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Avoiding predators at night antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus).

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American Journal of Primatology 69:611–624 (2007)
RESEARCH ARTICLE
Avoiding Predators at Night: Antipredator Strategies
in Red-Tailed Sportive Lemurs (Lepilemur ruficaudatus)
CLAUDIA FICHTEL
Department of Behavioral Ecology and Sociobiology, German Primate Center,
Göttingen, Germany
Although about one-third of all primate species are nocturnal, their
antipredator behavior has rarely been studied directly. Crypsis and a
solitary lifestyle have traditionally been considered to be the main
adaptive antipredator strategies of nocturnal primates. However, a
number of recent studies have revealed that nocturnal primates are not
as cryptic and solitary as previously suggested. Thus, the antipredator
strategies available for diurnal primates that rely on early detection and
warning of approaching predators may also be available to nocturnal
species. In order to shed additional light on the antipredator strategies of
nocturnal primates, I studied pair-living red-tailed sportive lemurs
(Lepilemur ruficaudatus) in Western Madagascar. In an experimental
field study I exposed adult sportive lemurs that lived in pairs and had
offspring to playbacks of vocalizations of their main aerial and terrestrial
predators, as well as to their own mobbing calls (barks) given in response
to disturbances at their tree holes. I documented the subjects’ immediate
behavioral responses, including alarm calls, during the first minute
following a playback. The sportive lemurs did not give alarm calls in
response to predator call playbacks or to playbacks with barks. Other
behavioral responses, such as gaze and escape directions, corresponded to
the hunting strategies of the two classes of predators, suggesting that the
corresponding vocalizations were correctly categorized. In response to
barks, they scanned the ground and fled. Because barks do not indicate
any specific threats, they are presumably general alarm calls. Thus,
sportive lemurs do not rely on early warning of acoustically simulated
predators; rather, they show adaptive escape strategies and use general
alarm calls that are primarily directed toward the predator but may
also serve to warn kin and pair-partners. Am. J. Primatol. 69:611–624,
2007. c 2007 Wiley-Liss, Inc.
Key words: antipredator behavior; nocturnal primates; alarm calls;
playback experiments; sportive lemurs
Contract grant sponsor: Deutsche Forschungsgemeinschaft; Contract grant number: Fi 929/1-1.
Correspondence to: Claudia Fichtel, Dept. of Behavioral Ecology and Sociobiology, German
Primate Center, Kellnerweg 4, 37077 Göttingen, Germany. E-mail: Claudia.fichtel@gwdg.de
Received 17 March 2006; revised 20 April 2006; revision accepted 8 June 2006
DOI 10.1002/ajp.20363
Published online 23 January 2007 in Wiley InterScience (www.interscience.wiley.com).
r 2007 Wiley-Liss, Inc.
612 / Fichtel
INTRODUCTION
Antipredator behaviors can be broadly classified as strategies that reduce the
risk of detection by predators (precautions) and strategies that take effect when
potential prey detect a predator. The first strategy includes avoiding places where
predators are, and/or being vigilant against them. Many studies of a wide range
of birds and mammals have demonstrated that vigilance improves predator
detection before attack, thus allowing appropriate antipredator responses by the
prey [Elgar, 1989; Lima & Dill, 1990; reviewed in Caro, 2005; Caro et al., 2004].
Other precautions against predators of diurnal species are to form groups or
mixed-species associations [Hamilton, 1971; Heymann & Buchanan-Smith, 2000;
Lima, 1995; Powell, 1974; Pulliam, 1973; van Schaik & van Hooff, 1983]. Animals
thereby benefit from predator confusion, the ‘‘selfish herd and dilution’’ effect,
and improved detection of predators.
Once a predator has been detected, animals can respond in several ways.
They give alarm calls, flee, or seek confrontation with the predator. Alarm calls
are a widespread form of antipredator behavior in which one or more group
members give loud calls to signal the presence of predators to conspecifics.
Potential functions of alarm calls include pursuit deterrence [Caro, 1994; Tilson
& Norton, 1981] and signaling predator size and location [Blumstein & Armitage,
1997; Evans & Marler, 1995; Owings & Hennessy, 1984; Templeton et al., 2005]
and identity [Fichtel & Kappeler, 2002; Manser et al., 2001; Seyfarth et al., 1980;
Struhsaker, 1967; Zuberbühler et al., 1999] to conspecifics. Warning other group
members can cause increased vigilance, resulting in short-term benefits for both
caller and receivers obtained by monitoring the predator’s movements [Owings &
Leger, 1980], or long-term benefits for the caller by protecting kin and mates
[Hogstad, 1995; Sherman, 1977].
