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Comparative Population Ecology of Eleven Species of Rodents in the Chihuahuan Desert
Author(s): James H. Brown and Zongyong Zeng
Source: Ecology, Vol. 70, No. 5 (Oct., 1989), pp. 1507-1525
Published by: Ecological Society of America
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Ecology, 70(5), 1989, pp. 1507-1525
© 1989 by the Ecological Society of America
COMPARATIVE POPULATION ECOLOGY OF ELEVEN SPECIES
OF RODENTS IN THE CHIHUAHUAN
DESERT1
JAMES H. BROWN
Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131 USA
AND
ZONGYONG ZENG
Department of Biology, University of Sichuan, Chengdu, Sichuan, China
Abstract. Comparisons of mark-recapture data on life histories and population dynamics of the 1 1 commonest species of nocturnal desert rodents inhabiting our experimental
study site in the Chihuahuan Desert of extreme southeastern Arizona permitted assessment
of the role of evolutionary relationships and ecological factors in the coexistence of these
species. The species varied greatly in population density, extent of interannual variation
in abundance, timing of reproduction, extent to which reproduction was seasonal, rate of
disappearance of marked individuals, frequency and distance of lifetime dispersal movements, but perhaps less so in death rate and maximum longevity.
Most of the species showed positively correlated year-to-year fluctuations in population
density, suggesting that they responded similarly to interannual variation in precipitation,
primary production, and availability of food resources. In contrast, there were both positive
and negative correlations in seasonal patterns of reproductive activity and population
density. Lifetime dispersal movements were inversely related to body size, suggesting that
energy constraints cause the smallest species to move among rich patches in a coarsegrained manner. Patterns of similarities and differences among closely related (congeneric
and confamilial) species suggested that evolutionary constraints sometimes, but not always,
limited variation in life history and demography. The relationship between population
ecology and competition among these species was not clear.
We interpret the diversity of life histories and population dynamics in these coexisting
species to be a consequence of: (a) a productive and spatially and temporally variable
environment that provides a variety of resources that may be used in different ways, (b)
historical biogeographic events that have made available a large regional pool of species
from which potential colonists can be drawn, and (c) differences in population ecologies
among the species that evolved primarily in other environmental contexts, but that permit
coexistence by enabling the species to use different resources or to use the same resources
in different ways.
Key words: community;demography;desert;dispersal;evolutionaryconstraint;field study; life
history;populationdynamics;reproduction;rodent;southwesternNorthAmerica;survival.
INTRODUCTION
Communities are assemblages of species, and the
composition and dynamics of communities reflect the
structure and dynamics of the species populations. The
population ecologies of the component species are just
as relevant to understanding community organization
as are the patterns of resource utilization and the dynamics of interspecific interactions. Yet rarely have the
population ecologies of the species that coexist to form
a sizeable guild or community been compared.
Such comparisons should be of particular interest
because the population structures and dynamics of coexisting species, like their patterns of resource utilization, should reflect a compromise between opposing
forces. On the one hand, the species will tend to be
1
Manuscript received 3 April 1988; revised and accepted
25 September 1988.
similar because they inhabit a common environment.
Such similarities may represent both adaptations to
similar conditions and colonization of local areas by
species that already possessed similar tolerances and
requirements. Also, to the extent that communities
contain closely related species, similarities among them
may reflect evolutionary constraints owing to common
ancestry. On the other hand, species will tend to differ
because they interact with the same local environment
in different ways. These differences may reflect the resolution of interspecific interactions among the species
that permit or promote coexistence. Also, to the extent
that communities contain distantly related species, differences among them may reflect evolutionary constraints owing to divergent ancestry.
Although the rodents of the desert regions of southwestern North America have been the subject of many
studies of interspecific interactions and community or-
JAMESH. BROWN AND ZONGYONG ZENG
1508
ganization (e.g., Brown 1987, Brown and Harney, in
press), surprisingly little is known about the basic population biology of many species. Especially lacking are
long-term and comparative studies to provide data on
the population dynamics and life histories that enable
diverse species to persist and coexist in highly variable
desert environments. Here we present eight years of
data comparing the population ecology of the 11 species
of common heteromyid and murid (cricetid) rodents
that coexist on - 20 ha of Chihuahuan Desert in southeastern Arizona. On the one hand, all of these species
must cope with the same climate, soil, vegetation, and
predators. On the other hand, the species differ markedly in several respects: in taxonomic affinity, with
representatives of two families and seven genera; in
morphology, which varies from bipedal kangaroo rats
to quadrupedal mouselike forms; in body size, which
ranges from 7 to 175 g; in diet, which includes granivory, folivory, carnivory, and omnivory; and in many
other features of their biology.
METHODS
The study was conducted on the Cave Creek Bajada,
6.5 km east and 2 km north of Portal, Cochise County,
Arizona, at an elevation of 1330 m. We present data
collected from November 1977 to June 1985, a period
of 7 yr and 8 mo. We did not include either 4 mo of
preliminary data collected from July to October 1977
or data obtained after June 1985, although the study
is continuing.
The data were collected as part of a mark-recapture
study designed primarily to measure the response of
rodent populations to experimental removal of granivorous rodent and ant species and to addition of
supplemental seeds. The study site, experimental design, layout of the experimental plots, trapping regime,
and analytical methods are described in detail in previous papers (Brown and Munger 1985, Zeng and Brown
1987a, b), so they will be treated only briefly here. The
habitat is transitional between arid grassland and upper
elevation Chihuahuan Desert shrubland. The terrain
is relatively flat except where it is dissected by several
temporary watercourses. The 20-ha study site has been
fenced since 1977 to exclude livestock.
Rodents were censused on 24 experimental plots,
each 0.25 ha in area (see aerial photograph in Brown
and Munger 1985). All plots were fenced so as to render
them potentially rodent-proof, but 16 equally spaced
holes (gates) of varying sizes cut in the fences allowed
access of selected rodent species to appropriate plots.
The largest sized gates allowed free access of all rodent
species to 16 plots (8 seed-addition, 2 ant-removal, 2
Pogonomyrmex rugosus [a large harvester ant]-removal, and 2 unmanipulated control), medium-sized gates
excluded the large kangaroo rat, Dipodomys spectabilis,
from 2 plots, small gates excluded three kangaroo rat
(Dipodomys) species from 4 plots (2 of which also had
P. rugosus removed), and no gates at all excluded vir-
Ecology, Vol. 70, No. 5
tually all rodents from 4 plots (2 of which also had ants
removed).
Rodents were captured during a monthly live-trapping program that was used to monitor responses of
all rodent species to the experimental manipulations.
Each plot was trapped for a single night during a twoor three-night trapping period timed to correspond as
much as possible to the new moon. On the night of
trapping, the gates in the fences were closed so as to
catch only those individuals resident on that particular
plot. Forty-nine Sherman live traps (23 x 8 x 9 cm)
baited with millet or mixed birdseed were set at permanent grid stakes spaced at 6.5-m intervals. The
monthly trapping was sometimes interrupted by skipping a period in winter. Approximately once each year
we trapped with the gates open to capture both residents and those individuals that foraged on the plots
but had their home burrows outside.
Each individual was marked when first captured with
a numbered monel fingerling tag attached to an ear,
except for the three smallest species (Chaetodipus penicillatus, Perognathus flavus, and Reithrodontomys
megalotis) which were marked by toe-clipping. At each
capture, identification number, body mass, hind foot
length, and standardized data on reproductive condition (for males: testes abdominal or scrotal; for females:
vagina swollen or plugged, pregnant, and/or lactating)
were recorded for each individual.
The experimental design introduces some complications that affect the analysis and the comparison of
the results with other studies using unfenced, unmanipulated trapping grids. The use of fenced plots with
gates was quite effective in restricting captures to individuals resident on the plots. Only very infrequently
was the same individual caught on two different plots
on successive nights. Occasional trapping with the gates
open (reported in Brown and Munger 1985) showed
the extent to which individuals occupying burrows outside the fences moved onto the plots at night to forage.
