Download microhabitat use of deer mice: effects of

MICROHABITAT USE OF DEER MICE: EFFECTS OF INTERSPECIFIC
INTERACTION RISKS
JILL
C.
FALKENBERG AND JENNIFER
A.
CLARKE
Department of Biological Sciences, University of Northern Colorado, Greeley, CO 80631
Microhabitat use by deer mice (Peromyscus maniculatus) was tested under five different
simulated moonlight intensities, using an indoor habitat chamber with shrub covered areas
and open areas, and food sources. Tests were run in the presence and absence of a potential
competitor, Ord's kangaroo rat (Dipodomys ordii). From tracks in the sand, we determined
that, when alone, deer mice decreased total activity as moonlight increased and were more
active in areas with cover than in open areas. However, deer mice did not vary proportions
of activity allocated to open areas (ca. 20%) and cover/edge areas (ca. 80%) with variations
in moonlight. Deer mice consumed more seeds in areas with cover but also did not vary
the proportions of seeds eaten in the open (ca. 43%) or cover (ca. 57%) with variations in
moonlight. Using infrared video filming, we determined that deer mice increased use of
cover to nearly 100% in the presence of Ord's kangaroo rats. Aggression (active chasing
and locking fights) by kangaroo rats towards deer mice caused this shift. Our experiments
substantiate field observations of variable microhabitat use by deer mice in areas with and
without kangaroo rats and identify behavioral interactions involved.
Key words:
Peromyscus, Dipidomys, moonlight, interspecific competition, microhabitat
Microhabitat use by animals is influenced
by many factors, including risks of encountering predators and interspecific competitors. Numerous rodent species reduce use
of microhabitats that lack cover on bright
moonlit nights, which has been attributed to
decreasing risk of predation (e.g., Peromyscus maniculatus-Blair, 1943; Clarke,
1983; Dipodomys-Bowers, 1982; Daly et
aI., 1992; Kaufman and Kaufman, 1982;
Kotler, 1984a, 1984b; Lockard and Owings,
1974a, 1974b; Long1and and Price, 1991;
Onychomys leucogaster-Jahoda, 1973;
Microdipodops-Kotler, 1984a, 1984b;
Price et aI., 1984). In addition to influences
of predation risks on rodents' use of areas
with cover, interspecific interactions with
competitors also may affect use of structurally different microhabitats. Many sympatric rodent species use microhabitats that differ in vegetative cover, potentially reducing
competitive interactions (Kenagy, 1973;
Price, 1978; Randall, 1993). Differences in
sympatric species' uses of open areas and
Journal of Mamma/ogv. 79(2):558-565. 1998
areas with cover are often associated with
differences in locomotory patterns. Bipedal
kangaroo rats (Dipodomys) preferentially
use open habitats, but quadrupedal pocket
mice (Chaetodipus and Perognathus) use
habitats with cover (Randall, 1993). Additionally, aggressive interactions on the part
of a competitor may restrict another species' habitat use (Bowers and Brown, 1993;
Bowers et aI., 1987; Brown and Munger,
1985; Frye, 1983; Grant, 1972; Valone and
Brown, 1995). For example, in kangaroo
rats large individuals are typically dominant
and can display high levels of aggression
(Blaustein and Risser, 1976; Bleich and
Price, 1995; Eisenberg, 1963),
Deer mice (P. maniculatus) and Ord's
kangaroo rats (Dipodomys ordii) live sympatrically in desert and dry grassland areas
and have many of the same resource requirements (Koehler and Anderson, 1991).