Alarm calls typically elicit startle or escape behavior in conspecific recipients.
Animals can either flee in any direction or exhibit predator-specific escape
strategies that are adapted to the hunting strategies of predators. For example,
arboreal species may climb down the tree they are currently in when they are
attacked by aerial predators, or climb up in response to terrestrially hunting
predators [Cheney & Seyfarth, 1990; Fichtel & Kappeler, 2002; Macedonia &
Evans, 1993]. Detected potential prey may also preemptively attack the predator.
Such mobbing is a widespread form of antipredator behavior in birds and
mammals [Bartecki & Heymann, 1987; Curio, 1978; Fichtel et al., 2005; Tamura,
1989; Templeton et al., 2005] that can be explained as altruistic behavior, part of
parental care, or selfish behavior that serves to deter, confuse, and discourage a
predator from undertaking an attack [Curio, 1975, 1978; Curio et al., 1978;
Ficken, 1989, Zahavi & Zahavi, 1997]. These strategies are not mutually
exclusive, and diurnal animals usually employ a combination of these strategies
to avoid predators and cope with predator attacks.
Much less is known about antipredator behavior in nocturnal birds and
mammals. For example, one-third of all primate species are nocturnal and smallbodied, and face a high predation risk [Hart, 2000; Isbell, 1994; Janson, 2003;
van Noordwijk et al., 1993], but their antipredator behavior has rarely been
studied directly. For example, small body size and nocturnality have been
suggested to be a morphological adaptation to predation risk [Clutton-Brock &
Harvey, 1977]. Terborgh and Janson [1986] pointed out that antipredator
strategies available for diurnal primates that rely on early detection and warning
of approaching predators may not be available to nocturnal animals. Solitariness
and crypsis were considered to be viable alternative strategies.
Am. J. Primatol. DOI 10.1002/ajp
Antipredator Strategies in Sportive Lemurs / 613
However, the last decade of intensified research on nocturnal primates has
shown that they are not as solitary and cryptic as previously suggested. First,
several species that were thought to be solitary are in fact pairliving (Cheirogaleus medius [Müller, 1998; Fietz, 1999], Lepilemur edwardsi
[Rasoloharijaona et al., 2000], Phaner furcifer [Schülke & Kappeler, 2003], and
Lepilemur ruficaudatus [Zinner et al., 2003]) or exhibit even more complex types
of social organization (Tarsius spectrum [Gursky, 2000]). Second, anecdotal
reports of snake encounters in several species included conspicuous mobbing
behavior [Bearder et al., 2002; Gursky, 2001; Schülke, 2001] (Eberle, personal
communication). Also, alarm calls and mobbing in response to raptor dummies
and terrestrial predators have been reported in spectral tarsiers (Tarsius
spectrum) [Gursky, 2003b] and southern lesser galagos (Galago moholi) [Bearder
et al., 2002]. Thus, some nocturnal species rely on early warning and others show
mobbing behavior. Furthermore, some of these species give loud calls during the
night [Bearder et al., 2002; Rasoloharijaona et al., in press; Schülke & Kappeler,
2003] (Hilgartner et al., unpublished results), thereby advertising their presence
not only to conspecifics but also to predators. Thus, solitariness and crypsis can no
longer be considered as global, main antipredator strategies of all nocturnal
primates.
In an attempt to shed additional light on the antipredator behavior of
nocturnal primates, I studied antipredator strategies in red-tailed sportive lemurs
(Lepilemur ruficaudatus). These small-bodied (o1 kg), nocturnal lemurs are
organized in pairs and give birth once a year to a single offspring [PetterRousseaux, 1962; Zinner et al., 2003; Hilgartner et al., in press]. Sportive lemurs
are preyed upon by several predators, including fossas (Cryptoprocta ferox), longeared owls (Asio madagascariensis), and snakes (Acrantophis sp.) at night, as well
as during the day when they rest in their tree holes [Goodman et al., 1993;
Rasoloarison et al., 1995; Sussman, 1999] [Hilgartner et al., in press]. Fortuitous
observations have also revealed that Harrier hawks (Polyboroides madagascariensis) prey on lemurs by pulling them out of tree holes during the day [Schülke &
Ostner, 2001], and that fossas attempt to prey on sportive lemurs by opening the
tree hole (Dammhahn and Razafindrasamba, personal communications). In both
situations the sportive lemurs produced loud distress calls (barks), a call that is
also given during any disturbance at the tree hole. For example, Hilgartner
(personal communication) observed that barks were given when one of the pair
partners jumped on a tree in which the other pair partner was already resting in
the tree hole. Barks may therefore be a signal that is directed to a predator or
disturber that signals them to give up their attempt.
