Behavioral Ecology VoL 8 No. 4: 404-413
Why do kangaroo rats {Dipodomys spectabilis)
footdrum at snakes?
Jan A. Randall and Marjorie D. Matocq
Department of Biology, San Francisco State University, San Francisco, CA 94132, USA
We examined alternative hypotheses for the benefits of footdrumming in the presence of snakes by the banner-tailed kangaroo
rat, Dipodomys spectabilis, by testing whether the target of the signal includes conspecifics, the predator or both. Footdrumming
recorded in the field revealed that rats altered their footdrumming signatures when drumming at snakes. In playback tests,
however, neighbors failed to show any measurable change in behavior to broadcasts of die snake drumming pattern, but mothers
footdrummed significantly more than nonmothers in the presence of a tethered snake. Gopher snakes, Pituophis •mdanoUucus
affinis, responded to footdrumming vibrations created by a mechanical thumper. Nonhungry snakes avoided footdrumming,
while hungry snakes approached the seismic footdrumming. Snakes decreased stalking rates as footdrummmg increased, but
they spent more time stalking drumming than nondnimming rats. We conclude that D. spectabilis footdrums in individual
defense and in parental care, rather than to warn adult conspedfics. Footdrumming deters pursuit by informing die snake that
die rat is alert and the chances of predation are low. We find little evidence that footdrumming startles, confuses, or harasses
die snake. Hungry gopher snakes, however, may locate prey by eavesdropping on territorial footdrumming. Key words: antipredator behavior, communication, deterrence, Dipodomys spectabilis, footdrumming, kangaroo rat, pursuit, snakes. [Behav Ecol 8:
404-413 (1997)]
B
anner-tailed kangaroo rats, Dipodomys spectabiUs, are solitary, desert rodents that confront snakes in their territories (Randall and Stevens, 1987; Randall et al., 1995). Both
males and females approach snakes, jump back to avoid
strikes, and usually begin to footdrum. Snakes can probably
sense die footdrumming vibrations through low-frequency receptors in their skin, muscle, and ears (Hardine, 1971; Proske,
1969), and hearing sensitivity in gopher snakes (P. m. wtdanoleucus), which ranges from 25 to 700 Hz (Wever and Vernon,
1960), matches die frequency of die footdrumming signal
(Randall, 1984). Kangaroo rats also have ears well-adapted to
detect low-frequency vibrations (Webster and Webster, 1984),
and D, spectabilis responds to airborne sounds transmitted between territories and seismic vibrations transmitted into the
burrow (Randall 1984, 1994; Randall and Lewis, in press).
Because alarm signals are costly in time and energy and can
attract the attention of predators (Caro et aL, 1995; Hump
and Shaker, 1984), they must be adaptive and provide fitness
benefit to die prey such as warning genetic relatives of danger
(Hamilton, 1964). In D. spectabilis, related neighbors can occupy territories close together to form a loosely organized and
spatially dispersed aggregation of kin (Jones, 1984; Jones et
aL, 1988; Randall, 1984). Territories consist of large dirt
mounds, which are a scarce resource that contain burrows
essential for shelter, food storage, and reproduction (Randall,
1984, 1991). A single rat occupies a mound, unless it is a female with young, and defends die territory by chasing away
intruders. The rats communicate territorial ownership to conspecific neighbors widi individually distinct footdrumming signatures, which they can discriminate as coming from a familiar neighbor or unfamiliar stranger (Randall, 1989, 1994,
1995).
Footdrumming in die presence of snakes could also protect
vulnerable offspring. Because of dieir smaller size and inex-
M. Matocq U currently at the Museum of Vertebrate Zoology, University of California, Berkeley, CA. 94720, USA.
Received 17 June 1996; reviied 18 November 1996; accepted 19
November 1996.
1045-2249/97/$5.00 O 1997 Intem»oon»] Sodety for Behavioral Ecology
perience (Owings and Coss, 1977; Owings and Loughry, 1985;
Tamura 1989), young rats may be more vulnerable to snakes
dian adults and benefit from protection by their mothen
(Hennessy and Owings, 1988). Female D. spectabiUs have
young rats in the mound during die summer when snakes are
abundant (Randall, 1991). Footdrumming could inform die
offspring directly of danger, or die drumming might assemble
adults for snake-directed mobbing (Klump and Shalter, 1984;
Owings et aL, 1986).
Alarm signals can also benefit die prey by reducing die alarmist's vulnerability (Triven, 1971). Conspecifics could be die
target, while die drummer benefits (Hersek and Owings,
1993; Sherman, 1985), or die target of die drumming could
be die predator. Alarm calls function in individual defense
when they are directed toward die predator to cause it to
abandon the attack on die individual exhibiting die behavior
(Buder and Roper, 1994; Caro, 1995, 1986a,b; Caro et aL,
1995; Klump and Shalter, 1984).
We examined alternative hypotheses about die benefit of
footdrumming in die presence of «nalr<»T by die banner-tailed
kangaroo rat by testing whether die target of die signal includes conspedfics, die predator, or both (Caro, 1986a,b;
Caro et aL, 1995; Hasson, 1991) (Table 1). We hypothesized
dial footdrumming might function as an alarm signal to communicate a warning to relatives about the type of predator
(Seyfarth et aL, 1980; Slobodchikoff et aL, 1991; Tamura and
Yong, 1993) or die extent of threat and degree of risk (Blumstein and Arnold, 1995; Owings and Hennessy, 1984; Weary
and Kramer, 1995). We also hypothesized dial footdrumming
in the presence of f"a*»t functions in self-preservation of D.