Further, these two species have been found
to be active during the same nocturnal
hours in winter, and activity of both is af558
May 1998
FALKENBERG AND CLARKE-DEER MOUSE MICROHABITAT USE
fected by moonlight (O'Parrell, 1974), The
role of behavioral interactions between
these species in determining microhabitat
use is unknown. We investigated microhabitat use by deer mice and evaluated effects
of increased predation risk in conjunction
with presence and absence a larger and potentially aggressive competitor, Ord's kangaroo rat. Activity of deer mice in open areas and areas with cover was compared in
tests with different moonlight intensities, as
moonlight is associated with predation risk,
with and without the presence of a kangaroo rat. We tested hypotheses that deer mice
would decrease activity and foraging in
open areas as moonlight increased, because
moonlight represents increased predation
risk, and that deer mice would further decrease their use of open areas as moonlight
increased when an Ord's kangaroo rat was
present, because the latter represents an aggressive bipedal competitor that prefers
open areas. The role of behavioral interactions between these species in producing
microhabitat associations and the summative effect of interactions between risks of
predation and an encounter with an aggressive competitior on habitat use by deer mice
are unknown.
MATERIALS AND METHODS
Study animals.-Because many factors can
affect activity of animals in the wild, we performed our study in a large indoor chamber with
semi-natural habitat and where the majority of
variables influencing activity patterns could be
controlled. Adult deer mice (11 females, 12
males) and adult Ord's kangaroo rats (four females, three males) were live trapped in an area
dominated by sand sagebrush (Artemesia filifolia) in Weld Co., Colorado. Animals were maintained and tested in the University of Northern
Colorado Animal Care Facility under conditions
of 16°-1SoC and a photoperiod of 12L:12D. Animals were housed individually in 46 by 23 by
20-cm plastic boxes with stainless steel wire
tops. Each deer-mouse box had hardwood shavings, cotton, and a 455-ml metal can in which
to construct a nest. Kangaroo-rat boxes had
sand, cotton, and a 1.3-L metal can in which to
559
construct a nest (J. Randall, pers. comm.). All
animals were provided food and water ad lib.
Deer mice were fed Purina Rodent Chow supplemented with sunflower seed, millet seed, oats,
meal worms, crickets, apples, and lettuce. Kangaroo rats were fed Purina Rodent Chow, oats,
and a commercial gerbil diet. Tests were conducted from 1 September to 15 April 19921993. No individual was kept more than S
months and all animals were released at their
original capture site after testing.
Test conditions.-In the first phase of our
study, we recorded total activity levels, activity
allocation to open and cover-edge areas, and foraging patterns in open and cover-edge areas of
the deer mice under different simulated moonlight intensities in the absence of kangaroo rats,
and in the second phase of our study, a kangaroo
rat was present. Tests were conducted in a chamber with semi-natural habitat. The chamber measured 3.5 by 2 by 2 m and was constructed of
wood and glass. The floor of the chamber was
divided into 25.5 by 25.5 cm squares with a
wooden grid covered with fine-grain sand. Four
shrubs were placed in the chamber, one in each
of the corners. One-half of the chamber's grid
squares were in the open, and one-half of the
squares were shaded by the shrubs or were along
the walls of the chamber (cover-edge areas).
Light bulbs (105 bulbs, 0.5 W each) on rheostat
control were distributed evenly over the ceiling
and were used to simulate five different moonlight intensities. We obtained moonlight reflectance measurements on clear nights using a standard 90% white card and a Luna-Pro light meter
(Gossen, Germany) in an agrarian area of Colorado that lacked any unnatural light sources.
Moonlight-reflectance levels were new moon
(0.05 lux), quarter moon (0.17 lux), half moon
(0.35 lux), three-quarters moon (0.93 lux), and
full moon (2.2 lux). We reproduced these light
levels in the chamber using the standard card,
light meter, and the 0.5 W bulbs on rheostat CODtrol. Two infrared lights in the chamber's ceiling
provided illumination for infrared camera recording in the second phase of our experiment.