The sportive lemurs in this study were part of a long-term study and were
individually known and equipped with radiocollars [Zinner et al., 2003]
[Hilgartner et al., in press]. During the 4 study years, 16 out of 45 marked adult
individuals became the most likely victims of predation. Predator species could be
determined in 10 cases by predator-specific leftovers or bite marks of victims
[Hilgartner et al., in press]. Seven individuals were killed by a fossa, one by a
Harrier hawk, and two by a boa. Although during the 4 study years the predation
rate on adult individuals was about 36%, and the sportive lemurs were constantly
observed, no predation attempt or predator encounters were observed at night.
The absence of predators may reflect the fact that human observers at night
sometimes might defer predators from attacking.
To elicit antipredator behavior and potential alarm calls, I presented the
sportive lemurs with the vocalizations of two predators (fossa and Harrier hawk)–
a design that has successfully been used in studies of other sympatric lemurs
Am. J. Primatol. DOI 10.1002/ajp
614 / Fichtel
[Fichtel & Kappeler, 2002]. Additionally, I presented the sportive lemurs
with playbacks of their own barks. I used barks of unknown individuals to avoid
confounding pair-specific responses. As a control, I used territorial calls of
sympatric fork-marked lemurs (Phaner furcifer). Since alarm calls are considered
to be an investment in kin or mates, I studied only individuals that lived in pairs
and had offspring. If these sportive lemurs are not only cryptic but also rely on
early detection and warning of predators, I expected them to give alarm calls, scan
the sky, and climb down after the presentation of the calls of the Harrier hawk.
I expected that after playbacks of fossa calls they would give alarm calls,
scan the ground, and climb up. In response to the presentation of their own barks,
I expected them to scan the ground, where the loudspeaker was placed, to locate
the source of disturbance, and to climb up or flee. In response to the control,
I expected the sportive lemurs to scan around and stay.
MATERIALS AND METHODS
Study Site and Subjects
This study was conducted in Kirindy Forest, western Madagascar, where
the German Primate Center operates a research station within a forestry
concession operated by the Centre Formation Professionelle Forestière de
Morondava [Sorg et al., 2003], in March and April 2005. Several sportive lemurs
in the 60-ha study area were part of an ongoing study and had been equipped with
9-g radiocollars (Biotrack; Wareham, Dorset, UK) that weighed less than 3% body
mass. The individuals were observed regularly at night between 2000 and 2004,
and were therefore well habituated to human presence. Seven individuals (three
males and four females) that lived with a pair-partner and had at least one
offspring from the last birth season (about 6 months old) were chosen as
focal subjects.
Playback Stimuli
Playback stimuli of predators were made with the vocalizations of fossas
(Cyptoprocta ferox) and Harrier hawks (Polyboroides radiatus) (Fig. 1). Spectrograms were made with Avisoft SASLAB Pro (Berlin, Germany) (1024-point
Fourier transformation, Hanning window function, 32,000-kHz sampling rate
resulting in a 31-Hz frequency resolution, and 8-ms temporal resolution, with
75% window overlap). Recordings of sportive lemur barks were made during
disturbances by humans (i.e., approaching the tree hole and knocking on the
tree). Additionally, I used territorial vocalizations of the fork-marked lemur
(Phaner furcifer) (Fig. 1) as a control. To avoid pseudoreplication [e.g., Kroodsma,
1989; Wiley, 2003], I used different vocalizations as playback stimuli (fossa: n 5 4;
Harrier hawk: n 5 5; sportive lemur barks: n 5 7; fork-marked lemur: n 5 7).
Vocalizations of the Harrier hawk and the fossa were recorded at the study site
and at Duisburg Zoo, Germany, using a Sony WM TCD-100 DAT recorder
(frequency response 5 20–20,000 Hz) and a Sennheiser directional microphone
K6 power module and ME66 recording head with an MZW66 pro windscreen.
