extent, monitoring populations
of non-seed-eating rodents, which presumably have the
same predators, is a control for this. This control would
be invalidated, however, if the non-seedeaters are not
susceptible to predators (as is perhaps suggested by the
clumsy locomotion and strong, unpleasant odor of the
two Onychomys species). Another problem is that the
rodents might ultimately be indirectly affected as a
consequence of the differential exclusion of other kinds
of organisms, such as insectivorous lizards. Also, to
the extent that aggressive interactions among rodents
are important, the fact that individuals must enter and
leave the plots through the gates may facilitate the
defense of space by dominant individuals and species.
3) The kind of seeds added and their method of
distribution may have influenced the response to these
manipulations. Most natural seeds are smaller and different in details of their packaging and chemical composition than the millet particles we added. In addition,
native seeds fall to the ground beneath the parent plant
and are disseminated gradually over a period of weeks,
and many become buried in the soil where they may
remain for many years (Tevis 1958). Although we cannot evaluate the effects of all of these factors, it is likely
that we are supplying exceptionally attractive and
available food particles. It seems likely that species
JAMESH. BROWN AND JAMESC. MUNGER
1560
(such as D. spectabilis) that can efficiently harvest seeds
and store them in large caches would benefit most from
our seed additions, but perhaps not so much from more
natural increases in native seed production.
We do not believe that these potential problems detract unduly from the importance of our experimental
results. Indeed, the creation of possible artifacts is the
price of human intervention in any natural system;
some form of this problem is common to all experiments.
In conclusion, we wish to emphasize not only how
much we have learned about the ecology of desert rodents from the present and previous studies, but also
how much still remains to be done. Desert rodents
probably have been studied more intensively by modern population and community ecologists than any other
group of terrestrial organisms. These studies have been
conducted by many independent scientists, who have
used sophisticated observational, experimental, and
statistical techniques to test current theories and investigate general questions. Although these studies generally agree in suggesting that food supply, interspecific
competition, predation, habitat structure, and climate
interact to regulate the abundance of particular species
and to influence the composition of rodent communities, they have produced few other satisfying generalizations. Instead, they have revealed tremendous
variation between sites as well as a wealth of complex
interactions within local communities that serve only
to underscore what challenging problems remain.
ACKNOWLEDGMENTS
This researchis part of a collaborative study supervised
jointly by D. W. Davidson and J. H. Brown and sponsored
by the National Science Foundation, most recently by Grant
BSR-8021535. So many people have contributed to the project that we hesitate to list them all for fear of forgetting someone. We hereby express our gratitude to all of these good
people, and we humbly acknowledge that if it were not for
the help of many of them, this research could never have been
done.
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1562
JAMES H. BROWN AND JAMES C. MUNGER
Ecology, Vol. 66, No. 5
APPENDIX
Summary of the most important results of seed addition and species removal experiments on desert rodents. For each
entry, top line gives mean values for plots subjected to the same treatment, and bottom line gives value of F or MannWhitney U, from a comparison of treatment means, followed by the probability level (underlining indicates P < .05).
Treatment:
Comparison:
Plots:
Dipodomys spectabilis
Change in density (mean
no. captures per plot
per period)
Change in energy consumption (kJ plot-'
d-1)
Adult body mass (g)
Percent reproductive
Residence time (mo)
Percent residents (% multiple captures)
Dipodomys merriami and
D. ordii
Change in density (mean
no. captures per plot
per period)
Change in energy consumption (kJ plot-.
d-l)
Adult body mass (D. merriami only; g)
Percent reproductive (D.
merriami only)
Residence time (D. merriami only; mo)
Percent residents (D. merriami only)
Small seedeaters
Change in density (mean
no. captures per plot
per period)
Change in energy consumption (kJ plot-I
d-1)
Onychomys species
Change in density (mean
no. captures per plot
per period)
Change in energy consumption (kJ plotd-l)
Adult body mass
(Onychomys leucogaster
only; g)
Percent reproductive (O.