Experimental procedure.-In the first phase of
the study, we tested 12 deer mice (six of each
sex) under the following protocol: 1) ca. 1.5 h
after the onset of night, nocturnal illumination
was set to one of the five simulated moonlight
intensities (hereafter referred to as simply
"moonlight intensity") selected from a random-
560
JOURNAL OF MAMMALOGY
ized schedule; 2) fOUT seed dishes, each with 20
shelled sunflower seeds of about equal sizes,
were placed in the chamber-two dishes were
placed in locations randomly selected in areas of
cover edge and two were in the open (water and
a nest refuge were also provided); 3) a deer
mouse was selected from a randomized schedule
and placed in the chamber for 12 b; 4) seed dishes were removed the following morning, and the
number of seeds eaten in the open and coveredge areas were recorded to determine where the
individual focused its foraging activity; 5) the
mouse was allowed to remain in the chamber for
the remaining 12-h daytime period (daytime
light reflectance = 300 lux) and during this time,
each mouse remained in the nest refuge; 6) 1 h
after the night commenced (observed to be the
onset of the peak activity period), the mouse was
removed from the chamber and the sand was
redistributed to prevent scent trailing and was
swept smooth to determine tracking; and 7) the
mouse was reintroduced into the chamber for 12
min and then removed, and its activity for the
12-min period was measured by determining the
amount of tracking in the sand.
We used the sand-tracking method to estimate
the amount of tracking in each grid square based
on the following scale: 0 = 0% tracked, 1 = 110% tracked, 2 = 11-20% tracked, 3 = 21-30%
tracked. and so on to 10 = 91-100% tracked.
We summed tracking scores for all grid squares
to obtain an index of activity for each test (the
maximum possible index was 980 if all 98 grid
squares were 100% tracked) and calculated indices and relative proportions of activity in open
and in cover-edge areas. Before the next test
commenced with a different mouse and different
moonlight intensity, we redistributed and
smoothed the sand. This cycle was repeated until
all deer mice were tested under all of the five
moonlight intensities.
In the second phase of our study, we used 11
deer mice (five females, six males) and seven
Ord's kangaroo rats. As in the first phase, each
individual was allowed to become familiar with
the test chamber, alone and overnight with seed
dishes. Then we placed two individuals (one
deer mouse and one kangaroo rat, randomly
paired) in separate comers of the chamber 1.5 h
after sunset under one of the five moonlight intensities selected from a randomized schedule.
Because individual tracking could not be distinguished with more than one animal in the cham-
Vol. 79, No.2
ber, we filmed activity levels and individuals'
interactions using a Sanyo VDC9212 infrared
camera and a Sanyo lLS900 VCR for 1 min.
After 12 min, the two animals were removed
from the chamber, and the film was analyzed to
determine activity patterns of the deer mouse
and use of open and cover-edge areas (filming
and tracking methods produced identical results). Using a transparent acetate sheet with a
grid matching that of the chamber's that was positioned on the video screen, the rodents' locations were marked every 5 s for 12 min. The
cycle was repeated until all deer mice had been
tested under all five moonlight intensities with
one of the seven kangaroo rats. We recorded
number and proportions of observations that occurred in open areas and cover-edge areas and
behavioral interactions of aggression and avoidance. Aggression was defined as rushing or locking fights (Eisenberg, 1963), and avoidance was
defined as one individual moving to another area
of the chamber when the other animal moved in
its general direction. We recorded aggression
and avoidance as separate events.
We conducted 50 additional tests with a different set of 10 mice to determine if tracking
and filming yielded statistically comparable results regarding mouse use of open and coveredge areas. One observer analyzed mouse activity using the tracking method, and a second observer analyzed activity using the video tape.
Results from the two methods did not differ regarding deer mouse use of open areas (MarmWhitney U test z = ~0.63, P = 0.50) and areas
with cover (z = -0.62. P = 0.51). Thus, activity
data regarding use of open and cover-edge areas
using tracking and filming techniques were statistically identical and comparable.