Bouts of vocalizations with a duration of approximately 471 sec were duplicated
three times with 5-sec intervals of silence in between, using Cool Edit 2000
(Syntrillium, Phoenix, AZ), and used as playback stimuli. Playback amplitudes were calibrated by ear to match the amplitude of naturally occurring
vocalizations.
Am. J. Primatol. DOI 10.1002/ajp
Antipredator Strategies in Sportive Lemurs / 615
Fig. 1. Spectrograms of calls of a fossa, a Harrier hawk, and a fork-marked lemur, and sportive
lemur barks used as playback stimuli.
Playback Procedures
The vocalizations were played back with a Sony Professional Walkman and a
Nagra DSM amplifier-loudspeaker hidden behind a bush or tree at a distance of
about 5 m. Only animals engaged in relatively quiet activities, such as foraging,
resting, or self-grooming were chosen as focal subjects. All subjects were tested
once with each of the four stimuli. Since Harrier hawks are active from dawn to
dusk, playback experiments with vocalizations of the Harrier hawk were
conducted at dusk after the sportive lemurs had left their tree holes. All other
playback stimuli were presented during the night in a randomized but counterbalanced order. Each playback stimulus was tested only once per night and pair.
To measure the occurrence, frequency, and duration of subject responses,
I documented them in real time on a Sony Professional Walkman connected to the
directional microphone 1 min after the onset of each playback. Recordings were
transferred onto a computer using Cool Edit 2000 (Syntrillium, Phoenix, AZ). As
shown in earlier studies of other lemur species [Fichtel, 2004; Fichtel & Kappeler,
2002], 1 min of observation after the onset of the playback stimulus is sufficient to
record immediate startle responses and potential alarm calls, which are the main
behavioral patterns that characterize the alarm-call system of a given species.
Data Analyses
Using real-time spectrograms, I scored the occurrence, frequency, and
duration of the following responses within the first minute after the onset of a
playback: 1) vocalization: occurrence; if yes, call type; 2) stay: subject did not move
away, but changed its looking direction; 3) look: duration of looking in different
directions (up or down); 4) scan: head movements of more than 451 in any
direction; 5) startle: subject moved away (r10 m); 6) flee: subject moved out of
Am. J. Primatol. DOI 10.1002/ajp
616 / Fichtel
sight (410 m); 7) other: subject foraged or self-groomed. In addition, I measured
the latency between the onset of the playback and the first of these possible
responses.
For a comparison of latency, duration of looking direction, and number of
scans among playback stimuli, I used the RMwV 1.0-test [Mundry, 1999]. This
permutation test is a variant of a Friedman one-way analysis of variance
(ANOVA) that accepts missing values. The distribution of startle responses,
and the number of individuals engaged in other activities across treatments
were compared with Cochran’s exact test. In addition, I used a binomial test
to compare startle responses. I classified them as either ‘‘appropriate’’ or
‘‘inappropriate.’’ An appropriate response to playback experiments with calls of
predators was to flee in the opposite direction from which the simulated predator
would normally attack. For example, an appropriate response to calls of the fossa
was to flee or climb up. An inappropriate response to calls of the Harrier hawk
was to climb up.
RESULTS
All playback treatments elicited at least one of the possible behavioral
responses from the sportive lemurs. Their mean latency of response varied
between 2.2971.63 sec after the presentation of calls from a fossa, and
8.17711.78 sec after the presentation of calls from a fork-marked lemur
(Fig. 2). However, there was no significant difference in latency across playback
stimuli (RMwV 1.0: P 5 0.255).
No individual responded with vocalizations after the different playback
stimuli were broadcast (binomial test for each of the four stimuli: n 5 7,
P 5 0.016). However, sportive lemurs responded by changing their location
(Cochran: treatment-control: Q 5 14.727, P 5 0.002). Following playback
experiments with sportive lemur barks, the subjects showed the strongest
response and five individuals fled, one climbed up, and one stayed stationary.
Thus, all startle responses were appropriate (binomial test: n 5 7,
P 5 0.031; Table I). After the presentation of the fossa calls, only four
individuals startled and three showed appropriate responses. One individual
Fig. 2. Mean (7SEM) latency between the onset of the respective playback stimulus and the first
response of sportive lemurs (n 5 7) across the different playback treatments.