Because of the exclusion experiments, different species
had free access to different numbers of plots: D. spectabilis to 14, D. ordii and D. merriami to 16, and the
other eight species to 20. Biomass was calculated using
only data for the unmanipulated control plots. Population densities were calculated as the number of individuals captured on a plot in a trapping period divided by the area of the plot (0.25 ha), and the resulting
values were then averaged over all trapping periods
when the gates in the fences were closed. Population
densities were determined both for all of the plots to
which each species had free access and for only the two
unmanipulated control plots. Although individuals
captured on plots designated for removal of that species
were not used to calculate population density, all other data collected from those animals were used in the
analyses. N. albigula, Pm. eremicus, and R. megalotis
are excellent climbers; these species quite frequently
immigrated onto exclusion plots despite monthly trap-
October 1989
DESERTRODENT POPULATIONECOLOGY
ping and removal. To maximize the continuity and
reliability of the life-history data, marked individuals
captured on plots designated for exclusion of that species
were removed from the plot but released elsewhere on
the study site.
NATURAL HISTORY OF THE SPECIES
The 11 species considered in this paper differ greatly
in taxonomic affinity and natural history. They represent seven genera and two families: Heteromyidae:
Dipodomys spectabilis, D. ordii, D. merriami, Chaetodipus penicillatus, and Perognathus flavus; and Muridae: Neotoma albigula, Onychomys leucogaster, 0.
torridus, Peromyscus eremicus, Peromyscus maniculatus, and Reithrodontomys megalotis.
The heteromyids are endemic to arid and tropical
regions in southern and western North America and
northernmost South America. The three genera represented here are widespread in the southwestern deserts and possess several characteristics that have been
interpreted as adaptations for arid environments. These
include external cheek pouches used to collect and
transport the seeds that comprise the majority of their
diets, and kidneys capable of concentrating urine so
that most species can subsist without drinking water
on a diet consisting solely of dry seeds. In addition,
the kangaroo rats, genus Dipodomys, have inflated
tympanic bullae and bipedal, saltatorial locomotion,
characteristics that have been interpreted as facilitating
the detection and avoidance of predators in open desert
habitats. Pocket mice, genera Chaetodipus and Perognathus, do not possess such extreme morphological
and locomotor specializations, and this has been related to observations that they usually do more foraging under and up in vegetation than do kangaroo rats.
Unlike the kangaroo rats, which are active all year,
most pocket mice hibernate for several weeks or months.
All heteromyids are nocturnal and spend the day in
burrows. As indicated in Table 1, body size of the
desert heteromyids varies by more than an order of
magnitude, from 7 g in Pg. flavus to 123 g in D. spectabilis.
Although the heteromyids are usually considered to
be the most specialized North American desert rodents, the study site is not unusual in being inhabited
by even more species of murids. The family Muridae
is a very large, diverse group of rodents with a worldwide distribution. The species here are members of the
subfamily Cricetinae whose center of distribution, diversity, and abundance is North and South America.
Although these mice are relatively unspecialized morphologically compared to the heteromyids, they are
more diverse behaviorally and ecologically. The wood
rats, Neotoma, are primarily folivorous and build large
dens of sticks and debris. The grasshopper mice,
Onychomys, are carnivores that feed on a variety of
invertebrates and small vertebrates. The harvest mice,
Reithrodontomys, like the heteromyids, feed largely on
1509
seeds. The deer mice, Peromyscus,
are the least spe-
cialized and are highly omnivorous and opportunistic,
although seeds comprise a substantial fraction of their
diet. These murids are nocturnal and active throughout
the year, although harvest mice and deer mice can
utilize torpor to avoid short periods of severe weather
or food shortage. The murids also span a wide range
of body sizes, from 10 g in R. megalotis to 175 g in N.
albigula.
In evaluating the variety and specializations of these
rodents it should be mentioned that the study site is
typical of the habitats of the three genera and all five
of the species of heteromyids. In contrast, although
some murid species such as N. albigula, 0. torridus,
and Pm. eremicus are confined to desert environments,
others are much less restricted. The most extreme case
is Pm. maniculatus, the most widely distributed small
mammal in North America, which inhabits alpine tundra, coniferous and deciduous forest, and grasslands
as well as deserts.
RESULTS
The data base
Our analyses are based on 9090 captures of 3039
individuals of 11 species (Table 1). Not included in the
analyses are six additional species (Chaetodipus hispidus, Sigmodon hispidus, Reithrodontomysflavescens,
Ammospermophilus harrisi, Spermophilus spilosoma,
and Thomomys bottae) that were present but captured
too infrequently (<50 times) to provide reliable data
(Brown 1984, Brown and Munger 1985).
Also in Brown and Munger (1985) but not in the
present paper are analyses of the responses of individual rodent species to the experimental manipulations.
Addition of seeds and exclusion of other rodent species
had substantial effects on the population densities of
certain species. Table 1 presents data for standing-stock
population densities of each species averaged for all
14-20 plots to which it had access and for only the two
unmanipulated control plots. Brown and Munger (1985)
compared several life history parameters between experimentally manipulated and control plots, and found
virtually no significant differences. This suggests that
those species that responded to the experimental perturbations did so primarily by adjustments in population density, while other aspects of their population
ecologies remained characteristic of the site as a whole.
Population density and dynamics
We determined the mean population density of each
species by direct enumeration, based on the average
number of individuals caught in each 0.25-ha plot for
all trapping periods when the gates in the fences were
closed. More than 80% of the individuals of most species
known to be alive were captured each month. Since
there is considerable movement, even of adults, across
and beyond the study area (Zeng and Brown 1987a, b;
JAMESH. BROWN AND ZONGYONG ZENG
1510
Ecology, Vol. 70, No. 5
1. Data on the size and composition of the populationsof 11 species of desert rodents inhabitingthe experimental
study site near Portal,Arizona.
TABLE
Species
Dipodomys
spectabilis
Dipodomys ordii
Dipodomys
merriami
Chaetodipus
penicillatus
Perognathus
flavus
Reithrodontomys
megalotis
Peromyscus
Number of
Number of captures
Numindividuals
Popu- Coeff. of
ber of Sex ratiot Body Biolation variation
FeFemass mass density§
juve- (male:
Male male Total Male male Total niles female)
yr
(g) (g ha- ) (no./ha) mo
1019 921 1940 273 239
130
1.11:1* 123.4 504.8
512
5.30 0.25 0.31
389
384
773
135
145
280
33
1847
1642
3489
511
457
968
156
59
121
180
37
52
89
20
Total
64.9
505.1
9.0
(0.71:1)
272
184
456
118
96
214
2
221
177
398
88
92
180
7
89
52
141
36
38
74
9
maniculatus
Peromyscus
eremicus
Onychomys
leucogaster
Onychomys
torridus
Neotoma albigula
(1.14:1)
1.01:1
48.1
(0.93:1)
1.12:1*** 42.8
(1.12:1)
0.49:1*** 16.0
150
106
256
59
49
108
23
249
245
494
87
81
168
44
265
254
519
129
120
249
55
189
255
444
90
107
197
73
3039
562
9090
1.48:1***
(1.23:1)
1.25:1*
(0.96:1)
1.71:1t
(0.95:1)
1.42:1**
(1.20:1)
1.02:1
(1.07:1)
1.04:1
(1.08:1)
0.74:1t
(0.84:1)
7.0
3.9
10.2
5.7
21.4
4.1
21.2
5.5
34.7
64.5
24.6
28.0
174.7
235.8
1431.1
(4.09)
1.82
(1.35)
7.93
(11.81)
0.39
(0.56)
0.93
(0.56)
0.65
(0.56)
0.28
(0.19)
0.43
(0.26)
0.89
(1.86)
0.97
(1.14)
0.95
(1.35)
23.73
(20.54)
0.36
0.60
0.13
0.31
0.85
0.26
0.31
0.73
0.74
0.93
0.38
1.16
0.23
0.76
0.39
0.26
0.35
0.20
0.46
0.36
t Two values are given for sex ratio: above, based on number of captures;below, in parentheses,based on number of
individuals. Statistical significance of departure from 1:1 ratio: * P < .05, ** P < .01, t P < .005, *** P < .001.