Analyses.-Due to the small samples and
non-normal distribution of the data, nonparametric statistical analyses were performed using
SAS (SAS Institute, Inc., 1988). Spearman rank
correlation (r,) was used to examine relationships between moonlight intensity and rodent
activity. Kruskal-Wallis (H) one way analysis of
variance was used to determine if activity differed significantly between more than two
moonlight intensities. Mann-Whitney U tests
with the z statistic (SAS Institute, Inc., 1988)
were used to determine if activity differed significantly between two moonlight intensities,
and for comparisons between activity levels in
May 1998
FALKENBERG AND CLARKE-DEER MOUSE MICROHABITAT USE
TABLE I.-Average number of seeds eaten by
deer mice in an enclosure under five simulated
moonlight intensities in the absence of knngaroo
rats and the range and average percentage of
seeds eaten in the open and cover-edge areas
(12 trials in each moonlight level).
X
Range
Percentage
Moonlight
seeds
eaten
Open Cover
Open Cover
New
Quarter
Half
Three-quarters
Full
37.5
31.0
36.8
32.5
39.7
2-38 0-40
2-33 0-29
2-40 4-40
1-40 9-40
1-40 6-36
46.8
39.5
45.1
38.8
43.3
53.2
60.5
54.9
61.2
56.7
open areas and cover-edge areas. Significance
was set at P < 0.05 for all tests.
RESULTS
Deer mice alone in various moonlight intensities. -Total number of seeds consumed
did not differ between moonlight intensities
and averaged 35.5 seeds eaten/trial (n = 60
trails, H ~ 1.844, P ~ 0.764; Table I). Deer
mice consumed seeds in open areas and
cover-edge areas in each moonlight intensity and ate fewer seeds in the open than in
cover-edge areas (z = 2.485, P = 0.013).
On average, deer mice ate 42.7% (17/40) of
the seeds in the open and 57.3% (23/40
seeds) of the seeds in cover-edge areas.
Deer mice did not vary that pattern with
changes in moonlight intensity, and no differences existed between moonlight intensities in number of seeds consumed in open
areas (H = 2.422, P = 0.909) or cover-edge
areas (H ~ 1.962, P ~ 0.743). Deer mice
never ate all seeds available in either area.
When deer mice were alone in the chamber, their overall activity level was correlated negatively with simulated moonlight
intensity (r, ~ 0.4522, P ~ 0.001). Mean
activity indices were 75.8, 118.8, 179.1,
145.3 and 233.8 in full, three-quarters, onehalf, quarter and new moonlight, respectively. Activity levels varied between
moonlight intensities (H = 12.07, P =
0.016). Pairwise comparisons revealed that
activity in new moonlight was higher than
561
in three-quarters or full moonlights (z =
-2.325, P ~ 0.020 and z ~ -2.811, P ~
0.005, respectively), and activity in half
moonlight was higher than that in full
moonlight (z ~ 2.295, P ~ 0.022).
Deer mice were more active in coveredge areas than open areas (z = -8.323, P
= 0.0001; Fig. la), but their proportional
allocation of activity (use of open versus
cover edge areas) did not vary between
moonlight levels (H ~ 3.\85, P ~ 0.527).
On average, deer mice allocated 21.2% of
their activity to open areas and 78.8% to
cover-edge areas, regardless of moonlight
intensity.
Deer mice with Ord's kangaroo rats.In the presence of Ord's kangaroo rats, deer
mice exhibited an increase in their use of
cover-edge areas compared with their use of
cover-edge when alone (z = -8.09, P =
0.0001). Cover-edge areas of the chamber
were used almost exclusively (2:95%) at all
moonlight intensities (Fig. Ib). Aggression
toward deer mice by kangaroo fats and
avoidance by deer mice of kangaroo rats
contributed to this shift in microhabitat use
by deer mice. In the 55 trials, aggression
directed by kangaroo rats toward deer mice
was observed 74 times. The average number of cases of aggression was 1.3 casesl
trial. Deer mice never reciprocated with aggressive behavior; rather they fled the rushing kangaroo rat. In two cases, we observed
physical contact; the kangaroo rat chased
the deer mOUSe, caught it, and the two
rolled in the sand together. The fight ended
with the deer mouse on its back and the
kangaroo rat backing off for a moment only
to chase the mouse again when it fled. In
one case, the mouse escaped into a shrub;
in the other case, one researcher interfered
with the fight because injury to the deer
mouse appeared imminent. In another case,
after a kangaroo rat had chased a mouse up
into a shrub, it began pulling branches
down on the shrub, seemingly in an attempt
to reach the deer mouse. Each of the kangaroo rats displayed about equal numbers
of aggressive actions toward deer mice.