Am. J. Primatol. DOI 10.1002/ajp
Antipredator Strategies in Sportive Lemurs / 617
TABLE I. Behavioural Responses of Sportive Lemurs to Playback Experiments
Startle
Treatment
Harrier hawk
Fossa
Barks
Fork-marked lemur
Flee
Up
Down
Stay
N Individuals grooming or foraging
0
1
5
0
0
2
1
0
0
1
0
0
7
3
1
7
1
1
0
5
Number of individuals that showed one of the several responses, remained stationary or that started to groom or
forage during the playback experiment (‘‘appropriate’’ escape strategies are in bold; see Results for detailed
definitions).
fled, two climbed up, one climbed down, and three remained stationary
(binomial test: n 5 7, P 5 0.625; Table I). In response to the presentations of
Harrier hawk and fork-marked lemur calls, all of the individuals remained
stationary (Table I).
However, after the presentation of the control, five individuals were engaged
in other activities, such as grooming or foraging. Only one individual was engaged
in activities other than scanning the environment after playbacks of Harrier
hawk and fossa calls, and none after the presentation of the barks (Table I,
Cochran: treatment-control: Q 5 11.8, P 5 0.008).
After the calls of the Harrier hawk were broadcast, the individuals spent
more time looking up than they did after the broadcast of fossa calls, their own
barks, or calls of the fork-marked lemur (RMwV 1.0: P 5 0.001; Fig. 3). After the
fossa calls and barks were broadcast, the control individuals spent more time
looking down than they did after the broadcast of the calls of the Harrier hawk
(RMwV 1.0: P 5 0.045; Fig. 3). Thus, a stimulus-specific reaction was detectable in
the animals’ looking direction, i.e., they looked in the direction from which the
respective predator would normally attack. Individuals also scanned the
environment more often after fossa calls and sportive lemur barks were broadcast
than after the calls of the Harrier hawk and the fork-marked lemur were
broadcast (RMwV 1.0: P 5 0.002; Fig. 4).
DISCUSSION
The results of this study show that although the sportive lemurs associated
vocalizations of predators with a potential attack, they did not respond with alarm
calls to this perceived risk. In response to the calls of the Harrier hawk, the
sportive lemurs remained stationary and scanned the sky, but not the ground
where the sound source was hidden, clearly indicating that they associated the
calls of the Harrier hawk with the presence of the raptor. In response to the calls
of the fossa, they fled or climbed up, scanned the ground, and increased their scan
rate. Thus, after the presentation of predator calls, the sportive lemurs scanned
the direction from which the simulated predator would normally attack, and fled
in the opposite direction. After hearing sportive lemur barks, individuals showed
the strongest response. They fled or climbed up, scanned the ground, and
increased their scan rate, indicating that they associate a potential danger with
these calls. In response to the control, they remained stationary, scanned around,
and foraged or groomed themselves, indicating that they did not associate any
danger with these calls.
Am. J. Primatol. DOI 10.1002/ajp
618 / Fichtel
Fig. 3. Mean (7SEM) of the percentage of time sportive lemurs (n 5 7) spent looking up or down
after the presentation of the four playback stimuli.
Fig. 4. Mean (7SEM) of number of scans per minute of sportive lemurs (n 5 7) after the
presentation of the four playback stimuli.
Sportive lemurs showed escape responses after the presentation of the
fossa calls, but not after the presentation of the calls of the Harrier hawk.
Since predation attempts of Harrier hawks presumably occur more often during
the day, when sportive lemurs take a sunbath while sitting in or next to their
tree hole, it may be advantageous to stay, scan the sky to locate the hawk, and,
Am. J. Primatol. DOI 10.1002/ajp
Antipredator Strategies in Sportive Lemurs / 619
in case of an attack, to descend into the tree hole. However, differences in
strategies to escape hawk and fossa predation attempts may also be explained by
taking their different hunting strategies into account. Because raptors usually
hunt silently and make sudden dives at their prey, it may be advantageous for
sportive lemurs to remain stationary to locate the raptor because they would not
have a chance to locate the raptor while fleeing. In contrast, it may be
advantageous to flee during an attack by a fossa because these animals make
more noise while approaching, allowing the prey to locate the predator by acoustic
cues while fleeing. However, diurnal primates usually flee downwards in response
to a raptor attack, even though they cannot locate the silently attacking raptor.
Group-living animals benefit from dilution and confusion effects [Hamilton,
1971], which makes flight responses for a single individual more advantageous.