spectabiUs (Buder and Roper, 1994; Caro, 1986a,b; Caro et aL,
1995; Klump and Shalter, 1984). First, because snakes rely on
crypsis to ambush their prey (Raddiffe et al., 1986; Sweet,
1985), we predicted that footdrumming informs die snake of
detection and diat die chances of ambush are thwarted
(Woodland et aL, 1980). Second, we predicted that die rats
footdrum to advertise their alertness and awareness of die
snake and to communicate that continued pursuit is costly
(Caro, 1995). Third, footdrumming could inform die snake
that die rat is healthy and can out-maneuver it (Caro, 1995;
FitzGibbon and Fanshaw, 1988). Finally, footdrumming may
Randall and Matocq • Footdnunming at antipredator behavior
405
imUel
Hypotheses for to ttdr
Hypotheses
Behavior directed to conspccifics
1. Signal to other adulti
2. Mother signals young
Behavior directed to snake
1. General
2. Signal to predator
a. Detection
b. Coat of continued
pursuit
c Healthy condition
S. No signal
a. Harasses, startles or
confuses predator
Prediction
Outcome
of this
study
Neighbors alert to snake fbotroU
Rats without dose neighbors are less likely to drum snake footrofl
Only mothers drum snake footroO
Mothers drum more than nonmotbers
%ung respond to mothers' drumming
Rejected
Rejected
Rejected
Accepted
Untested
Rats drum die snake pattern in absence of con specifics
Rats drum in the presence of snakes
Accepted
Accepted
Rat drums at first sighting of •nnfr^
Snake moves away on hearing drumming
Rat drums after approaching y^pk^
Rat drums until snake stops pursuit
Rats in poor condition do not drum
Rejected
Rejected
Accepted
Accepted
Untested
Snake appears disoriented or exhibits defensive behavior
Rejected
confuse, startle, or harass the snake so the rat can escape.
Footdnunming might be «ixnilar to mobbing, in which an individual rat fbotdrums to harass a snake to cause it to leave
(Loughry, 1987; Owings and Loughry, 1985; Tamura, 1989).
METHODS
Footdrmmning directed to cosspedfica
Study sites and animals
We tested kangaroo rats on two study sites in southeastern
Arizona, USA. Data collected from 1986 to 1992 were from a
population of D. sptctabi&s on a 3.6-ha site established near
Portal, Arizona, in 1980 (Randall, 1984). Data collected in
1993 were from a site in an arid grassland about 50 km southeast of the Portal site (Jones, 1984). Populations on the Portal
site ranged from 23 rats in 1986 to 35 rats in 1989 with
mounds that averaged 20-40 m apart (see Randall, 1995, for
details). The 54 animals (21 adult females, 16 adult males,
and 17 juveniles) on the second site averaged 35 m apart in
1993.
We tethered 430-731 g Arizona gopher snakes, P. m. affinis,
at the mounds of kangaroo rats to elicit footdnimming. A
tether consisted of a strip of nylon underwrap wound around
the snake about 20 cm behind the head to prevent damage
to the snake's skin while providing a slip-free surface on which
to wrap a strip of adhesive tape and to tie monofilament nylon
lines (see Randall and Stevens, 1987, for more details). We
r"3"|"|1y manipulated the snake's position with the monofilament line until 1990, when we tied the snake between two
stakes about 0.6 m apart so it could move and strike.
Observations of behavior
We used the same procedures in all tests. An observer in a
chair 10-15 m from the mound watched the test subject with
binoculars or, after 1991, a night-vision scope (Noctron V)
mounted on a tripod. The mound was illuminated by moonlight or by a dim light from a lantern on a 2-m high tripod
set at least 10 m from the mound. Behavior was described by
speaking into a hand-held tape recorder. All rats were habit-
uated to the observer presence and the dim lights for a minimum of 4 h on a night before a test.
Fooidruwtming signals
We compared footdnunming in the territorial (social) and
snake (antipredator) contexts of 15 solitary rats (10 males and
5 females) and 6 females with young for changes in the signal
elements that compose the footdnimming pattern. We recorded footdrumming during spontaneous territorial drumming and in response to a snake in 1986, 1988, 1991, 1992,
and 1993. Three recordings occurred during natural interactions between a rat and snake; the other recordings were
obtained after tethering a gopher snake. Drumming of seven
rats was recorded in both contexts on the same night; drumming of the remaining rats was recorded on different nights
a Tna-riT"'"" of 2 weeks apart
We used the same recording procedures and data analysis
as reported in Randall (1989, 1994, 1995). We recorded footdrumming with Uher tape recorders at a tape speed of 9.5
cm/s with a 25-dB preamplifier via geophones placed on the
mound near a burrow entrance. We digitized multiple sequences of footdrumming for each individual and counted
and measured signal elements in the footdrumming pattern
that are known to account for individual differences in the
territorial footdrumming signatures (Randall, 1989, 1995).
The /Statistic associated with Wilts' lambda was used to test
for differences in the footdnimming elements of an individual in the two contexts. If a significant result was found, the
univariate /kests determined which signal element! differed
(SYSTAT MANOVA; Wilkinson, 1990).
PtaybaA Usts
We conducted two playback tests with slightly different methods to determine whether rats differentiated territorial footdrumming from antipredator drumming. In July 1989, we
compared responses of 15 adult D. sptctabilxs (5 males and 10
females) to three playback stimuli: (1) footdnimming in the
presence of snakes, (2) the territorial signature of the same
rat, and (3) a control of short bouts of single thumps of a
hammer hitting the ground at a rate of about 8/s. We used
406
original recordings of three rats, recorded in both the territorial and snake contexts in 1987, in five playbacks each. Footdrumming patterns differed in one or more «ignni elements
from the footdrumming pattern of the nearest neighbor
(Randall, 1994).
