Avoiding predators at night antipredator strategies in red-tailed sportive lemurs (Lepilemur ruficaudatus).код для вставкиСкачать
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.firstname.lastname@example.org 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  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 ), 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  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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