562
JOURNAL OF MAMMALOGY
"'"
.,
a
A voidance of kangaroo rats by deer mice
was observed in every trial (68 instances
during the 55 trials). In all cases of avoidance, deer mice moved away from a kangaroo rat but remained near cover-edge areas. All deer mice displayed about equal
numbers of avoidance behaviors during our
study (one to two cases of avoidance per
trial). Cases of avoidance increased over the
course of our study from one case to two
cases per trial but cases of aggression decreased from two or three cases to no cases
per trial.
C
.~
.:du
-< "'
"
~
;;:" "
0
0
"'~
0.D3
Vol. 79, No.2
0.17
0.35
0.93
2.20
Moonlight (lux)
•
Open
•
Cover
•
Moonlight (lux)
Open
• Cover
c '"
>
u
-< "'
"0
;;:" "
~
~
FIG. I.-Average proportions of activity of
deer mice in the open and under cover in five
simulated moonlight intensities in an enclosure:
a) in the absence of kangaroo rats, ± 1 SD (60
trials, 12 trials per moonlight intensity); b) in the
presence of kangaroo rats, SD < 1.5 (55 trials,
11 trials/moonlight intensity). The lux values of
0.05, 0.17, 0.35, 0.93, and 2.21 correspond to
new, quarter, one-half, three-quarters. and full
moonlight. respectively.
DISCUSSION
Our experiments revealed that deer mice
decreased overall activity as moonlight increased, consistent with findings of prior
studies (Clarke, 1983), and they were more
active in areas with cover under all levels
of nocturnal illumination. However, contrary to our expectations, deer mice maintained the same relative proportions of activity in the open (ca. 20%) and in cover
(ca. 80%) in all moonlight intensities; thus,
microhabitat use remained comparatively
unchanged. The open-cover activity allocation may be related, in part, to predation
costs. Activity in the open would likely increase a mouse's exposure to avian and
mammalian predators, but remaining strictly under cover on bright nights may also
increase a rodent's chances of encountering
a snake predator (Randall, 1993) because
rattlesnakes (Crotalus viridis) also avoid
bright moonlight by remaining near cover
(Clarke et aI., 1996). Due to the low metabolic requirements of the snake and its
highly efficient digestive systems (Pough,
1978), days may pass before a meal is required. Thus, risk of predation to the deer
mouse by an endotherm in the open may
exceed the risk of snake predation under a
shrub.
The observed activity allocation of 20%
open to 80% cover by deer mice also may
be related to foraging benefits. Deer mice
ate about the same number of seeds in each
moonlight intensity and maintained the
Muy 1998
FALKENBERG AND CLARKE-DEER MOUSE MICROHABITAT USE
same relative proportions of seeds eaten in
the open (ca. 43%) and in cover (ca. 57%)
in each test. Because proportions of seeds
eaten in the open and in cover did not reflect activity allocations, deer mice appear
to have concentrated on foraging when in
the open on bright nights without engaging
in other activities. On dark nights, they
were more active in the open (more open
areas were tracked) but consumed nearly
the same number of seeds in the open as on
bright nights, indicating that perhaps they
engaged in other activities in the open in
dim moonlight (e.g., searching for other
food sources). Given increased risks to predation in the open and the fact that mice
never depleted all seeds available under
cover, the question arises as to why deer
mice consumed such a large proportion of
seeds away from cover. This activity pattern
may be related to balancing predation risks
under cover and in the open and it also may
be related to foraging benefits. Vickery et
aJ. (1994) observed that deer mice (P. m.
gracilis) prefer energy-rich foods over protein-rich foods and were energy maximizers. We currently are investigating if seeds
that are dispersed distances from the parent
plant (into the open) contain higher energy
stores than those that germinate in the immediate vicinity of the parent plant in habitats of sand sagebrush. Deer mice may
have been using energy-maximizing strategies, (i.e., to exploit energy-rich seeds in
the open) but only sunflower seeds were
available in these experiments.