We broadcast the three drumming stimuli in a counterbalanced order on the same night into an apparatus that generated both airborne and seismic sound (Randall, 1994). The
output of a Uher recorder passed through a car radio amplifier into a voice coil analyzer that transmitted the vibrations
through a fiberglass horn with trimmed edges buried face
down into the ground 2 m from the base of the mound. The
rat was out of the mound and engaged in normal activity for
at least 5 min before the playback began. Each playback lasted
10 min, with a 10-min post-test observation and 20-min rest
period in between so that a total of 30 min occurred between
each stimulus presentation. We set signal amplitude to mimic
the sound of natural footdrumming in the mound and equated the length of drumming during each playback.
We recorded all footdrumming responses from the test subject and from neighbors at adjacent mounds and counted the
number of footrolls from the tapes. We also tabulated the
number of approaches to within 1 m of the speaker and the
time spent out of die burrow. Data were analyzed, after log
transformations, with a repeated-measures ANOVA (SYSTAT)
in a 3X2 design: three playback stimuli (hammer, snake, and
territorial footdrumming patterns) and two test periods (playback and post-test). We report multivariate /Statistics when
possible because assumptions of homogenous variances and
compound symmetry are not required (Wilkinson, 1990).
Critical levels of post-hoc t tests were corrected by the Bonferroni pairwise procedure. If data could not be normalized,
we combined data from the test and post-test periods and analyzed for different responses to the three playback stimuli
with nonparametric statistics.
In July 1992, we tested four females and six males for their
response to playbacks of the snake and territorial footdrumming of neighbors at adjacent mounds. Playback recordings
of 4 neighbors were used once and 3 were used twice in the
10 playback tests. Procedures were similar to those used in
playbacks in other studies (Randall, 1994). We broadcast the
territorial and snake footdrumming of neighbors in a counterbalanced order via separate 60-s tape loops from a cassettetape recorder through a battery-operated Realistic-brand
speaker (RadioShack) placed on the edge of the neighbor's
mound facing the mound of the test subject Drumming on
the tape loops occurred 10-15 s apart with approximately 30
s o f drumming each 60-« revolution of the loop.
Each playback began with a 10-min pretest for observations
of baseline behavior, followed by a 10-min playback and a
10-min post-test A 10-min rest period preceded the next baseline observation. We recorded footdrumming and counted
footrolls from the tapes and tabulated the number of alert
postures and the time spent out of the burrow. We analyzed
data in a 2 x 3 (two playbacks and three test periods) design
with the same statistical procedures used in the earlier playback experiment
Footdrumming to warn offspring
We tested 10 mothers and 7 nonmothers for their responses
to tethered gopher snakes in their territories from 3 to 14
June 1993 (Table 2). We trapped at mounds of these females
before and after the tests and agaia from 14 to 25 July to
determine the presence of pups. The trapping evidence, observations, and vanning for the presence of umall, unmarked
rats revealed that the 10 mothers had young in the mound at
the time of testing ranging in age from about 1 week to 4
month*. The older juveniles of five females weighed 75-120
Behavioral Ecology VoL 8 No. 4
TaMel
Description of belmloi of D. tpretnbiht in retponw to a gopher
Behavior
Description
Alert
Rat (tops activity. When quadruped, rat arches la neck
about 45° and scant the area. When bipedal the body is
held at a 45-90* angle.
Rat stands motionless in alert posture and watches the
Orient
Approach
Withdraw
Footdrum
Latency
Distance
Rat moves toward the snake in elongated posture with
slow, jerky motion.
Rat moves away from an approaching snake or jumps
back after a strike.
Hind feet are lifted and their proximal end repeatedly
struck against the ground. Each time the feet hit the
ground is a footdrum; these are grouped into footrolls
that make up a sequence. Footdrumming is quantified
by counting the number of footrolls.
Time after the beginning of the test for the first
footdrum to occur.
Estimated distance from snake when rat approaches or
footdrums.
g and were estimated to be 2 5 - 4 months old. Because rats of
these ages are known to footdrum at snakes (Randall and
Stevens, 1987), we removed them from the mound during a
test to assure that the animal drumming jp»nH^ the mound
was the mother. Four of these five females had a second litter
of small pups in the mound. The other five females also had
one or two pups in die burrow about 4-5 weeks old, which is
the age of first emergence. Pups of this age do not appear
able to footdrum with any consistency.
We tethered a gopher snake at the base of the mound 2-3
m from the female's main burrow entrance as determined by
observed activity of the rat The 10-min test began when the
rat emerged from the burrow and approached the snake. We
recorded the frequencies of all behavior, tabulated time with
a stop watch, and compared the behavior of mothers and nonmothers with nonparametric tests. Footdrumming was recorded continuously during the tests, and footrolls were counted
from the tapes. We later analyzed for differences in footdrumming patterns in the territorial and snake contexts for six
mothers widi the same procedures described above.
Frtrtf oriiiiHiilinT
o 4? lrTCtfn tO 8BJUKC8
Study animals
We tested 42 P. m, affinis in the laboratory and field from
1990 to 1993. All snakes were captured by hand from a 40-km
radius near Portal, Arizona, USA. In the laboratory, each
snake occupied a wood and glass terrarrum measuring 70 X
55 X 40 cm with 4-5 cm of fine wood substrate in a windowless room with an average temperature of 24°C and a 12:12 h
light:dark cycle. When not in an experiment, we offered
snakes live mice weekly, which was important to maintain natural hunting behavior.