§ Two valuesaregiven forpopulationdensity: above, meanforall plotsto whichthe specieshadaccess;below,in parentheses,
mean for the two control plots.
see also Dispersal, below), many of those individuals
not captured but known to be alive could have been
residing temporarily outside the fenced plots. Our
method of counting captures within fenced plots avoids
the problem that unfenced grids sample an unknown
area larger than that covered by the traps. We believe
our estimates of density are far more accurate than
those calculated from mark-recapture data using assumption-laden, indirect methods (e.g., see Seber 1986).
Table 1 shows total number of captures, estimated
population densities, and standing-stock biomass for
the 1 1 species. Combined density of all species totaled
23.73 individuals/ha (20.54 individuals/ha for the unmanipulated control plots). Including the captures of
the six additional species present on the study site would
only increase this figure to 21 individuals/ha for the
control plots. Rodent biomass totaled - 1.43 kg/ha. As
is typical for most communities, the contributions of
different species to these totals were highly uneven.
Population densities ranged from <0.56 individual/ha
in C. penicillatus, Pg.flavus, R. megalotis, Pm. maniculatus, and Pm. eremicus, which made up collectively
only 6.7% of the total, to 11.81 individuals/ha in D.
merriami, which accounted for 50% of the total. Biomass ranged from < 10 g/ha in each of the same five
rare species to >500 g/ha for D. spectabilis and D.
merriami. Although the number of species in the two
families were similar, the heteromyids dominated the
community, accounting for 77.5% of the population
density and 76% of the biomass, and the kangaroo rat
genus Dipodomys alone accounted for 73% of the population density and 75% of the total rodent biomass.
The population densities of the species fluctuated
substantially over the study period (Fig. 1). The combined densities of all species attained their highest levels
in 1982 and 1983 and their lowest levels during 1979
and 1984. Most of the species showed generally similar
trends, except for the two Onychomys species, which
did not exhibit significantly lower numbers in 1979
and 1984 than in most other years. Of the 11 species,
only D. merriami and D. spectabilis were captured in
every monthly trapping period. Because the wide fluctuations included zero density for most species, the
coefficient of variation provides perhaps the best measure of relative differences among them. We have calculated this statistic for two different time intervals,
months and years, which give somewhat different results (Table 1). On a month-to-month time scale, D.
merriami exhibits by far the least severe fluctuations,
followed by Pm. eremicus and D. spectabilis. At the
other extreme, C. penicillatus showed the most variation, followed by R. megalotis and N. albigula. The
apparently higher densities of the two Onychomys
species in the winter, compared to the summer, months
October 1989
DESERT RODENT POPULATION ECOLOGY
A--
1511
D. merriami
+-+-+ D. ordii
15 -
*-.
D. spectabilis
*--
C penicillatus
10
5
0
--
6
0
Pg. flavus
5
-c
._
c,n
0
4
3
"0
2
C)
0
A
-= In
II I I I I I I I 1 11
z
LUJ
T
I
I
I
I
I
**
R. megalotis
A-A
N. albigula
I
I
I
I
I
1
11
1
1
1
1
1
i
1
II Ii II i
i li
II
I
Iii I
1
I
I
I
1
iI ii I
I.
I
I
I
I
111
1
z
0
I-
_J
:D
O_
0
0-
* * Pm. maniculatus
3
a-nA
Pm. eremicus
--
0. leucoguster
2
0
O
3r
A-nLO
1978
torridus
1979
1980
1981
1982
1983
1984
1985
DATE
FIG. 1. Fluctuations in population density in the 11 species of rodents inhabiting the Chihuahuan Desert study site. Note
that Perognathus flavus was locally extinct for the last 18 mo of the study, whereas the two species of Peromyscus did not
attain significant densities on the study site for the first 4 yr of the study.
Ecology,Vol. 70, No. 5
JAMESH. BROWN AND ZONGYONG ZENG
1512
C
-,
X
a
D merriami
A
C penicillatus
\
1
Pm eremicus
/o
+ R megalotis
/
+
flus
pg Afl
-c0
8
8-
0. leucogaster
# 0 torridus
20- -
i
--
0
0
4
J'
F
MAMJ
J
/ASON5
J
FMAMJ
JASOND
MONTH
MONTH
FIG.2. Seasonalpatternsof variationin populationdensity of the 11 speciesof desertrodents.Valuesplottedare the mean
densities for each species for each month averagedover the durationof the study (1977-1985). Note that differentspecies
reachpeak densities at differenttimes of year.
might in part reflect increased trapability during cold
seasons when insect prey are less available, but the
increases in late summer and fall probably also reflect
recruitment from breeding in spring and summer. Much
of the month-to-month variation in density of C. penicillatus can be attributed to the fact that this pocket
mouse hibernates. When assessed on a year-to-year
scale, this species and the two Onychomys exhibited
the least fluctuations, and Pm. maniculatus, R. megalotis, Pm. eremicus, and Pg. flavus showed the greatest
fluctuations.
The general patterns of year-to-year fluctuations in
the different species can be characterized as follows.
All three species of kangaroo rats were reliably present,
but showed substantial variation and attained high
densities in 1982 and 1983. In addition, D. ordii showed
a clear trend of increasing density throughout the eight
years of the study. C. penicillatus was consistently present at low density every summer and absent (in hibernation) each winter. Pg. flavus increased to a peak
of 3-6 animals/ha in 1982-1983 and then almost disappeared for the last two years of the study (and remained virtually absent from the study area until the
summer of 1988). R. megalotis and the two Peromyscus
species showed similar patterns; they were almost absent from the area during the first four years (except
for a modest number of R. megalotis in late 1979),
attained substantial numbers in 1982-1983, and then
declined to low densities. The two Onychomys species
showed substantial month-to-month variation within
years, but maintained very constant populations from
year-to-year. N. albigula attained its highest densities
in the summers of 1982-1984.
The coefficient of variation in population density by
years (Table 1) provides a good measure of interannual
fluctuations. O. torridus, 0. leucogaster, C. penicillatus,
D. merriami, and D. spectabilis maintained the most
constant populations over the seven years of the study,
whereas Pm. maniculatus, R. megalotis, Pm. eremicus,
and Pg. flavus showed the greatest year-to-year variation.
The species differed in the extent to which they
showed annual population cycles and also in the time
of year at which peak densities were attained. Inspection of Fig. 2 suggests that those species (C. penicillatus,
Pg. flavus, and Pm. maniculatus) that had the lowest
average densities also showed the least seasonal fluctuation. This is misleading, however, and the coefficients of variation by month (Table 1) provide a much
more accurate estimate of the magnitude of annual
cycles. These show that C. penicillatus and R. megalotis
had the greatest variation, whereas D. merriami, D.
spectabilis, and Pm. eremicus had the least. The season
of maximum population size varied from winter for
D. merriami, D. ordii, R. megalotis, and 0. leucogaster,
to spring for D. spectabilis and Pg. flavus, to summer
for C. penicillatus and N. albigula (Fig. 2).