Although deer mice have been observed
to use open areas in full moonlight in the
lab and field in Montana (Clarke, 1983),
Kotler's (1984a) trapping results revealed
that deer mice remained in areas of cover
regardless of moonlight intensity in the
field in Arizona where kangaroo rats were
present. A difficulty noted in interpreting
trapping data regarding rodent microhabitat
use is that a species' occurrence in a local
habitat may not be due preference, but rather it could be excluded from more choice
habitats and resources by competitors (Hol-
563
brook, 1979a, 1979b; Miller, 1967). Results
of our study confirm that when deer mice
were alone, they used open areas in all
moonlight intensities and completely avoided open areas in the presence of kangaroo
rats, abandoning activity allocation of 20%
open to 80% cover that they exhibited when
alone. Similar alterations in habitat use and
niche shifting have been observed between
other sympatric rodent species such as deer
mice and voles, Clethrionomys gapperi and
Microtus pennsylvanicus (Crowell and
Pimm, 1976); Ord's kangaroo rats and
grasshopper mice, O. leucogaster (Rebar
and Conley, 1983), and chipmunks, Eutamias umbrinus and E. dorsalis (Brown,
1971). Thus, as Blaustein and Fugle (1981)
noted, biotic factors (e.g., competition) can
supersede abiotic factors (e.g., moonlight)
in determining habitat use by rodents.
When deer mice in this study ventured
into the open, they were immediately
chased back into cover by kangaroo rats.
Chasing and fighting has been documented
between members of the genus Dipodomys
(Bartholomew and Caswell, 1951; Blaustein and Risser, 1976; Bowers and Brown,
1993; Bowers et aI., 1987; Brown and
Munger, 1985; Frye, 1983), but not between deer mice and kangaroo rats. Those
studies and our study were conducted in enclosures, which tend to escalate cases of aggression because one species cannot entirely get away from the other, as would be
possible in the wild (J. Randall, pers.
comm.). However, interspecific aggression
has been proposed as a mechanism maintaining ecological separation between Dipodomys, with the species that is more specialized (e.g., food habits) being the most
aggressive and successful competitor (Blaustein and Risser, 1976; Miller, 1967). We
observed that presence and behavior of the
more specialized kangaroo rats caused deer
mice to shift from broad (open and cover)
to narrow (cover only) microhabitat use.
Subdivision of habitat by vegetative type
has been identified as an important mechanism for coexistence of sympatric rodent
564
JOURNAL OF MAMMALOGY
species and is related to adaptations for arboreal and terrestrial modes of locomotion
(Holbrook, I 979a, 1979b; Zegers and Ha,
1981), and interspecific aggression.
Deer mice exhibit a lower extinction
probability and increased population size in
areas where kangaroo rats have been removed or have exhibted declines (Valone
and Brown, 1995; Valone et al" 1995),
Based on our findings, where kangaroo rats
and deer mice co-occur, deer mice may be
unable to forage on resources in open areas
or evade predators that remain under cover.
Thus, the absence of kangaroo rats in the
study areas of Valone and Brown (1995)
and Valone et al. (1995) may have allowed
deer mice to use a broader range of microhabitats and antipredator and foraging strategies that could not be used in the presence
of Dipodomys. Our study revealed that
presence of Ord's kangaroo rats, a large and
often aggressive bipedal rodent competitor,
directly influences microhabitat use by deer
mice and may limit foraging and antipredator strategies of deer mice.
ACKNOWLEDGMENTS
We thank J. Randall, A. Blaustein, and S.