We housed gopher snakes for field tests on sand in aquaria
in the animal quarters at the Southwestern Research Station,
which was an open screened area under natural photoperiod
and temperatures. The snakes were offered mice every 7-10
days. We transported snakes by automobile to and from the
field in large, cotton bags and placed them in their home
cages immediately after returning to the research station each
night
Rats used in the laboratory study were live-trapped in south-
Randall and Matocq • Footdrumming as antipredator behavior
eastern Arizona in 1988, 1991, and 1992. We transported the
rats to San Francisco State University via automobile and
maintained them in a windowless room on a 14L:10 h light:
dark cycle in individual 42 X 22 X 20 cm plastic cages with
wire lids on 4 cm of sand with a tin can burrow. We provided
wild bird seed and iceberg lettuce ad libitum.
Snakt responses to stismie thuntptr
We tested gopher snakes in the field for their responses to
the footdrumming patterns of D. sptttabiHt. A "thumper" designed by EJR. Lewis, University of California-Berkeley, created
seismic footdrumming from cassette recordings of the territorial and snake drumming patterns by hitting a metal rod
onto a pad in the same rhythm as the recordings. We used
60-s tape loops of continuous drumming to run the thumper
during the tests.
We tested snakes in a large enclosure (18 m long X 3.25 m
wide X 1 m high) in an open, desert area near Portal, Arizona. Sides of the enclosure consisted of black, plastic window
screening stapled to stakes pounded into the ground every 2 3 m with 10 cm of the bottom of the screening covered with
a layer of soiL We observed f"aVT with a night vision scope
mounted on a tripod outside the center of the arena. Lanterns on 2 m poles on each end of the enclosure provided
dim light for the scope. Soil in the area was raked thoroughly
between tests to control for olfactory cues.
Snakes could move from die center of the arena toward an
adult D. specUMUs that moved freely in 52.7 X 15.5 X 155
cm open wire-mesh cages. We positioned one rat at the back
of the seismic thumper and die other rat without the thumper
approximately 1 m from die ends of the arena. Footdrumming by die rats was dampened with a 2.3 cm layer of foam
rubber on the bottom of die cage. We buried die diumper
1.3 m from die end of die enclosure in a 30-cm deep hole
and covered it with a wooden box and soil so there was no
visual evidence of its presence. Location of die diumper was
shifted to control for position effects. Therefore, half die
snakes in a sample heard footdrumming coming from one
direction and die other half heard it from die opposite direction.
We introduced snakes into die center of die test arena, one
at a time, in their cotton bags. Appearance of die snake's head
from die bag marked die beginning of die test. We recorded
quiedy into a hand-held tape recorder die time snakes sampled dieir environment by moving their heads and flicking
dieir tongues and die time to travel to die end of die arena.
A test ended when die snake struck at die caged rat, reached
die end of die arena, or laid in die bag widiout moving for
45 min.
We tested snakes diat varied in hunger for dieir responses
to die footdrumming patterns. Injury 1990, we tested six large
gopher snakes > 1 m that had been kept at die Soudiwestern
Research Station since capture and dius had been widiout
food for at least 2 months. In July 1991, we tested 14 snakes
ranging from 0.82 to 13 m in length and weighing 214-998
g for dieir responses to die territorial and snake footrolls of
diree different rats, selected at random, so diat half of die
snakes were tested first for dieir response to die territorial
footdrumming and half to die snake footdrumming. We only
used data from die first test, however, because snakes tended
to move in die same direction die second time in die arena
as in die first independent of die position of die diumper. We
fed die snakes when captured and deprived diem of food for
4 weeks to control for hunger.
In July 1992 we conducted a diird experiment. We tested
18 snakes diat differed in die amount of time deprived of food
for dieir response to die snake footrolL We captured 12
snakes ranging from 0.69 to 1.26 m and weighing 100-1136
407
g (average 525 g). The remaining six snakes weighed an average of 753 g and had been in die laboratory since 1991 and
returned to Arizona by car in 1992. We divided die 6 snakes
evenly between 2 food regimes and tested 8 snakes widiin 1
week of eating 1-2 mice and die remaining 10 snakes after
being deprived of food for 6 weeks. The snakes deprived of
food showed a significant weight loss of 23 g (« = 3.18, df 9, p - .01).
Because we predicted die snakes would move away from die
diumper, we tested for choice as determined by direction
moved widi a one-tailed binomial test. We compared hungry
and nonhungry snakes for die time it took to reach die end
of the test arena widi a 2 (hungry and nonhungry) X2 (drumming and no drumming) ANOVA after data were normalized
widi log-transformations (SYSTAT, Wilkinson 1990). We designated snakes diat had not eaten in 6 weeks or more as hungry (n « 15) and snakes diat had eaten in 4 weeks or less as
nonhungry (n = 21).
Drumming and nondrumming rats
Because only a portion of D. sptctabihs drum consistendy in
laboratory tests, we could compare snake responses to drumming and n on drumming rats. We tested 10 gopher snakes
(434-1240 g) from December 1992 to February 1993 in encounters widi four rats diat were active footdrummers and
four rats diat had "never drummed during a rat-snake interaction. We fed die snakes a regular diet of live mice and water
but deprived diem of food for 5 weeks before a test to increase
dieir predatory behavior. We were unable to use data from
diree snakes because rats failed to footdrum as predicted or
die snake captured die rat.
We analyzed videotapes of nine additional animal* ranging
in size from 200 to 791 g diat were used as stimulus animah
widi rats in odier experiments (Randall JA, Matocq MD,
Hatch SM, unpublished data). All procedures were die same,
except we deprived die snakes of food 2-4 weeks instead of 5
weeks.
We used procedures developed by Randall et al(1995) in
all tests. We staged 15-min interactions in die laboratory in a
large 4X1.2X1 m rectangular arena widi OS m of sand in die
bottom. We habituated bodi die snake and rat to die arena.
The snake moved freely in die arena for 1 h. We removed die
snake, raked die sand dioroughly to distribute odors, and introduced die rat into die arena in its tin can burrow for 2436 h widi food and in a normal lighcdark cycle.
