behavior in primates , article

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Anti-Predator Behaviour in a Nocturnal Primate, the Grey MouseLemur ( Microcebus murinus)

Moritz Rahlfs* & Claudia Fichtel* Division of Wildlife Ecology, Research Institute for Forest Ecology and Forestry, Trippstadt, Germany

Department of Behavioral Ecology and Sociobiology, German Primate Center, Gottingen, Germany

Introduction

Predation is a major evolutionary force that has

resulted in a variety of adaptations to avoid and deal

with predators (Lima & Dill 1990; Caro 2005). Anti-

predator behaviour can be broadly classified into

strategies and tactics employed before and after

encountering predators. The former include predator-

sensitive foraging, vigilance and formation of groups

or mixed species associations (Elgar 1989; Caro 2005).

Animals thereby benefit from predator confusion, the

selfish herd and dilution effects as well as from

improved detection by predators (Hamilton 1971;

Lima 1995; Ruxton et al. 2007). After detecting pre-

dators, potential prey can either flee, confront andor

mob the predator, and they can give alarm calls.

Mobbing is a common behaviour in this context in

mammals and birds (Curio et al. 1978; Tamura 1989).

Alarm calls are given when predators are detected

and signal the presence of predators to conspecifics

(Caro 2005). Potential functions include pursuit

deterrence (Caro 1995), signalling predator size and

location (Evans & Marler 1995; Blumstein & Armitage

1997; Templeton et al. 2005) as well as identity to

conspecifics (Seyfarth et al. 1980; Zuberbuhler et al.

1999b; Manser 2001; Fichtel & Kappeler 2002).

In principle, the preys circadian activity has a

strong effect on the types of potential anti-predator

Correspondence

Claudia Fichtel, Department of Behavioral

Ecology and Sociobiology, German Primate

Center, Kellnerweg 4, 37077 Gottingen,

Germany.

E-mail: [email protected]

Received: October 14, 2009

Initial acceptance: November 27, 2009

Final acceptance: January 27, 2010

(J. Wright)

doi: 10.1111/j.1439-0310.2010.01756.x

Abstract

Although one-third of all primates are nocturnal, their anti-predator

behaviour has rarely been studied. Because of their small body size, in

combination with their solitary and nocturnal life style, it has been

suggested that they mainly rely on crypsis to evade predators. However,

recent studies revealed that nocturnal primates are not generally cryptic

and that they exhibit predator-specific escape strategies as well as alarm

calls. In order to add to this new body of research, we studied anti-pred-

ator strategies of nocturnal grey mouse lemurs experimentally. In order

to elicit anti-predator behaviour and alarm calls, we conducted experi-

ments with a carnivore-, snake- and raptor model. We also conducted

playback experiments with mouse lemur alarm calls to characterize their

function. In response to predator models, they exhibited a combination

of anti-predator strategies: in response to carnivore and snake models,

mouse lemurs monitored the predator, probably to assess the potential

risk that emanates from the predator. In response to raptor models they

behaved cryptically and exhibited freezing behaviour. All mouse lemurs,

except one individual, did not alarm call in response to predator models.In addition, during playback experiments with alarm calls, recorded

during real predator encounters, mouse lemurs did not emit alarm calls

nor did they show any escape behaviour. Thus, as in other nocturnal

primatesmammals, mouse lemurs do not seem to rely on routinely

warning of conspecifics against nearby predators.

Ethology

Ethology 116 (2010) 429439 2010 Blackwell Verlag GmbH 429

ethology international journal of behavioural biology


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strategies. If alarm calling evolved to communicate

with predators, animals should alarm call only when

it is possible to locate and track predators visually,

because visual predator detection may more accu-

rately assess the risk of predation (Lima 1988a,b).

Hence, it has been suggested that alarm-calling spe-cies are diurnal and that alarm calling should be rare

or absent in nocturnal species (Terborgh & Janson

1986; Stanford 2002).