Reproduction
The species differed markedly in seasonality of reproduction, as indicated by the months when individuals were in reproductive condition and when juveniles
were recruited into the population (Fig. 3). In all species
a larger proportion of males than of females were in
reproductive condition in any one month. This is not
surprising since "reproductively active" males were
potentially capable of breeding, whereas reproductively active females were actually breeding. We used Shannon's diversity index, H/Hmax where H = -2 piln p,
and pi is the proportion of females in reproductive
DESERTRODENT POPULATIONECOLOGY
October 1989
D spectabilis
100 -
100 - *-_
+0
- +-
1513
Pm maniculatus
+
+
0
D ordii
,
100-
Pm. eremicus
100 -
+
_
I-+ I +I I
+, i
I
I
+
I
I
I
I
I
00
D. merriami
100 -
Z
LLJ
100 --
+
+
O-++
+
+
100 -
+
C. penicillatus
0--
0
0
0. leucogaster
-(3
1
1
1
1
1
1
1
1
1
1
1al
0 torridus
I
100-
Pg flavus
100 -
0+
0-+---+I
100 -
!+--- I +----+
I
I
-+I
I
+
I
+
I
I
+
I
|
N. albigula
R megalotis
++
O- M-+
t+-+ M
J F M A M J J A
+
100 -
--- ++D
S
0J
d
O N D
I
I
I
I
F M A M
I
I
J
I
3d A S
I
I
0 N DD
MONTH
FIG.3. Percentof males (0) and females (0) in reproductivecondition and the percentof individualscapturedthat were
juveniles (+). Note that for each speciesthe appearanceof juveniles usuallyclosely followedthe peak of reproductiveactivity,
especially in females, and that the appearanceof juveniles correspondswell with the seasonal peak in population density
shown in Fig. 2.
condition in the ith month, to compare species with
respect to the evenness of the proportion of females in
reproductive condition from month-to-month over the
annual cycle (Table 2). The three Dipodomys species
and the two Onychomys species had the highest values,
indicating the least seasonal reproduction. The kangaroo rats in particular were very aseasonal breeders:
in D. merriami both sexes were reproductively active
and juveniles were recruited in every month (see also
Zeng and Brown 1987a); in D. spectabilis some females
apparently had three widely spaced litters in favorable
years (see also Jones 1984, 1986). By contrast, Pm.
maniculatus, C. penicillatus, N. albigula, and R. megalotis showed the most seasonal reproductive patterns;
in particular, breeding of C. penicillatus, an apparently
obligate hibernator, was confined to a few months in
spring and early summer. In general, maximum appearance of new juveniles followed peak reproductive
activity of females with a lag of 1-2 mo, and this timing
of recruitment corresponded well with the season when
the highest population densities were attained (compare Figs. 2 and 3).
There was also substantial variation in the extent of
reproductive activity in different years. We assessed
this by calculating the coefficient of variation among
years in the percentage of females in reproductive condition for the seven complete years of the study. Table
2 shows that Pm. eremicus, D. merriami, D. ordii, and
C. penicillatus showed relatively little year-to-year
variation, whereas R. megalotis, Pg. flavus, and Pm.
maniculatus showed the greatest variation in reproductive activity.
Sex ratios
Sex ratios (males: females) varied from female-biased
in C. penicillatus (0.49:1) and N. albigula (0.74:1) to
male-biased in Pm. maniculatus (1.71:1) and Pg. flavus
(1.48:1) (Table 1). These ratios were calculated on the
1514
JAMESH. BROWN AND ZONGYONG ZENG
2. Year-to-yearand month-to-monthvariationin the
proportionof females of the 11 rodent species in reproductive condition. Note that low values of the coefficient
of variation indicate low interannualvariation, whereas
high values of evenness indicate low seasonal variationin
reproductiveactivity.
TABLE
Evennessof
the proportion
Coefficient of females
of variation each month
in the
showing
proportionof reproductive
females each
activity
Species
Dipodomysspectabilis
Dipodomysordii
Dipodomysmerriami
Chaetodipuspenicillatus
Perognathusflavus
Reithrodontomysmegalotis
Peromyscusmaniculatus
Peromyscuseremicus
Onychomysleucogaster
Onychomystorridus
Neotoma albigula
year showing
(H/Hma,,
0.63
2.97
0.31
0.58
0.64
0.52
3.44
3.60
3.53
3.15
reproductive where H=
-I pilnpi)
activity
0.53
3.72
0.44
3.62
0.35
4.03
0.48
2.89
0.70
3.42
0.71
3.29
basis of number of captures; sex ratios calculated on
the basis of number of individuals showed qualitatively
similar, but less extreme, deviations from 1.0:1 for
most species (Table 1). This wide range suggests potentially interesting differences among the species in
sex-specific mortality, dispersal, and home range size,
and/or in social structure and breeding systems.
Dispersal
We used the frequency distributions of the distances
between captures of the same individual to assess shortterm and lifetime movements in these rodents. Figs. 4
and 5 show the data, respectively, for distances between
successive captures 1 mo apart and distances between
first and last capture for those individuals that lived
>4 mo. Nearly all of these distributions show a concentration of values at distances of <50 m and a tail
of values out to much greater distances. Naturally, the
lifetime data show a greater frequency of long-distance
movements (Table 3).
These raw data underrepresent the frequency of longdistance dispersal because, with increasing distance
from each capture site, a smaller proportion of the area
into which individuals could potentially move is actually sampled by traps. We have developed a method
to correct for this bias and accurately estimate the real
frequency distribution of dispersal movements (Zeng
and Brown 1987b). We applied this method and calculated the median lifetime dispersal distance for each
species (Table 3). These values range from lows of 32,
53, and 70 m in D. spectabilis, D. ordii, and D. merriami, respectively, to highs of 286 and 202 m in R.
Ecology,Vol. 70, No. 5
megalotis and Pg. flavus, respectively. These results
indicate a high frequency of long-distance movements
by adults of all species except D. spectabilis.
Another indication of the importance of adult dispersal is the large percentage of individuals that were
first captured as adults (>74% in all species except N.
albigula; Table 3). This indicates that the majority of
individuals were not recruited into the adult population on the same plot where they were born and weaned,
but instead dispersed to their present home range as
an adult. Note that this does not imply any differential
movement onto or off the experimental plots in response to differences in recruitment or survival. In fact,
Brown and Munger (1985) found virtually no consistent differences in reproduction or persistence among
experimental treatments. It is just the case that if there
is a great deal of movement by individuals of all ages,
most of the recruitment will consist of immigrating
adults, most of the disappearances will be emigrating
adults, and at any given time most of the individuals
will be residing at some distance from where they were
born.
Mortality
Mortality of individuals was assessed in two ways.
One was simply to calculate the time between first and
last capture for each marked individual. By combining
data for all individuals of each species we obtained a
persistence curve that is similar to a survivorship curve
with two important exceptions. First, persistence is
measured from first capture, which usually occurred as
an adult (Table 3), rather than from birth. For most
species we had too few juveniles to measure survival
as a function of age, but newly caught juveniles had a
probability of being recaptured in the next trapping
period that was slightly lower than or indistinguishable
from first-captured adults (e.g., see Zeng and Brown
1987a). Second, the disappearances of marked individuals included those that had dispersed into areas
not sampled by traps as well as those that had died.
Bearing these caveats in mind, the persistence curves
were nearly linear when the proportion of individuals
recaptured was plotted on a logarithmic scale, suggesting that each species had approximately a constant
probability of disappearing per unit time (Fig. 6). The
slopes of these persistence curves varied among species
by a factor of >2, from -0.055 and -0.060 in C.
penicillatus and D. spectabilis, respectively, to -0. 134,
-0.130, and -0.129 in R. megalotis, Pm. eremicus,
and Pm. maniculatus, respectively (Table 4). These
correspond to disappearance rates that varied from
0.699 to 0.885 yr-' (Table 4). These slopes were estimated only for the first 10 mo following initial capture,
because only small numbers of individuals of some
species persisted for longer periods, making calculations over a longer period inaccurate. For the same
reason, the data on maximum survivorship of marked
individuals (Table 4), which exhibited great variation,
......
October 1989
DESERT RODENT POPULATION ECOLOGY
-
400
D spectabilis
n =972
320 -
1515
Pm maniculatus
n =37
10 -
8-
240 160 -
80 0
- .
. .
o
.
.
,
.
.
.
,
0
n)
o
0
L
C\J
0
0
cc-j
0
00O000
O D (M- 000J
r )r rro r
100 -
D. ordii
80 -
n =273
10 -
40 -
8-
20 -
6-
0
4O
0o
0
o
UL
0o
n
o0
o0
LO
0
0°
O0
0
LO
U3
60 -
d
.i.
.
o
O
In
0
0O
0
.
0
0
o0
.,,
Lo
cN
^~~~~~~~-
400
:~-
*~D
2-
merriami
=1504
~~~~~n
0o
cJ
r
o
Pm. eremicus
n =71
WI
.
500
0o
in
0
0
0
0
-
-
...
0
0o
cj
cJ
0
0
r0
L 300
T 200
-- 100
30 -
0
24 -
<
0
L
LL.