We videotaped 15-min encounters between a rat and snake
simultaneously under red lights widi two 8-mm video, low-light
intensity cameras on tripods from a raised (2 X 2 X 0.675 m
high) pladbrm positioned 1.0 m from die end of die experimental arena. We focused die video cameras directly into die
arena or on a 1.35X1.2 m mirror suspended at a 20 s angle at
die end of die arena opposite die camera. Filming began 3 5 h into die dark cycle immediately after removing die tin can
burrow.
We reintroduced die snake into die opposite end of die
arena from die test subject. An encounter was initiated when
eidier die rat or die snake approached to widiin 1 m and an
interaction occurred, which we defined as a change in behavior of die animal being approached. Capture of a rat (n =• 3)
by die snake caused immediate termination of die test and
removal of die rat from die snake. We returned bodi die rescued rat and die snake to dieir respective home cages and
fed die snake laboratory mice. Sand in die arena was raked
dioroughly after each test.
We compared behavior of die 16 snakes in diree 5-min segments for dieir responses to drumming and nondrumming
rats in (1) time stalking defined by an approach of a snake to
widiin 1 m and continued monitoring of die rat until die
408
snake moved away and (2) number of approaches that resulted in stalking. We also counted the number of footroHs
drummed by rats in response to stalking snakes. We analyzed
data with multivariate repeated-measures tests, after log transformations, in a 2 (drumming versus nondrumming)XS
(times) design. If dgnifiranf Fkesa were found with Wilks'
lambda, we did paired / tests with Bonferroni corrections.
Snake behavior was examined in more detail in tests with
drumming rats. We tabulated the number of approaches, moving away and lying with head oriented toward footdnimming
rats. Neutral behavior consisted of moving around the edge
of the arena with no noticeable response to the rat Because
we found no measurable difference* across time, we combined the data, and, after log transformation, compared the
four behaviors with a one-way ANOVA and paired t tests with
Bonferroni corrections. Data are presented as means ± SE.
RESULTS
Comparison
sod territorial footdrmmiiing
Footdrumming signals
All rats drummed different patterns in the territorial and
snake contexts as determined by «ign Hi r^pt Wilks' lambda.
The rats changed the two signal elements of the footdrumming pattern that account for individual differences in territorial drumming (Randall, 1989), the number of fbotdrums
in the first footroll, and the number of footrolls in a sequence
(Figure 1). Paired t teats of the means of these two signal
elements for each rat in each context showed a «igntfimnt
decrease by 7.68 footdrums in the average length of the first
footroll (t -» 6.47, df - 14, p - .0001) and an average increase
by 5.6 footrolls in the number of footrolls in a sequence (/ "
4.29, df - 14, p - 0.001; Figure 1).
Mothers altered the same signal elements that were
changed by adult rats without offspring. In the presence of
f ? t ^ « . they decreased the average length of the first footroll
in their territorial footdrumming by 3.6 footdrums (t «• 2.4,
df ™ 5, p •» .058) and increased die average number of footrolls in a sequence from 5.0 ± 0.7 in die territorial context
to 8.2 ± 0.5 in the snake context (( - 5.1, df • 5, p - .004).
Drumming rate significantly increased from 18.0 ± 1.7 fbotdrums/s during territorial drumming compared with 20.5 ±
1.7 footdrums/s during die snake footdrumming ( ! « 2.8, df
- 5, p - .058).
Footdnimming in die presence of snakes did not attract
conspedfics. No neighbors visited territories of drumming
rats during the tethered-snake trials.
Playback tests
The rats altered their drumming with die type of playback
(main effect for playback: Fra — 4.76, p - .014; Figure 2a).
They fbotdmmmed significantly more to die territorial playback than to die control (t « 2.32, df » 14, p <.05). The
amount of drumming did not differ significantly between die
snake playback and the control, between the territorial and
snake playbacks after die Bonferroni correction (p >.O5), or
between die test and post-test (Flta - 0.98, p •» .33). The
playback by tune interaction was not significant {F±a •» 2.06,
p = .14).
The rats spent similar time out of die mound during each
playback (F%At «= 0.26, p - .77): 3.2 ± 0.9 min during the
hammer thumps, 2.5 ± 0.9 during die snake playback, and
2.81 ± 0,85 d u m g the territerial playback. The average total
time out of the mound during die playback test was 2.82 ±
0.9 min, compared with die post-test time of 4.6 ± 1.2 min
(*i.« " 3 - 3 2 . P " ° 7 6 ) - The r* 0 approached die speaker an
average of two to three times during die 10-min test and posttest periods for all three stimuli.
Behavioral Ecology VoL 8 No. 4
Footdrt
j directed to
Signal to adult neighbors
Dipodomys sptctabiBs did not respond to playbacks of antisnake footdrumming of neighbors. In the first test, neighbors
did not differ significantly in die number of footrolls
drummed in response to playbacks of die territorial, snake,
and hammer control (Freidman's - 4.625, df -> 2, p » .099;
Figure 2b). In me second test, few rats drummed in response
to broadcasts of neighbor footdrumming. Six of 10 rats
drummed during die test and post-test of the territorial playback. No rats drummed during die snake playback, and only
diree drummed during die post-test of the snake playback.
Two rats drummed in die pretest
The neighbor rats seemed to hear die playback broadcasts;
mey stopped activity and stood in alert postures when die
playbacks began. The number of alert postures did not differ
significantly, however, in die two playback contexts(.Fj,ls »
0.93, p - .45). The rats exhibited 6.8 ± l& alert postures
during die playback of die territorial footdnimming compared with 4.4 ± 1.7 during the snake playback. Pretest and
post-test responses were similar (p > .05). The rats stood alert
8.5 ± 2.85 times in die pretest and 5.1 ± 2.4 during die posttest of the territorial playback and 4.9 ± 0.95 in die pretest
and 6.8 ± 2.8 in the post-test after die snake playback. They
spent about die same percentage of time out of die mound,
widi 54.4% out during die territorial playback and 56.9% out
during the snake playback.