Mackessy for their valuable comments on the
manuscript; M. Trudgian for trapping assistance;
the Wells family for granting us pennission to
trap on their ranch; D. Ausmus, K. Pritchard, R.
Bookman, and M. Lawlor for their data collection in the methodology trials; S. Patrilla for his
support throughout the study; and two anonymous reviewers. Research was funded by a Faculty Research and Publications Award from the
University of Northern Colorado; reprint requests should be addressed to J. A. Clarke.
LITERATURE CITED
BARTHOLOMEW, G. A., AND H. H. CASWELL 1951. Locomotion in kangaroo rats and its adaptive significance. Journal of Mammalogy, 32:155-169.
BLAIR, W. E 1943. Activities of the Chihuahua deer
mouse in relation to light intensity. The Journal of
Wildlife Management, 7:92-97.
BLAUSTEIN, A R, AND G. N. FuGLE. 198\. Activity
patterns of Reithrodontomys megalotis in Santa Barbara, California. Journal of Mammalogy, 62:195199.
BLAUSTEIN, A R, AND A. C. RISSER, JR. 1976. Inter-
Vol. 79, No.2
specific interactions between three sympatric species
of kangaroo rats (Dipodomys). Animal Behaviour,
24:381-385.
Bl.EICH, V. C., AND M. V. PRICE. 1995. Aggressive behavior of Dipodomys stephensi. an endangered species, and Dipodomys agiiis, a sympatric congener.
Journal of Mammalogy, 76:646--651.
BOWERS, M. A. 1982. Foraging behavior of heteromyid
rodents: field evidence of resource partitioning. Journal of Mammalogy, 63:361-367.
BOWERS, M. A, AND J. H. BROWN. 1993. Structure in
a desert rodent community: use of space around Dipodomys spectabilis mounds. Occologia, 92:242249.
BOWERS, M. A, D. B. THOMPSON, AND 1. H. BROWN.
1987. Spatial organization of a descrt rodent community: food addition and species removal. Oecologia, 72:77-82.
BROWN, J. H. 1971. Mechanisms of competitive exclusion between two species of chipmunks (Eutamias).
Ecology, 52:306-311.
BROWN, J. H., AND J. C. MUNGER. 1985. Experimental
manipulation of a desert rodent community: food addition and species removal. Ecology, 66:1545-1563.
CJ-ARKE, J. A 1983. Moonlight's influence on predatorl
prey interactions between short-eared owls (Asio
fiammeus) and deer mice (Peromyscu.s maniculatus).
Behavioral Ecology and Sociobiology, 13:205-209.
Cl.ARKE, J. A., J. T. CHOPKO, AND S. P. MACKESSY.
1996. The effect of moonlight on activity patterns
of adult and juvenile prairie rattlesnakes (Crota[u5
viridis viridis). Journal of Herpetology, 30: 193-197.
CROWELL, K. L., AND S. L. PIMM. 1976. Competition
and niche shifts of mice introduced onto small islands. Oikos, 27:251-258.
DAl.Y, M., P. R BEHRENDS, M. I. WIl.SON, ANO L F.
JACOBS. 1992. Behavioral modulation of predation
risk: moonlight avoidance and crepuscular compensation in a nocturnal desert rodent, Dipodomys merriami. Animal Behaviour, 44:1-9.
EISENBERG, J. F. 1963. The behavior of heteromyid rodents. University of California Publications in Zoology, 69:1-100.
FRYE, R. J. 1983. Experimental field evidence of interspecific aggression between two species of kangaroo rats (Dipodomys). Oecologia, 59:74-78.
GRANT, P. R. 1972. Interspecific competition among
rodents. Annual Review of Ecology and Systematics,3:79-106.
HOl.BRooK, S. J. 1979a. Vegetational affinities, arboreal activity, and coexistence of three species of rodents. Journal of Mammalogy, 60:528-542.
- - - . 1979b. Habitat utilization, competitive interactions, and coexistence of three species of cricetine
rodents in east-central Arizona. Ecology, 60:758769.