0
0_
0
Lu
0
rt
m
2
0
u~
r_
-
0
0o
\j
0
c
20-
000
or
) re)
C penicillatus
n =47
16 -
0. leucogaster
n =140
18 12 -
66-J
J
0
12-
0
Ln
0
o
o
i
-
s8 4
.
'
o
o
LU
o
o
o
i
0
in
n.
n.
o0
0
rN)
Pg flavus
n =119
3224 16 -
20 -
o
in
o
o
cM
r)
0. torridus
n =128
16 128-
4-L
. . . . . . . . . . . . . . . . ., . . .
0
o
8-
0
i>
o
0
in
0
0
0
0
0
in
0
n\j
in
N
20-
0
n
0
o0
--
0
l
-
-
0
0Oc0\j
-.oC\J
Frequency distributions for the
11
o
-
o
cCJ
. . . . . . .
o
in
(cM
o
o
rN
N albigula
n= 140
50 40 30 20 10 -
.
0
o
-
CD" CO
rN cr
12 -
84-
o
o0-
C3D o
R megalotis
n =92
16-
FIG.4.
cM
.
'
o
o
40 -
0
o
o
0
in)
c
0000
fOrn;-
0
0
iO
0
0o
0
-0
0
0
in
c\j
cN
0
o
DISTANCE (m)
rodent species of the distance between successive captures of the same individuals
in successive trappingperiods 1 mo apart.Although these are raw data, not adjustedfor the distributionof traps, note the
high frequencyof relativelyshort-distancemovements and comparewith lifetime movements in Fig. 5.
should be interpreted with caution. We suspect that
some individuals of all species may live 3-5 yr in the
field.
The other way we assessed mortality was by using
the estimated dispersal distances to correct the disappearances for the proportion of individuals that dispersed into areas not sampled by traps (see Dispersal,
above, and Zeng and Brown 1987b). This can be done
only for a species population as a whole, because the
fates of individuals that have disappeared cannot be
determined. It is also subject to error unless the numbers of individuals are large and the dispersal distances
are modest with respect to the size of the study area.
For these reasons we have separated the disappearance
1516
JAMES H. BROWN AND ZONGYONG ZENG
60 -
4
D. spectabiiis
n= 162
45 -
Ecology, Vol. 70, No. 5
Pm. maniculatus
n =5
3
30
2
15
0
I
I
J I .
0
I&
L I..
...
0
iI,.
.
0
to
mmmm.
~
.
.
(
J
0
i)
0
\J -C J
C--
LO
0
m
I J &
I,
0
0
J J7 I i
0
0
.1 .& . &
0
L5
r)
0
r')
iiii
.
L_J I ,i I
0
0
0
I 1. J
0
LO
0
0
. .
.
0
LO
I-
I
..
. .
, . ...
0
o
Cj
..
..
0
0
0
tn
C\
rf)
.............. 4
0
LO
re)
0
0
<
D. ordii
n =78
20
15
4-
Pm. eremicus
n 18
10
3
5
0
0o
O
It i
*C*:ii
0
0
0
,--,o..II
i
U merriam
n =306
80
I
o0
0o
.,.
l
I
,,..
0
0
,n
o
1 1'.1
0
,n
0
o
1.
0
0
to
0
,n
o
60
CO
_J
:D
0
0
lr-
40
10 -
20
0. leucogaste .r
n254
0
0
z
o0
Ln
©.
-LL
0
10
0
L.
-
0
ca
0
0
0
0
Ln
0
LO
rn
rN-
c\a
001
B5-
C. penicillatus
n =21
~~~-
cr
LJ
1-
:7
:D
0
5
0O
O
t
0O
0
0O
u)
0
0M
0
CM
Ct
o
0
I~(
Lo
rI'
o
o
O
7Z
0
i
I
o
0
0
0
o
..
0
Lto
.
..
0
0
CM
I
I
0
L
C\
.
0
0
r(
10-
0
0
1-
0
Lto
rtO
Pg flovus
=46
07~n
~1
10
0. torridus
n =44
5
5-
0
0__iL
o
o
L
LO
IiI
r0
> o
L0
o
C-
4
0
o0
L
- rC
'ih,.vML
0
0
to
0
o0
0
to
0
-0o
0
to
I
Or)
0
,
o
CM
LO
CM
Lo
o r
o
r
0
'I
))
cD
-
0
LO
t
R. megalotis
n =35
3
2
I
m
N. albigula
I0
n =28
5
...
0
\CM
0
0
ro
... I I__i__..~_J
to
r
0
I
0
0
n
DISTANCE
0
0
OO
( m)
0
0
0
-
-
CM
0
O
CM
0
0
ro
0o
ro
0
0
^-r
DESERTRODENT POPULATIONECOLOGY
October 1989
1517
TABLE3. Data on month-to-monthand lifetime movements of individualsof the 11 species of rodents.
Percent
first
Percent first
captured
Species
Dipodomvsspectabilis
Dipodomvs ordii
Dipodomvs merriami
Chaetodipuspenicillatus
as adult
74.6
X
X no.
recaptures
X distance between
recaptures (m)
per individual 1 mo apart
21
3.79
Median lifetime dispersal
distance (m)
Lifetime
36
Observed
20
Calculated*
32
88.2
83.9
2.76
3.60
24
24
51
52
25
26
53
70
77.5
2.02
33
77
30
150
202
40
87
37
99.1
2.13
Perognathusflavus
95
286
164
2.21
87
96.1
Reithrodontomys megalotis
75
116
91
65
74.3
1.91
Peromvscus maniculatus
110
117
148
2.37
76
78.7
Peromvscus eremicus
72
133
71
91
2.94
73.8
Onvchomys leucogaster
73
132
95
70
77.9
2.08
Onvchomvs torridus
109
23
23
63
2.25
62.9
Neotoma albigula
* This is the best estimate of distances moved over a lifetime. See Zeng and Brown (1987b) for method of calculation and
other details.
rate into dispersal and death rates only for the three
Dipodomys
species (Table 5). Note that
70-75%
of
the individuals of each species disappeared each year,
and about half of these disappearances can be attributed to dispersal off the trapping grids and the other
half to mortality. Dispersal appears to be less pronounced in D. spectabilis, which inhabits large permanent mounds that may be occupied by parents and
offspring for many generations (Jones 1984, 1986).
Although we did not feel that we could accurately
calculate death rates for the other species by this method, we note that most of them had substantially longer
dispersal distances than the three kangaroo rat species
(Table 3). Therefore we would expect a larger proportion of the disappearances to be due to dispersal rather
than to mortality. Thus the steeper slopes of the persistence curves for these species, especially the murids
and Pg. flavus (Fig. 6), may not mean that these species
necessarily have higher mortality than the kangaroo
rats. This is reinforced by the fact that maximum longevities of N. albigula, R. megalotis, and 0. torridus
were comparable to those of the three Dipodomys
species (Table 4).
DISCUSSION
Trade-offs
Most life history theory assumes a trade-offbetween
reproductive investment and survivorship. We tested
whether there was a significant cost of reproduction
that was expressed in terms of reduced survivorship
of those individuals that had made a reproductive commitment compared to those that had not engaged in
reproductive activity. For each species we compiled a
FIG. 5.
2 x 2 contingency table comparing whether those individuals that were reproductively active or inactive
were either recaptured or had disappeared. None of
these tables showed significant nonrandomness (all Ps
> . 1), except for Pm. maniculatus (. 1 > P > .05), which
showed a greater tendency for those individuals that
had not reproduced to disappear. Since one result significant at the <.1 level is expected in the 11 tests, we
can attribute this result to chance. It is also consistent
with the interpretation made below (see Dispersal) that
individuals facultatively move to better sites as they
become available.
We emphasize that this should not be construed as
a strong test for postulated trade-offs between present
reproduction and survival to future reproduction. A
rigorous test for such a trade-off would hold all variables except magnitude of reproductive commitment
constant: year, season, age, sex, body size, and so on.