Signal to offspring
Females with pups footdrummed at higher rates than those
with no pups and actively came closer to die snake (Table 3).
Nine of 10 mothers drummed compared widi 4 of 7 nonmothers (Fisher's Exact test, p < .05). Mothers drummed 62%
of dieir fbotroDs on the mound at an estimated distance of
0.3-13 m from die snake. Only two of seven nonmothers
drummed out of die mound. Eight mothers approached die
head of die snake, compared widi only two nonmothen. AH
females were very active when a snake was present, and both
mothers and nonmothers spent a majority of time out of die
mound. Other behaviors did not differ significantly (Table 3).
Most mothers (80%) had vulnerable pups in tile burrow
that were quiet and did not exit the mound or footdrum inside the burrow when die mother drummed during a test
Only one rat at a time drummed inside die mound and was
presumed to be die mother.
Co
Response to seismic thumping
Snakes detected die seismic vibrations but did not differentiate the snake and territorial drumming (Table 4). Snakes that
had not eaten in 6 weeks or more took 11.7 ± 3.0 min (n "
6 snakes from 1990) to reach the end of die arena widi die
territorial footroll compared widi 9-5 ± 1.5 min to reach the
end of die arena widi die snake footroll (n — 4 snakes in
1992; t - 036, df = 8, p >.O5).
Hunger influenced tile snakes' response to die seismic
thumping. Snakes that had recently eaten tended to move to
the end of the area without die thumper (16 of 21; Table 4).
In contrast, 10 hungry snakes approached die seismic drumming, while five hungry snakes moved away (x1 with date's
concoction • 4.98, df • 1, p •= .026). We found a significant
interaction between hunger and direction; hungry snakes
moved more slowly than nonhungry snakes when approaching the thumper (.FI-M «• 8.607, p - .006; Figure 3). Nonhungry and hungry snakes did not differ significantly in total time
traveling (main effect for hunger F liM •* 0.43, p m 32) or in
409
Randall and Matocq • Footdrumming as anrJpredator behavior
1
i
i
•
i
i
i
i
I
i
i
i
6
8
10
12
14
16
18
20
22
24
26
28
Footrolls in Sequence (X±SE)
Figure 1
Footdrumming patterns of 15 D. sptrtnNHt during territorial drumming (shaded ellipses) compared with drumming patterns (open ellipses)
of the same rats in the presences of snakes. Ellipses are plots of the average (± 1 SE) number of footdrums in the first footroD and average
(± 1 SE) number of footrolls In a sequence.
time traveling toward or away from the thumper (main effect
for direction: FlM = 3.01, p = .088). The time sampling with
head out of the bag before moving from the center of the
arena also was not significant {flM » 0.34, p » .82).
Response to drumming rats
Gopher snakes spent significantly more time stalking drumming ran (mean ± SE, 4.09 ± 1.0 min) than nondnimming
rats (2.22 ± 0.46 min) during the 15-min tests {F^ - 4.47,
p = .045). Total time stalking decreased significantly during
the test (Fug " 17.6, p " 0.0001), with significantly more time
stalking in the first 5 min interval (1.8 ± 0.36 min) than during the second (0.81 ± 0.22 min; I = 439, df - 31, p < .01)
or third (033 ± 0.25 min; t = 6.09, df = 32, p < .01) 5 min
intervals.'The snakes stalked drumming rats for 2.29 ± 0.41
min in the first 5 min of the test, compared with 1.1 ± 0.2
min for nondrumming rats (interaction: /"us ~ 3.498, p "
.044).
The snakes sharply decreased the time they stalked drum-
ming rats during the first 5 min of the test (Figure 4). Time
stalking and the number of footrolls were negatively correlated (r • - . 9 3 , p = .025). A majority of rats (81%) began to
footdrum during the first 5 min of the test (Figure 4). Snakes
spent almost the same amount of time stalking drumming rats
during the second (0.92 ± 0.27 min) and third (0.89 ± 0.32
min) 5-min periods of the test, and rats continued to footdrum at an average rate of 3-5 footdrumming bouts/min for
the remainder of the test
Although time stalking differed in tests with drumming and
nondrumming rats, the number of predatory approaches was
similar <flx ™ 2.43, p «= .13). The snakes averaged 1.27 ±
0 5 predatory approaches to drumming rats, compared with
1.93 ± 0 3 to nondrumming rats in the first 5 min of the test.
In the second 5-min interval, snakes approached drumming
rats 1.0 ± 0.03 times and nondrumming rats 0.94 ± 0 3 times.
The number of predatory approaches continued to decrease,
and snakes approached drumming rats only 0.75 ± 035 times
410
Behavioral Ecology VoL 8 No. 4
Table 4
Response of gopher snakes, P. m. aflmb, at different leveb of
hunger to playbacks of D* tpn titbuu territorial and soaks
footdramming crested by a seismic dumipei
Weeks
since
Type of
footroll
Experiment 1
Experiments
Experiments
Territorial
Territorial
Snake
Snake
Snake
Approach Avoid Strike
thumper thumper (%)•
>6
4
4
1
6
0*
5*
6
5
5
100
14
0
14
14
CO
' p < .03, binomial test for choice of direction; data are combined in
experiments.
* Strike tnAirmttt percentage of snakes striking at a rat protected in a
wire cage.
1
3-
(b)
T
1
r -.