The sportive lemurs did not vocalize after predator calls and their own barks
were broadcast, indicating that they do not have an early warning system.
However, barks are directed toward predators, during disturbances at the tree
hole, and rarely toward conspecifics, which suggests that they are primarily
directed toward predators or disturbers. In response to playback experiments
with barks, sportive lemurs showed the strongest response and fled. Either
sportive lemurs associate a danger with barking conspecifics and flee, or they flee
because they associate an intruding conspecific with the barks. However, the
latter explanation is less likely because I used barks of strange sportive lemurs,
simulating a strange individual advertising a danger within the territory of the
experimental subject. Because no sportive lemur approached the loudspeaker in
order to seek a confrontation with the intruder, I conclude that barks have an
alarm function.
Other playback experiments with territorial calls of sportive lemurs that
were conducted to simulate intruders never resulted in escape responses
(Hilgartner et al., unpublished results), making flight an implausible response
to intruders. Moreover, scan rates after calls of predators or barks were two to
three times higher than after playback experiments with simulated intruders
(Hilgartner et al., unpublished results). Interestingly, the sportive lemurs never
approached the loudspeaker after presentations of barks in order to jointly mob
the potential predator. The facts that sportive lemurs’ social activities are
predominantly characterized by avoidance of both pair-partners and neighbors,
and the rare interactions of pair-partners are mainly of an aggressive nature
(Hilgartner et al., unpublished results) may explain why jointly mobbing
predators is an implausible antipredator strategy for this species. This is in
contrast to the previously observed joint mobbing behavior of pair-living forkmarked lemurs, during which family members were attracted by mobbing calls
given toward a snake [Schülke, 2001]. However, social interactions between pairpartners occur at a higher rate in fork-marked lemurs than in sportive lemurs,
and are also of affiliative nature, suggesting that social cohesion among pairpartners may influence communal mobbing behaviors. Moreover, during these
encounters the family members of the fork-marked lemurs were not the only ones
attracted by the calls–a Coquerel dwarf lemur (Mirza coquereli) also joined the
mobbing [Schülke, 2001]. This observation supports the notion that mobbing
serves a deterrence function.
But why do sportive lemurs give loud barks during disturbances at their tree
hole? Barks are given in response to conspecifics and predators, but also more or
less ‘‘blindly’’ (i.e., when the sportive lemur is resting in a tree hole and cannot
see the source of the disturbance), and may have a pursuit-deterrence function.
Pursuit-deterrence signals are given in response to predators that rely on an
Am. J. Primatol. DOI 10.1002/ajp
620 / Fichtel
ambush hunting strategy, to signal the predator that pursuit is likely to be
unprofitable. Since the pursuit of prey imposes similar costs on a predator, it
sometimes pays for a predator to take note of the signal and give up [Woodland
et al., 1980]. Although the sportive lemur may have only a small chance of
escaping, such signals may still successfully deter a fossa, since no instances of
tree holes being opened by a fossa have been reported to date (Hilgartner,
personal communication). However, before we can conclude that barks are in fact
pursuit-deterrence signals, further studies on predator-prey interactions of the
fossa are required.
Sportive lemurs defend relatively small territories (about 1 ha) and
their barks are loud enough to be heard within the territory by pair-partners
and offspring. Sportive lemurs usually rest alone in their tree holes, and
only females and their infants share them regularly for the first 2 months
after the birth of the infant [Hilgartner et al., in press]. Barks given by
resting males or females may thus serve to warn kin and the respective pairpartner [Hogstad, 1995]. Barks given by females may also be involved
in social transmission of dangers to their offspring [Bartecki & Heymann,
1987; Curio et al., 1985; Srivastava, 1989]. Moreover, sportive lemurs also
spend some time during the day out of their tree holes to take sunbaths or to
forage. In this context the warning function of barks is of vital importance for
pair-partners and kin when they are out of a shelter. Thus, sportive lemurs barks
are general alarm calls that do not indicate any specific threats, are also given
during aggressive interactions with conspecifics (see also Fichtel and Kappeler
[2002]), and may serve to warn kin and pair-partners. Barks are primarily
directed to predators or threatening conspecifics, and may serve to confuse
predators/disturbers or to recruit other predators to increase the likelihood
of fleeing.