However, we do not have sufficient data for even the
most abundant species (see also Zeng and Brown 1987a)
to perform such an analysis. Also, it would be important to ensure that those individuals that disappeared
had died rather than dispersed. We believe that two
important lessons can be drawn from these results.
First, it may not be easy to document postulated tradeoffs between reproduction and survival at the level of
individuals within populations. Although selection
causing life history evolution is presumed to operate
at this level, most of the "tests" of life history theory
have involved comparisons between different populations or different species (e.g., Stearns 1976, 1977).
Second, our data do imply that if there is a significant
cost of reproduction, those individuals that make reproductive efforts do so at times when the environment
Frequency distributions for the 11 rodent species of lifetime movements (distance between first and last capture)
of all individualsthat were capturedat least 4 mo apart.Althoughthese raw data have not been adjustedfor the decreasing
number of traps at increasing distances from the initial capture site, compare with Fig. 4 and note the substantial proportion
of individuals that moved > 150 m.
JAMES H. BROWN AND ZONGYONG ZENG
1518
Ecology, Vol. 70, No. 5
05
0201 005
-
002
-
001
0.005
.
0002
0001
C
0.5,
--
R. megalotis
-o-o
Pm maniculatus
+-+-+ Pm. eremicus
)>-
z
Ln
D
:_
LL
0.2
0.1
005
002
001
LU'
_J 0005
cr
0002
0001
28
32
36
-.-
o-o
05
40
44
48
O0leucogaster
0. torridus
+-+-+ N. albigula
02
0.1
005
002001
\
-.
.
....
0.005- \-
++
0002 0.001-1
I I
,,,,,,,,,,,
0
I
4
8
I
12
I I I
16
I I I I
II
20
24
I
I I II
I II
28
32
I I II
36
I
I I
40
I
44
I, I
48
NO. MONTHS
FIG.6. Disappearance curves for the 1 rodent species. The proportion of individuals recaptured is plotted (on a logarithmic
scale on the ordinate) as a function of the number of months since first capture (on the abcissa). These are analogous to
survivorship curves, except that dispersal as well as death may account for the disappearance of individuals. Note that the
small murid species (middle panel) had higher rates of disappearance than the heteromyids (upper panel) or large murids
(lower panel), but these small murids also tended to disperse longer distances (see Table 3).
DESERTRODENT POPULATIONECOLOGY
October 1989
TABLE4.
1519
Longevityand rates of disappearanceof the 11 species of desert rodents.
Species
Maximum
longevity
(mo)
50
35
Dipodomys spectabilis
Dipodomys ordii
Dipodomys merriami
Chaetodipus penicillatus
Perognathus flavus
Reithrodontomys megalotis
Peromyscus maniculatus
Peromyscus eremicus
Onychomys leucogaster
Onychomys torridus
Neotoma albigula
43
25
35
40
19
19
24
35
45
Coefficientof
variation
Slope of persistence Disappearance of disappearancerate
rate (yr-1)
curve from 0 to 10 mo
year-to-year
0.70
0.18
-0.060
0.13
0.75
-0.085
0.09
0.72
-0.070
0.12
0.79
-0.055
0.12
0.77
-0.099
0.07
0.89
-0.134
0.10
0.86
-0.129
0.09
0.85
-0.130
0.24
0.79
-0.082
0.16
0.83
-0.101
0.18
0.76
-0.097
is sufficiently favorable and their own condition is sufficiently good so that risks of mortality are minimized.
This is the standard explanation for the highly seasonal
reproduction often exhibited by rodents in other environments.
We also tested for a relationship between present
nutritional status of individuals and their probability
of survival. We reasoned that we might expect individuals that had been losing body mass (excluding
pregnant females that gave birth) to suffer higher mortality than those that had been gaining mass, in part
because they might spend more time foraging and experience more intense predation. We tested for this
using 2 x 2 contingency tables for each species to compare whether individuals that either gained or lost mass
between two successive trapping periods either were
recaptured or disappeared. All of these tests were indistinguishable from random (all Ps > .2), except for
C. penicillatus in which individuals that gained mass
showed a greater tendency to disappear (.1 < P < .05).
This pattern might be expected for a hiberator such
as C. penicillatus, but if so it implies substantial mortality or dispersal associated with hibernation. Since
one such result would be expected by chance in 11
tests, we are reluctant to attach any significance to it.
We find the apparent lack of relationships between
change in mass and disappearance to be interesting,
since it suggests that a recent history of mass loss does
not necessarily imply that a particular individual is any
less fit than members of the population as a whole.
Although we did not present data on changes in body
mass in the populations of these 11 species (but see
Zeng and Brown 1987a), there were tendencies for individuals to gain and lose mass in synchrony, apparently in response to temporarily favorable and unfavorable environments. The analyses suggest that such
periods of mass change were not strongly associated
with altered risk of mortality. They further imply that
if predation is a major cause of mortality, either the
rodents do not respond to temporary energy deficits
by increasing the amount of time spent foraging, or
during periods of food stress foraging time can be increased without increasing the risk of predation, perhaps because other rodents behave similarly and the
risk is shared by the population as a whole.
Dispersal
One of the striking features of our results is the high
frequency and long distance of adult dispersal in all
species (Fig. 5, Table 3). More than 50% of the individuals that lived at least 4 mo moved >30 m from
the site of their initial capture, and since the experimental plots measured 50 x 50 m, this means that
most of them had dispersed to a new plot. These observations contrast with much of the traditional dogma
regarding dispersal in small mammals. Dispersal has
been viewed primarily as a phenomenon of newly
weaned, recently independent juveniles or of competitively inferior adults in poor condition (e.g., Lidicker
1975, Shields 1982, Waser 1985). Movements of young
Disappearanceratebrokendown into its componentdeathrateand dispersalratefor the threekangaroorat species.
The method of Zeng and Brown (1987b) was used to estimate the proportionof those individuals that disappearedeach
year that had dispersedinto areas not sampled by traps, and the remainderwere assumed to have died. Coefficientsof
variationfor death rate and dispersalrate from year-to-yearare also given.
TABLE 5.
X disappearance X dispersal
X death
Coefficientof variation
Death rate
Dispersalrate
Species
rate (yr-1)
rate (yr-1)
rate (yr-1)
Dipodomys spectabilis
Dipodomys ordii
Dipodomys merriami
0.70
0.74
0.72
0.39
0.39
0.37
0.31
0.56
0.43
0.35
0.46
0.43
0.35
0.35
0.35
JAMESH. BROWN AND ZONGYONG ZENG
1520
Ecology, Vol. 70, No. 5
g make the shortest lifetime movements, and both
smaller and larger rodents disperse substantially farther. Although the linear relationship between disz 200
Pg9 f
Pm. m.
Ipersal distance and body mass is marginally significant
or)
0·C 0 0
_ -- .
(r = -0.54; .1 < P < .05), the linear fit becomes highly
Op t.
J
a
N.
significant if both variables are log-transformed and
< 100
Pm. e
cr)
the value for N. albigula, the largest species, is omitted
012
L!
D.m.®0
(r = -0.93; P < .01). The best fit to the entire data
c) 60
D D.o
set is given by a parabola in whose equation both the
Do
z
mass term and the square of mass contribute highly
< 40
D.s.
significantly (both Ps < .01) to accounting for the ob6
10
20
100
40
60
200 served variation in lifetime dispersal distance.