JAHODA, J. C. 1973. The effects of the lunar cycle on
the activity pattern of Onychomys Jeucogaster breviauritus. Journal of Mammalogy, 54:544-549.
KAUFMAN, D. W., AND G. A. KAUFMAN. 1982. Effect
of moonlight on activity and microhabitat use by
Ord's kangaroo rat (Dipodomys ordii). Journal of
Mammalogy, 63:309-312.
KENAGY, G. J. 1973. Daily and seasonal patterns of
May 1998
FALKENBERG AND CLARKE-DEER MOUSE MICROHABITAT USE
activity and energetics in a heteromyid rodent community. Ecology, 54:1201-1219.
KOEHLER, D. K., AND S. H. ANDERSON. 1991. Habitat
use and food selection of small mammals near a
sagebrush/crested wheatgrass interface in southeastern Idaho. The Great Basin Naturalist, 51:249-255.
KOlLER, B. P. 1984a. Risk of predation and the structure of desert rodent communities. Ecology, 65:689701.
- - - . 1984b. Harvesting rates and predatory risk in
desert rodents a comparison of two communities on
different continents. Journal of Mammalogy, 65:9196.
LOCKARD, R. B., AND D. H. OWINGS. 1974a. Moonrelated surface activity of bannertail (Dipodomys
spectabilis) and Fresno (D. nitroides) kangaroo rats.
Animal Behaviour, 22:262-273.
- - - . 1974h. Seasonal variation in moonlight avoidance by bannertail kangaroo rats. Journal of Mammalogy,55:189-193.
LONGLAND, W. S., AND M. V. PRICE. 1991. Direct observations of owls and hetcromyid rodents: can predation risk explain microhabitat use? Ecology, 72:
2261-2273.
MILLER, R. S. 1967. Pattern and process in competition. Advances in Ecological Research, 4:1-74.
O'FARRELL, M. J. 1974. Seasonal activity patterns of
rodents in a sagebrush community. Journal of Mammalogy, 55:809-823.
POUGH, E H. 1978. Ontogenetic changes in endurance
in water snakes (Natrix. sipedon): physiological correlates and ecological consequences. Copeia, 1978:
69-74.
565
PRICE, M. V. 1978. The role of microhabitat in structuring desert rodent communities. Ecology, 59:910921.
PRICE, M. v., N. M. WASER, AND T. A. BASS. 1984.
Effects of moonlight on microhabitat use by desert
rodents. Journal of Mamrnalogy, 65:353-356.
RANDALL, J. A. 1993. Behavioral adaptations of desert
rodents (Heteromyidae). Animal Behaviour, 45:263287.
REBAR, C, AND W. CONLEY. 1983. Interactions in microhabitat use between Dipodomys ordii and Onychomys leucogaster. Ecology, 64:984-988.
SAS INSITfUTE, INC. 1988. SAS/user's guide, release
6.03 edition. SAS Institute, Inc., Cary, North Carolina, 1028 pp.
VALONE, T. J., AND J. H. BROWN. 1995. Effects of competition, colonization, and extinction on rodent species diversity. Science, 267:880-883.
VALONE, T. J., J. H. BROWN, AND C. L. JACOBI. 1995.
Catastrophic decline of a desert rodent, Dipodomys
spectabilis: insights from a long-term study. Journal
of Mamrnalogy, 76:428-436.
VICKERY, W. L., J. L. DAOUST, A. EL WARun, AND J.
PELTIER. 1994. The effects of energy and protein
content on food choice by deer mice, Peromyscu.t
maniculaus (Rodentia). Animal Behaviour, 47:5564.
ZEGERS, D. A., AND J. C HA. 1981. Niche separation
of Peromyscus /eucopus and Blarina brevicauda.
Journal of Mammalogy, 62:199-201.
Submitted 15 November 1995. Accepted 15 April 1997.
A.tsnciate Editor was Earl G. Zimmerman.