Reports on usage of alarm calls in other nocturnal primates suggest that
they also use general alarm calls, that are, alarm calls given towards predators,
but also during aggressive interactions with conspecifics. For example, gray
mouse lemurs (Microcebus murinus) give whistles in response to snakes or snake
dummies, but these calls are also used during various interactions with
conspecifics, including aggression [Stanger, 1995; Zimmermann, 1995; Zimmermann et al., 2000]. Southern lesser galagos emit alarm calls in response to various
predators, which are also given during aggressive interactions between
conspecifics [Bearder et al., 2002]. In contrast, Gursky [2003b] reported different
alarm calls given by two mother–infant pairs of spectral tarsiers toward raptor
and snake models and raptor calls, respectively. However, since these studies
involving playback experiments with alarm calls did not record the behavioral
responses of conspecifics, the possible functions of these calls remain elusive for
the time being.
Reports on predator encounters in nocturnal primates reveal that they
show mobbing behavior in response to predators, indicating that mobbing
predators is an effective antipredator strategy for both diurnal and nocturnal
species. Most observations on the mobbing behavior of nocturnal species have
been made during encounters with snakes [Bearder et al., 2002; Gursky, 2001,
2003b; Schülke, 2001] (Eberle, personal communication). Gursky [2005] studied
mobbing behavior in spectral tarsiers experimentally by presenting snake
models and conducting subsequent playback experiments with mobbing calls,
and concluded that mobbing in tarsiers may also have a pursuit-deterrence
function. A recent study of predator–prey communication between snakes
and rodents revealed that snakes moved away from ambush hunting sites after
Am. J. Primatol. DOI 10.1002/ajp
Antipredator Strategies in Sportive Lemurs / 621
they received mobbing displays from their prey species [Clark, 2005]. This
clearly indicates that predators respond to displays by giving up their ambush
prey in the vicinity of the signaler, and supports the notion that mobbing may
be a form of predator–prey communication. Moreover, a comparative analysis
on the evolution of alarm calls in rodents suggests that alarm-calling evolved
in diurnal species, probably as a means of communicating with predators [Shelley
& Blumstein, 2004]. Because nocturnal strepsirrhines are considered to be the
most evolutionarily basal-living primates, representing a phylogenetic link
between basal mammals and anthropoid primates [Martin, 1990], and many
strepsirrhines appear to mob predators, these calls may be the ancestral form of
alarm-calling.
As mentioned above, antipredator behavior can be broadly classified as
strategies that reduce the risk of detection (precautions) and strategies that take
effect once potential prey have detected a predator. This study focuses on the
latter strategy for sportive lemurs. However, nocturnal animals may also reduce
their vocalizations, as well as foraging and moving activities, during periods of
bright moon as a precaution to avoid the risk of detection by predators [reviewed
in Caro, 2005]. In contrast, a previous study reported that nocturnal Tammar
wallabies (Macropus eugenii) were more active and allocated less time to
antipredator vigilance during experimentally induced higher levels of nocturnal
illumination [Biebouw & Blumstein, 2003]. Similarly, in many nocturnal
primates lunar philia, rather than lunar phobia, seems to be the rule [Bearder
et al., 2002; Erkert & Grober, 1986; Gursky, 2003a; Nash, 1986; Wright, 1997].
Preliminary data on a closely related species, the white-footed sportive lemur
(Lepilemur leucopus), suggest that moonlight does not affect activity patterns
[Nash, 2000]. Vigilance, which was measured in this study as an increase in scan
rates after playbacks with predator vocalizations and barks, seems to be an
important antipredator behavior of sportive lemurs. Vigilance is also a precaution
used by diurnal primates to reduce the risk of detection by predators. Thus,
further studies on activity patterns and vigilance are needed not only to complete
our understanding of red-tailed sportive lemur antipredator strategies in
particular, but also to illuminate additional antipredator strategies employed by
nocturnal primates in general.
ACKNOWLEDGMENTS
I thank Mme. Olga Ramilijaona and M. Daniel Rakotondravony at the
University of Antananarivo, the Comission Tripartite de Direction des Eaux
et Forêts, and the C.F.P.F. Morondava for their authorization and support of this
study. I thank Mario and Roland Hilgartner for their assistance during playback
experiments in the field. I am especially grateful to Roland Hilgartner for
his companionship in the field and many discussions about the very ‘‘sportive’’
lemurs. Comments by M. Dammhahn, R. Hilgartner, P. Kappeler, D. Blumstein,
and an anonymous referee improved an earlier version of this manuscript.
The experiments complied with the current laws of the country in which they
were performed.
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