21 -
T-
It
__
Hammer
Territorial
Snaka
Figure 2
Rate of footrolls by (a) residents (n ~ 15) and (b) neighbon (n 10) to playbacks of three different drumming patterns: hammer
thumping as a control, snake footroll, and territorial footdnimming
signatures of the same rat.
and nondrununing rats 0.13 ± 0.1 times in the last 5 min of
the test.
The snakes exhibited four different responses to the footdrumming rats (main effect for response: Fi3> — 6.7, p —
.006). They moved both toward and away from drumming
rats, oriented to the drummer, and engaged in neutral behavior of exploring the arena (Figure 5). The snakes explored
the test arena at a consistently higher rate than they engaged
in any other behavior. They averaged 8.3 ± 1.5 explorations
Table 5
OTiiUxrlnTii of responses of fc ale* with young and whh no young
m the natal mound to a gopher snake tethered at the base of the
nimiiwl dm lug a 10-mm test (•"—"« ± SEj Mann-Whitney V teat)
Mothers
(n - 10)
during the 15-min test compared with approaching the rat 3.0
± 0.73 times (t - 3.38, df - 15, p - < .01), moving away
1.25 ± 0.60 times(< - 4.46, df - 15, p - < .001), and orienting to the rat an average of 4.1 ± 1.42 times (t •* 2.9, df
« 15; p > .05 after Bonferroni correction for this and all
other comparisons).
DISCUSSION
We are able to answer the question of why D. sprctabilis footdrums in the presence of snakes from tests of alternative hypotheses summarized in Table 1. In general, we reject the
hypothesis that D. sptttabilis footdrums to warn conspedfics,
except in the case of mothers with young, and accept the
hypothesis of footdnimming directed to the snake. The kangaroo rats footdrum after an initial interaction with a snake
to deter its continued pursuit, rather than as a signal of detection or to harasses, startle, or confuse the snake.
; directed to adult conspedfics
It is unlikely that D. sptctabiHi footdrums to warn neighbors
of danger (Table 1). First, D. spectabihs is a solitary specie*,
and both males and nonreproductive females drum in the
presence of snakes in the absence of conspecifics in both the
field and laboratory (Randall and Stevens, 1987; Randall et
aL, 1995). In contrast, rodents that emit alarm calls to warn
E 10 •
LU
53
Nonmothers
(n-7)
IX
- *
Frequency
Footrolls
Approach snake
Alert to snake
Time (min)
Oriented to snake
Out of mound
Latency to drum
Closest distance (m)
LU
190.2 ± 43.4
7.6 ± 1.4
5.1 * 0.96
1
1
^
~
60.9 £ 36.7
6.9 ± 23
4.4 ± 1.1
.035
.402
.768
ZS
7.5
5.6
0.56
.242
.432
.128
2
f=
• FED
• HUNGRY
•
••
IH
11H
5 •
TO DRUMMING
AWAY FROM DRUMMING
1
DIRECTION
4J i 0.9
5.0 * 3.77
2^*0.94
0.12 + 0.03
i
•
£
*
1.1
3.1
1.71
0.18
.047
Figure 5
Time taken for hungry gopher snakes to move toward (n - 10) or
away (n ~ 5) from seismic drumming compared with movement of
nonhungry (fed) snakes toward (n — 5) or away (n - 16) from the
drumminir.
Randall and Matocq • Footdrumming as antipredator behavior
2
3
4
5
Figured
Average time (s) spent by gopher snake* (filled circles)
stalking footdrumming rats
during each minute of 10-min
of a 15-min encounter compared with the mean frequency of fbotroDs drummed by the
rats (open drdes) and the
number of rats that began
drumming (open bars) each
6
MINUTES
conspedfics of danger only call when relatives are nearby
(Hoogland, 1983, 1996; Sherman, 1977).
Second, neighbors did not respond to the snake footdrumming. Although the territorial and snake drumming patterns
differed, the rats failed to respond to playbacks of the snake
footrolL In contrast, the rats discriminated playbacks of territorial footdrumming from the general thumping of a hammer and drummed more to the territorial drumming than to
the snake drumming. These results are consistent with behavior observed in other experiments in which rats recognized
differences in territorial footdrumming patterns (Randall,
1994). If the snake footroll communicates predation risk, the
rats should be able to discriminate the signal and respond
\n
•
0
•
accordingly (Blumstein and Arnold, 1995; Owings and Hennessy, 1984; Seyferth et aL, 1980; Slobodchikoff et al., 1991;
Tamura and Yong, 1993; Weary and Kramer, 1995).
Third, the drummer may gain little benefit from warning
neighbors. Neighbors can be unrelated as well as related, and
the distribution of territories makes it impossible for D. spectabiUs to direct its footdrum warning to benefit only neighboring kin. Furthermore, the drumming fails to recruit conspecifics for mobbing or to cause confusion (Caro, 1986a;
Hersek and Owings, 1993; Owings and COM, 1977). Therefore, the risk of a continued interaction with the snake and
energy cost of drumming seem to outweigh any benefits the
drummer might receive from warning neighbors, even at high
AWAY
TOWARD
ORIENT
NEUTRAL
0-5
5-10
MINUTES
10-15
Figure 5
Frequency of moving away, toward, and orientation of gopher snake*, P. mdancUucus,
(n - 16) to footdrumming D.sptctabilu during 5-min intervals of a 15-min encounter.
Neutral behavior was mainly
exploratory without regard to
the presence of the rat.
Behavioral Ecology VoL 8 No. 4
411
population densities when territories are close together and
neighbors have a greater chance of being related (Jones et
aL, 1988).
uzrcctco to
The data support the hypothesis that mothers footdrum in
the presence of snakes to protect vulnerable offspring (Table
1). Kangaroo rat mothers respond more intensely than nonmothers to the presence of a snake by footdrumming at higher rates and coming closer to the snake. What is unclear is
whether females footdrum to warn their pups of a snake on
the mound or if the behavior is directed toward the snake.