Among mammals, anti-predator behaviour of

primates has been studied in particular detail

(Cheney & Wrangham 1987; Caro 2005; Fichtel in

press). In primates, diurnal species usually rely on a

combination of anti-predator-strategies, such as vigi-

lance, grouping, predator deterrence, mobbing and

early warning of predators including alarm calls

(Seyfarth et al. 1980; Zuberbuhler et al. 1999a; b;

Fichtel & Kappeler 2002; Fichtel in press). However,

much less information is available about alarm call

behaviour and anti-predator strategies in nocturnal

primates, although one-third of all primates are

nocturnal, small bodied and, thus, face a high preda-

tion risk (Isbell 1994; Janson 2003; Hart 2007).

Small body size and nocturnality have, for example,

been suggested to be adaptations to predation risk

(Clutton-Brock & Harvey 1976). Because anti-preda-

tor 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 as viable

alternative strategies (Terborgh & Janson 1986).However, the last decade of intensified research

on nocturnal primates revealed that they are not as

solitary and cryptic as previously thought. First, sev-

eral species thought to be solitary are in fact pair-liv-

ing (Kappeler in press). Second, anecdotal reports of

snake encounters in several species documented

conspicuous mobbing behaviour (Gursky 2001;

Schulke 2001; Bearder et al. 2002; Eberle & Kappel-

er 2008), indicating that nocturnal primates not only

rely on crypsis by hiding and freezing in front of

snakes. Consequently, anti-predator behaviour of

some nocturnal primates has been studied in recent

years experimentally in order to shed light on their

anti-predator strategies as well as the usage and

function of their alarm calls. For example, nocturnal

pair-living red-tailed sportive lemurs (Lepilemur rufi-

caudatus) did not respond with alarm calls after play-

back experiments with vocalizations of their main

predators but did show adaptive escape strategies

that corresponded to the different hunting styles of

the simulated predators. In response to raptor calls

they showed freezing behaviour, contrarily, in

response to carnivore calls they scanned the ground

and climbed up the tree. However, during disturban-

ces at sleeping sites, when carnivores, i.e. the fossa,

tried to break open the sleeping site, other red-tailed

sportive lemurs tried to enter an already occupied

sleeping site, or when humans manipulated sleepingsites, red-tailed sportive lemurs responded with

alarm calls, indicating that these alarm calls are

primarily directed at the predatoraggressor. Thus,

red-tailed sportive lemurs do not seem to rely on

early warning of predators and alarm calls seem to

be directed at predators or aggressors (Fichtel 2007).

Spectral tarsiers (Tarsius spectrum), which are second-

arily nocturnal (Martin & Ross 2005), produce one

type of alarm call in response to aerial predator

models and another one in response to several

terrestrial predator models, i.e. civets, snakes and

lizards. In response to raptor models, they froze and

sometimes mobbed the raptor model, whereas carni-

vore and snake models elicited upwards climbing

and mobbing (Gursky 2006, 2007). Thus, nocturnal

primates also seem to rely on a combination of anti-

predator strategies. Solitariness and crypsis can

therefore no longer be considered as the only, main

anti-predator strategy of all nocturnal primates.

Furthermore, observations of solitary nocturnal

grey mouse lemurs revealed that alarm calls of an

individual caught by a snake recruited conspecifics

that cooperatively mobbed and attacked the snake

until the caught individual could escape (Eberle &

Kappeler 2008). Although grey mouse lemurs aremainly solitary during their active period, they inhabit

extensively overlapping home ranges, and females,

but sometimes also males, form sleeping groups with

closely related kin during daytime (Eberle & Kappeler

2002). Thus, the underlying socio-genetic structure

may explain the observed cooperative anti-predator

behaviour in this species (Eberle & Kappeler 2008).

In order to gain further insight into the anti-predator

strategies as well as the usage and function of grey

mouse lemur alarm calls, we conducted several field

experiments. Firstly, we exposed mouse lemurs to

three predator models to elicit anti-predator beha-

viour and alarm calls. Secondly, we conducted play-

back experiments with mouse lemur alarm calls to

study potential function of these calls.

Methods

Study Site and Study Animals

This study was conducted in Kirindy Forest, a dry

deciduous forest in Western Madagascar (Sorg et al.