leucogaster only)
Residence time (mo)
Percent residents
Seed addition
Seed size
Control
Added
Small
Mixed
11, 14
1, 2, 6,
9, 13, 18,
20, 22
2, 22
9, 20
-0.355
0.638
U= 1, P=.044
0.462
0.823
F= 0.344, P
Seed schedule
Large
Constant
Pulse
6, 13
2, 6, 9,
13, 20,
22
1, 18
0.871
.740
0.718
U=4,
0.396
P=.321
117.89
-76.83
U= 1, P=.044
142.63
81.91
F= 0.352, P
162.46
.729
129.00
U= 5,
84.54
P=.429
127.1
U=0,
43.8
U= 6,
5.67
U=4,
56.6
U= 7,
135.2
P=.022
44.8
P=.356
7.11
P=.200
57.1
P=.444
137.3
136.0
F = 0.692, P
38.6
32.0
P
F= 1.57,
7.24
6.40
F= 0.602, P
58.3
50.0
F= 0.387, P
130.1
.566
44.1
.341
6.43
.603
56.6
.709
134.5
U= 3,
38.2
U=0,
6.69
U=0,
54.9
U= 3,
137.3
P= .214
64.5
P=.036
8.36
P=.036
63.6
P= .214
0.113
U= 0,
-0.984
P=.022
-1.151
-0.854
F= 0.385, P
-0.683
.710
-0.896
U= 4,
-1.250
P= .321
15.75
U= 0,
-85.57
P=.022
-55.43
.611
-78.46
U= 5,
-106.89
P=.429
45.4
46.4
U= 3, P=.133
39.8
36.4
U= 6, P=.356
5.26
6.50
U= 4, P= .200
41.9
55.2
U= 0, P =.022
-104.39
-75.57
F= 0.584, P
44.5
46.5
F= 1.216, P=.410
40.0
35.1
39.0
F= 0.048, P=.953
6.47
5.73
4.21
P=.013
F=25.281,
41.7
44.1
37.3
F= 0.268, P=.782
45.4
U= 5,
38.0
U= 5,
5.47
U= 4,
41.2
U= 5,
45.5
P=.429
31.7
P=.429
4.63
P= .321
44.2
P=.429
0.022
U= 4,
0.231
P=.321
2.55
U= 4,
12.40
P=.321
45.2
0.193
U= 7,
0.074
P=.444
0.113
-0.218
0.170
F= 0.401, P =.701
8.39
U= 8,
5.01
P=.556
-7.91
0.446
U= 2,
0.123
P=.089
0.242
0.092
-0.186
F= 1.520, P=.350
31.25
U= 2,
9.53
P=.089
-9.18
17.65
6.58
F= 1.756, P= .313
23.07
5.02
U= 1, P=.071
36.2
U= 7,
36.6
P=.444
35.9
36.4
36.1
F= 0.173, P=.849
36.2
U= 4,
38.1
P= .321
40.5
U= 8,
4.80
U= 7,
29.2
U= 8,
37.3
P=.556
4.91
P=.556
29.8
P=.556
56.7
26.7
F= 0.710, P=.559
3.00
3.90
7.50
F= 2.021, P=.331
43.0
21.0
31.3
F= 0.219, P = .815
32.2
U= 4,
4.28
U= 2,
30.8
U= 5,
52.5
P=.321
6.50
P= .190
25.4
P=.429
13.2
7.47
8.10
F= 0.559, P=.622
0.345
0.049
U= 1, P=.071
APPENDIX.
1563
MANIPULATION OF A DESERT RODENT COMMUNITY
October 1985
Continued.
D. spectabilis
removal
Dipodomys spp.
removal
Po. rugosus
removal
Ant removal
Control
Removal
Control
Removal
Control
11, 14
5,24
8, 11,
12, 14
15, 19,
21
11, 14
Po. rugosus
removal
8, 12
Ant
removal
4, 17
Control
11, 14,
15, 21
Po. rugosus
removal
3,8,
12, 19
-0.233
-0.523
-0.355
F= 0.178, P = .845
-76.83
-37.09
-79.07
P=.845
F=0.172,
133.0
131.9
F= 2.389, P=.240
52.3
53.2
43.8
F= 0.151, P= .866
10.43
5.67
7.69
F= 1.966, P=.285
52.8
56.9
56.6
P=.936
F=0.067,
127.1
-0.278
1.300
0.113
P=.541
F=0.760,
1.174
F= 0.402,
1.806
P= .591
113.16
F= 0.224,
157.45
P= .683
-10.34
129.62
15.76
P=.530
F=0.790,
46.4
F= 0.014,
39.8
F= 0.393,
46.2
P= .916
44.1
P = .595
46.4
55.2
F=0.101,
52.1
P= .780
0.231
F = 0.984,
0.662
P = .426
0.198
U=0,
1.456
P=.014
-0.42
0.203
0.193
P=.682
F=0.435,
0.858
U=8,
0.796
P=.557
10.17
F= 0.769,
33.45
P= .473
8.71
U= 0,
54.21
P=.014
0.70
9.02
8.39
P=.667
F=0.446,
31.98
U= 8,
30.94
P=.557
0.077
F= 4.031,
-0.483
P= .183
0.312
U=3,
-0.143
P=.100
0.411
0.177
0.446
F= 2.846, P=.203
0.103
U= 7,
0.066
P= 0.443
5.89
F= 5.073,
-30.42
P=.153
21.98
U=3,
-8.50
P=.100
12.70
29.94
31.25
P=.149
F=3.834,
7.76
U=7,
5.71
P=.443
36.2
F= 12.066,
38.2
P=.074
37.0
U= 5,
33.9
P=.429
36.2
34.5
U= 6,
37.2
P=.571
40.5
F= 0.140,
4.80
F = 0.003,
29.2
F= 0.021,
30.0
P= .745
4.50
P = .959
32.1
P= .898
64.8
49.9
U= 4.5, P= .371
2.83
4.31
P=.500
U=4,
23.3
20.0
P=.443
U=7,
57.7
U=3,
3.40
U= 2,
28.0
U= 6,
54.4
P=.200
3.92
P=.267
15.4
P=.343
46.3
45.8
F= 0.062, P= .941
24.8
51.0
39.8
P=.0065
F=41.61,
6.39
6.97
6.50
F= 0.223, P=.812
66.7
56.9
55.2
P=.498
F=0.887,
35.8
37.8
P= .712
F=0.382,
32.1
59.4
P=.793
F=0.251,
3.33
2.62
4.80
P=.856
F=0.169,
10.7
56.4
29.2
F= 7.795, P=.065
40.5