The mother's footdrumming could convey the extent of
threat and risk to her pups (Bhimstein and Arnold, 1995; Nikolskii et aL, 1994; Owing* and Hennessy, 1984; Weary and
Kramer, 1995). Because we removed older juveniles from the
mound and the young pups remained inside, we have no information about responses of young rats to the drumming.
They seemed to remain quiet in the burrow. The temporal
differences in the territorial and snake footdrumming sequences could convey different messages, and it may be important for young rats to discriminate difference* in the two
patterns drummed by their mothers, especially if an inappropriate response results in their death.
Footdrmnming directed to the winkf
Our results support the hypothesis that D. sptttabiht footdrums in the presence of snakes to reduce its own vulnerability (Hump and Shaker, 1984; Trivers, 1971) (Table 1). The
rats drummed the snake footroll in the absence of conspedfics, and a decrease in stalking behavior of the snakes was highly correlated with an increase in footdrumming by die kangaroo rats. Snakes have been observed leaving the mound
during natural interactions in the field (Randall and Stevens,
1987). Hence, footdrumming seems to decrease predatory behavior of the snake and possibly inhibits further pursuit
Footdrumming, therefore, seems to communicate to the
snake that the rat is alert and aware and thus that the snake's
chances of successful capture are low. The continuous series
of footroDs may function as a tonic signal to maintain the
snake's attention (Hersek and Owings, 1993). The long, repeated rhythmic bouts of footdrumming may be the most efficient way for a rat to communicate directly to the snake. We
suggest that the change in footdrums from the territorial to
the snake footroll is a scaling change. The rats increase footroll repetition rate as they grow more excited, which could
communicate increased arousal and enhanced awareness of
the snake by the rat.
We reject the hypothesis that footdrumming informs the
snake of detection, because antipredator drumming always occurs after an encounter with the snake, not at first sighting.
We have never seen a rat begin to footdrum in the presence
of a snake before it has approached and interacted with it
(Randall et aL, 1995, this study). More likely, the physical approach of the rat to the head of the snake informs it of detection and that the chances of ambush are lowered. Antipredator behavior continues when the rat footdrums an intense
series of short fbotrous at a safe distance to inform the snake
its presence is being monitored. Rats footdrummed when they
interacted with more predatory snakes, which suggests that
predatory beHaVfor of (he fnake increases the probability that
a rat will footdrum.
We are unable to rule out that footdrumming communicates a healthy condition and the ability to avoid predation
(Caro, 1995). We have no evidence that rats in poor condition
fail to footdrum or are more vulnerable to snake strikes. We
do have evidence that very old rats footdrum in the presence
of snakes and can avoid snake strikes as well as younger rats
(Randall JA, Matocq MD, Hatch SM, unpublished data).
Finally, there is little evidence that footdrumming alone
confuses, harasses, or startles snakes. The snakes that moved
toward the end of me arena with the seismic thumper did not
avoid the vibrations and moved over the top of the buried
thumper to reach the caged rat. The f?fc*^ exhibited no obvious sign of discomfort or confusion when responding to the
artificial thumper or when a rat footdrummed. Sometimes
snakes pulled their head back and hissed defensively at the
approach of a rat, but this behavior was never observed in
response to footdrumming alone. We never observed rats biting or physically harming a snake.
We conclude, therefore, that D. spedabiUs footdrums in the
presence of snakes to communicate continued awareness of
the location and presence of the snake. Footdrumming functions as a less dangerous defense than contact with the snake
to deter pursuit after the rat has initially approached the
snake and interacted with it
Do snake* locate prey from footdrammmg?
Our results suggest that hungry ima^r* may locate kangaroo
rats from their territorial footdrumming. Hungry snakes
moved toward the seismic thumper during drumming of both
the territorial and snake footrolls, while nonhungry snakes
tended to move away from the drumming. By locating the
territorial footdrumming of kangaroo rats, hungry snakes
could save search time.
Some predators are able to use their prey's intraspecific
interactions to locate their prey (Ryan et al., 1981; Tuttle et
aL, 1982). A third party can eavesdrop on a dyadic interaction
because any attempt to reduce eavesdropping may decrease
effectiveness of die signal (MarU, 1985). Snakes, therefore,
could locate kangaroo rats by their territorial advertisement
Hungry snakes often travel long distances in search of rodents
with patchy distributions (King and Duvall, 1990). Occupied
D. spettabiHs mounds can vary considerably from year to year
in some areas, so it would be to a snake's advantage to locate
an area of occupied mounds from the territorial footdrumming and then wait in ambush of individual rats at specific
locations.
Our deep appreciation goe* to Maureen Sullivan for her tireless help
with the field portion of this study and to Ted Lewis, Department of
Electrical Engineering and Computer Science, University of California, Berkeley, for use of the thumper*. We also appreciate assistance
from Susan Hatch, Evon Hekkala, Patricia Kennedy, Jennifer Nymark,
Allie Rich, Jay Shore, Mary Beth Stone, and the staff at the Southwestern Research Station. We thank Peter Waser for allowing us to
work on his Rucker Canyon site in 1993, Wade Sherbrooke for the
use of his gopher snakes in 1990, and Larry Wolf and anonymous
reviewer! for their reviews and editing of the manuscript. We are
grateful for support to J.A.R. by the National Science Foundation,
BNS 87-16860. BNS 89-08827, BNS 91-09850, IBN 95-06688 and the
National Geographic Society (3273-86). Research approved by University Animal Care and Use Committee.
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