BODY MASS (g)
Interestingly, Brown and Maurer (1987) have presuch a curvilinear relationship between individdicted
FIG. 7. Median lifetime dispersal distance as a function
of body mass plotted on logarithmicaxes. The dispersaldis- ual movements and body mass in endothermic vertancehas been adjustedfor the probabilityof re(captureowing tebrates based on the relationship between population
to the placement of traps (see the last columr of Table 3)
size and body size in birds. The fact that no species of
Note that an inverse relationshipbetween disp)ersaldistance
such high local population
and body size appearsto characterizeall but the 1argstTeciese. very small birds attained
densities as species in the size range of 50-150 g suggested that intense energy requirements constrain the
individuals have been interpreted as an aLdaptationto smallest endotherms to move between the richest
avoid competition with parents or siblings at their natal patches of habitat, using them in a coarse-grained fashsite or to prevent deleterious inbreeding. Dispersal of ion. These data on desert rodents support this interadults has usually been considered to bee infrequent, pretation. The three kangaroo rat species that move
presumably because of the disadvantages of leaving a the shortest distances also have higher population denfamiliar site and an established territory or home range. sities (Table 1) and tend to use the environment in a
Although these traditional ideas ma,y accurately more fine-grained way in the sense that they have been
characterize some dispersal, especially thie sex-biased captured in a larger proportion of experimental plots,
movements of immature individuals ofce' rtain species, trap sites, and trapping periods (Brown and Kurzius,
in press) than the smaller heteromyids and murids. The
we doubt that they apply to most of the movements
we have observed in these desert rodent populations.
fact that individuals of the small granivorous species
Instead we suspect that individuals ofbotl h sexes, once (Pg. flavus, C. penicillatus, R. megalotis, Pm. manicuthey have become independent, move qu ite readily to latus, and Pm. eremicus) travel distances of more than
enhance their fitness. They are familiar with a large 100 m to utilize sequentially different plots from which
area surrounding the heavily used core region of their kangaroo rats have been experimentally removed (see
home range. When better food, den site s, or mating Brown and Munger 1985) further supports the interopportunities become available because ()f changes in pretation that increasingly severe energy constraints
cause the smallest rodents to use multiple, widely
the availability of resources, the death o)r movement
of a previous resident, or the ability to disi place another spaced, exceptionally rich patches over their lifetimes.
individual from a superior site, individua ils opportunInterspecific variation
istically shift the center of their activitie s to take adThese data provide an almost unique opportunity
vantage of these changes. This view of disp)ersalis much
more consistent with the distance and frequency of to compare the population ecologies in a diverse asmovements we have documented and wi th the obser- semblage of coexisting species of varying biological
vation that these shifts are often made b)y apparently similarity and taxonomic affinity. To what extent are
the life histories and population dynamics of these
robust, healthy, and sometimes breedinlg individuals
of both sexes. Other recent studies of srrlall mammal
species similar because of the constraints of an identical
environment and close taxonomic relatedness, and to
populations have also begun to question tthe traditional
dogma about dispersal and to advance interpretations what extent are they different because of interspecific
similar to ours (e.g., Waser and Jones 19)83, Lidicker competition, resource allocation, and distant relatedness?
1985, Waser 1985, Gaines and Johnson 1987).
The relationship between body size aLnd dispersal
We applied time series analysis to the data on popdistance (Fig. 7) is of particular interes;t, because it ulation densities to calculate cross correlation coeffiseems to challenge traditional thinking ;about the al- cients (r; for zero lag time, which is equal to the Pearson
lometric scaling of home range size andl movements
product-moment correlation coefficient) between each
(e.g., McNab 1963, Schoener 1968, Peters 1983, Calder pair of species for: (a) year-to-year variation in density,
1984). Our data suggest that the relatioriship is nonusing the average density of each species in each year;
linear: species with body sizes in the range of 40-140
and (b) seasonal variation in density, using the average
E
R. m
300
Li
)-
) -
October 1989
DESERTRODENT POPULATIONECOLOGY
1521
Significantcross correlations(0 time lag) in populationdensity between pairs of species from year to year (N = 9
yr). Data are broken down by rodent family; pairs of species are indicated by the first letters of the generic and specific
names (see Table 1). Note that all correlationsare positive.
TABLE 6.
Heteromyid/heteromyid
D.. -D.o.
0.73
0.70
D.o.-C.p.
D.s.-P.f
0.68
Murid/murid
P.e.-R.m.
0.87
P.m.-R.m.
0.83
P.m.-P.e.
0.68
density of each species for each month as plotted in
Fig. 2. To increase the power of these analyses we used
a more complete data set that included nine full years
of censuses (1977-1986). In each analysis, the number
of pairwise interspecific comparisons was 55, but the
sample sizes were modest (N = 9 yr and N = 12 mo,
respectively) so high values of the correlation coefficients are required for statistical significance.
For the year-to-year variation, all eight of the significant cross correlation coefficients were positive (Table 6). We call attention to three interesting results of
this analysis. First, the facts that all significant correlations were positive, that these involved 8 of the 11
species, and that these 8 are the largely granivorous
species suggest that the species with the most similar
resource requirements responded similarly to interannual variation in their common environment. A good
year for one species was good for most of the others.
This is consistent with the fact that the seeds consumed
by all these species are produced sporadically in desert
environments in response to precipitation sufficient to
wet the soil and result in significant primary production
(e.g., Went 1949, Tevis 1958, Beatley 1969, 1974, 1976,
Brown et al. 1979). Second, the lack of any strong
negative relationships suggests that the interannual
fluctuations in density cannot be attributed to strong
competitive exclusion and/or resource division on a
temporal basis (but see Hallett 1982). Third, some of
the species that showed very similar year-to-year fluctuations in abundance were closely related (e.g., congeneric D. ordii and D. merriami, r = 0.73), but others
were in completely different families (e.g., D. ordii and
P. maniculatus, r = 0.70). This suggests that interannual fluctuations in population density are more strongly
affected by convergent similarities in diet than by phylogenetically conservative aspects of history and demography.
The patterns of seasonal fluctuations in density were
much more variable. Out of 55 comparisons, there
were almost equal numbers of each sign, 9 significantly
positive and 7 significantly negative (Table 7). We call
attention to three aspects of these results. First, there
is no best time of year for reproduction and recruitment
of all species. This is reinforced by Figs. 2 and 3, which
show that peaks of reproductive activity and population sizes can occur at any time from midwinter to
midsummer depending on the species. A wide variety
of reproductive patterns appears to be capable of main-
Heteromyid/murid
0.70
D.o.-P.m.
D.o.-R.m.
0.67
taining rodent populations in this environment. Second, closely related species showed both some of the
most similar seasonal patterns (e.g., D. ordii and D.
merriami, r = 0.81; and 0. leucogaster and 0. torridus,
r = 0.70) and some of the most different patterns (e.g.,
D. spectabilis and D. merriami, r = -0.49; and R.
megalotis and N. albigula, r= -0.90). Distantly related
species exhibited both seasonally synchronous (e.g., D.
merriami and 0. leucogaster, r = 0.90) and asynchronous (e.g., C. penicillatus and 0. leucogaster, r = -0.87)
patterns of seasonal population fluctuation. Clearly,
closely related species are neither evolutionarily constrained to respond to seasonal environmental variation in similar ways, nor do they necessarily exhibit
marked differences associated with competition and/
or resource allocation. Third, there are no obvious relationships between the seasonality of recruitment and
any aspect of the biology of these 11 species, including
body size, morphology, physiology, diet, geographic
distribution, and taxonomy. The analysis suggests that
there may be processes that promote both similarities
and differences in life histories and population dynamics among the coexisting species in this assemblage, but
they do not act in such a way that we can predict a
priori which species will occur in the habitat, what
characteristics of population ecology they will possess,
and how the resulting community will be organized.
This wide variation and lack of clear patterns seem
to hold for most aspects of population ecology. Thus,
the heteromyids include the most and least seasonal
breeders (C. penicillatus and D. merriami, respectively)
and the highest and lowest sex ratios (Pg. flavus and
C. penicillatus, respectively), the murids include the
most and least variable populations from year-to-year
(Pm. maniculatus and 0. torridus, respectively), and
dispersal appears to be influenced by body size, but
relatively unaffected by taxonomy, mode of locomotion, diet, or other aspects of population ecology. Although the literature might suggest that the heteromyids have more "K-selected" and the murids more
"r-selected" life histories (e.g., Whitford 1976, Conley
et al. 1977), a critical examination of our data provides
little support for this generalization. Slopes of the disappearance curves would suggest such a trend (Fig 6),
but the facts that many of the disappearances probably
represent dispersal rather than death and that the maximum longevities are comparable (Table 4) suggest that
these may be misleading. Although we have not mea-
JAMESH. BROWN AND ZONGYONG ZENG
1522
Ecology, Vol. 70, No. 5
TABLE 7.
Significantcross correlations(0 time lag) in averagepopulationdensity between pairs of species from month to
month (N = 12 mo). Data are broken down by sign of correlationand by rodent family; pairs of species are indicatedby
the firstletters of the genericand specificnames (see Table 1).
Heteromyid/heteromyid
D.o.-D.m.
D.o.-C.p.
D.m.-C.p.
0.81
-0.88
-0.78
Murid/murid
Positive
O.l.-O.t.
0.70
P.e.-R.m.
0.69
Negative
R.m.-N.a.
-0.90
sured litter sizes, the data in the literature suggest that
they are very similar, averaging 2.0-4.3 in these species
of murids (Hoffmeister 1986) and 2.0-4.7 in the heteromyids (Hoffmeister 1986, Jones, in press). The apparent ability of some of the murids, such as Peromyscus and Reithrodontomys, to produce litters more
rapidly may be compensated for by the ability of the
heteromyids to reproduce under more adverse conditions (see Whitford 1976).
Taken together, the data on comparative population
ecologies of these 11 species suggest great interspecific
variation. In fact, the data presented here probably
seriously underestimate the total variation among all
the rodent species that coexist in this Chihuahuan Desert habitat. Not included in this study, because of small
sample sizes, are ground squirrels (Ammospermophilus
harrisi and Spermophilus spilosoma, family Sciuridae),
pocket gophers (Thomomys bottae, family Geomyidae), and cotton rats (Sigmodon hispidus, family Muridae), each of which may have characteristics of life
history and population dynamics as different from the
species we have studied as the latter are from each
other.
Population ecology and community structure
The desert rodent community at our study site was
comprised of at least 11 reasonably common and 6
rarer species, but this is an overgeneralization. Community composition varied temporally, both seasonally and from year-to-year, as species increased and
decreased in different patterns. Some of the more common species disappeared completely for substantial periods. Thus, C. penicillatus entered hibernation and
dropped out of the active community each winter, and
Pg. flavus hibernated some winters but remained active
and even reproduced during others. Pg. flavus, Pm.
maniculatus, Pm. eremicus, and R. megalotis were
completely or virtually absent from the study site for
years at a time, yet when they were present they reproduced, successfully recruited juveniles, and were
among the most abundant species. This temporal vari-
Heteromyid/murid
D.m.-O.l.
D.o.-O.l.
P.f-P.m.
C.p.-N.a.
D.m.-O.t.
D.o.-R.m.
C.p.-O.l.
C.p.-R.m.
C.p.-P.e.
D.o.-N.a.
0.90
0.86
0.78
0.72
0.70
0.69
-0.87
-0.78
-0.66
-0.59
ation in community composition is analyzed in more
detail elsewhere (Brown and Kurzius, in press). Here
it is sufficient to emphasize that the "community" was
very dynamic, varying even in its species composition
as some species colonized or went locally extinct in
response to the factors affecting their local population
dynamics.
How should the variation in population ecology
among species be interpreted, and what is its relationship to coexistence of species in this diverse assemblage? We consider three possibilities: coevolution, interactive sorting, and individualistic assembly. There
is no reason to think that any of the patterns represent
the results of coevolution of particular pairs or larger
sets of species to reduce overlap in use of limiting
resources and thus to facilitate coexistence. For one
thing, the modest intraspecific variation in the population ecologies of these species does not appear to be
related to occurrence with certain other species. Although population densities vary considerably among
habitats (e.g., Brown and Kurzius 1987), all features
of life history and demography of the populations inhabiting our study site apparently fall within the range
of variation reported for these species at other sites
(e.g., Reynolds 1958, 1960, Egoscue 1960, Eisenberg
1963, Chew and Butterworth 1964, MacMillen 1964,
French et al. 1967, 1968, 1974, 1975, Bradley and
Mauer 1971, Kenagy 1973, Maza et al. 1973, O'Farrell
1974, Smith and Jorgensen 1975, Whitford 1976, Conley et al. 1977, Wagner 1981, Petryszyn 1982, Munger
et al. 1983, Jones 1985, in press, Kenagy and Bartholomew 1985, Hoffmeister 1986). Furthermore, there is
so much variation in the combinations of species that
occur together at different times or in different places
(Brown and Kurzius 1987, in press), that it is difficult
to imagine that coevolution could be sufficiently fine
tuned to cause adaptations in one species in response
to coexistence with another (Schroder 1987, but see
Schroder and Rosenzweig 1975).
It is much more likely that the variety of population
ecologies represented by these species are the outcome
October 1989
DESERTRODENT POPULATIONECOLOGY
of some kind of sorting for compatibility (what Janzen
[1985] calls "ecological fitting"). There is abundant
evidence that interspecific competition plays a significant role in the structure and dynamics of desert rodent assemblages, including this one (e.g., Munger and
Brown 1981, Brown and Munger 1985, Brown et al.
1986, Bowers et al. 1987). Additional evidence shows
that species of desert rodents that differ in body size,
morphology, and taxonomic affinity are more likely to
coexist in local assemblages than species that are similar in these attributes (Bowers and Brown 1982, Brown
1987, Hopf and Brown 1986, Brown and Harney, in
press). Since differences in life histories and population
dynamics are likely to be correlated with differences in
resource use (the cause/effect relationship can go both
ways), it might be conjectured that the variation in
population ecologies reflects differences in resource use
that promote or at least permit coexistence. Unfortunately this is a very difficult proposition to test. Not
enough is known about the life histories and demographies of all those species that might be considered
to constitute the pool of potential colonists from which
local communities are assembled. This makes it impossible to build and test null models. The lack of clear
patterns, especially among the congeneric species, suggests that community organization in desert rodents is
less apparent in the population ecologies of the coexisting species than it is in their body size, morphology,
and taxonomy.
A third possibility is that the observed variation reflects the relatively independent assembly of species.
Since this particular assemblage of 11 species (like any
other combination) occurs infrequently in the North
American deserts (Brown and Kurzius 1987), it can be
assumed that the unique combination of traits possessed by each species evolved in response to physical
and biotic environments somewhat different from those
at our study site. But the life history and demographic
attributes of each species enable them to exist and coexist in this local environment. This interpretation does
not exclude the possibility that interspecific interactions play a major role in determining the relative
abundances, microspatial distributions, or even presence or absence of certain species with particular combinations of traits (see also Schroder 1987). However,
it suggests that potentially competing species are features of the local environment that are not necessarily
any more important in determining which life histories
and demographies will permit existence of each species
in that environment than are other features such as
physical conditions, predators, and food resources.
Our own opinion is that the population ecologies of
these 11 species reflect some combination of interactive sorting and independent assembly of species that
have evolved their attributes primarily in other contexts. Some of the similarities and differences among
species reflect evolutionary constraints of close and
distant phylogenetic relationships, respectively. Other
1523
similarities reflect the environmental constraints of the
spatial and temporal variation in limiting factors at
this locality, whereas other differences reflect adaptations, even in closely related species, to different environmental conditions in other parts of their present
or past range. We suspect that at least some of the
differences in life histories and population dynamics
promote coexistence in the sense that they enable the
species to use different resources or to use the same
resources in different ways. Together with the high productivity and the large spatial and temporal variation
that make a variety of resources available in this habitat and the historical biogeographic events that have
produced a large regional pool of species potentially
able to colonize the habitat (Findley 1969), these interrelated differences in population ecology and resource utilization probably account for the large number of rodent species that coexist at this site.
ACKNOWLEDGMENTS
This manuscript benefitted from the helpful comments of
G. Ceballos, L. Hawkins, E. Heske, A. Kodric-Brown, M.
Skupski, and two anonymous reviewers. We are indebted to
the people, too numerous to list individually, who have contributed to setting up and maintaining the experiments, trapping the rodents, and maintaining and analyzing the data.
From the beginning this research has been supported by the
U.S. National Science Foundation, most recently by Grant
BSR-8506729 to J. H. Brown. A foreign study award from
the People's Republic of China made possible the collaboration of Z. Zeng.
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