Anti-Predator Strategies in Nocturnal Grey Mouse Lemurs M. Rahlfs & C. Fichtel

430 Ethology 116 (2010) 429439 2010 Blackwell Verlag GmbH


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2003). Grey mouse lemurs at Kirindy are preyed

upon by numerous predators, including carnivores:

fossa (Cryptoprocta ferox), narrow-striped mongoose

(Mungotictis decemlineata), etc., snakes: the colubrid

snake (Ithycyphys miniatus), Madagascar tree boa

(Sanzinia madagascariensis) and Madagascar ground boa ( Acantrophis madagascariensis), nocturnal birds of

prey: the Madagascar long-eared owl ( Asio madaga-

scariensis) and the barn owl (Tyto alba) and diurnal

birds of prey: Hensts goshawk ( Accipiter henstii)

(Rasoloarison et al. 1995; Goodman 2003). Diurnal

raptors either prey upon mouse lemurs by pulling

them out of the tree hole or prey upon them at

dawn or dusk, where both species are active (Good-

man 2003).

Eight adult mouse lemurs (five males and three

females) were captured with Sherman live-traps.

During the experimental period, they were kept

individually in 1 m3 cages (on an average for 3 wk)

at the Kirindy research station. Animals were fed

with fruits and insects and water was provided ad

libitum. Predator model and playback experiments

were conducted in an experimental cage (Fig. 1b)

situated within the forest, an area that is inhabited

by grey mouse lemurs and from which we caught

three individuals. The experimental cage was divided

into two compartments (Fig. 1a); the experimental

compartment was fitted with a matrix of branches

and twigs and the other one was used to set up the

technical equipment.

Experimental Procedure

Before the start of experiments, each individual was

released at least once into the cage for 30 min with-

out exposing them to any treatment in order to

habituate them to the new environment. Experi-

ments were started after sunset, except the raptor

design, which was always presented at dusk in order

to ensure that the lighting conditions were sufficient

to discover fast moving objects. Animals were trans-

ported to the experimental cage in Sherman traps

and then released into the experimental cage. Exper-

iments were started after mouse lemurs showedneutral behaviour (i.e. foraging, grooming or scent-

marking; Table 1), which was usually within 10

15 min after releasing them. Responses to predator

and control models were videotaped with a hand-

held digital video camera (Sony DCR-PC100E, Sony

Deutschland GmbH, Koeln, Germany) with a night

shot function and an additional infrared spotlight.

Vocalisations were recorded with the camera and a

Toshiba Satellite Pro laptop (Toshiba Europe GmbH,

Germany) and the software AVISOFTRECORDER

v.2.96 (Avisoft, Berlin, Germany). Connected to the

laptop was a Polaroid electrostatic transducer 600

Series microphone via an Avisoft-UltraSoundGate

116 soundcard (sampling rate: of 500 kHz at 16 bit).

Responses of mouse lemurs were audio- and video-

recorded until they exhibited neutral behaviour

(Table 1). Each individual participated in one experi-

ment per night and nine experiments in total (six

predatorcontrol model experiments and three play-

back experiments). Each subject was tested once

with each predatorcontrol model and once with the

three playback stimuli. Immediately after the end of

each experiment, animals were recaptured using a

Sherman trap and returned to their housing cage. In

the night of the last experiment, individuals werereleased at the site where they have been originally

caught.

Predator Model and Control Experiments

Two observers conducted the predatorcontrol model

experiments; one concealed observer operated the

(a) (b)

Fig. 1: (a) Schema experimental cage. The western compartment housed the technical equipment. Experiments were conducted in the eastern

compartment. Dashed line: path of fossa design presentation; dotted line: path of snake design presentation; continuous line: path of raptor

design presentation. Stars indicate position of stimulus operator for each design. Position of camera and loudspeaker indicated by symbols.

(b) Picture of the semi natural enclosure; view from northeast. In the foreground: shelf for snake stimulus presentation.

M. Rahlfs & C. Fichtel Anti-Predator Strategies in Nocturnal Grey Mouse Lemurs



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predator models outside the experimental cage, and

the second observer recorded the animals vocal and

behavioural responses from within the cage

(Fig. 1a). Each design comprised a predator model

(fossa, snake or raptor) and a corresponding control

(Fig. 2). The predator model and the control of each

design were presented in the same manner. Before

and after the presentation, all stimuli were concealed

from the test subjects view. Experimental runs wereset up before the animals were released into the

cage. Stimuli were presented in a randomised order.

Predator models and respective controls, for example

snake and snakecontrol, were never presented on

the same or two consecutive nights. There was at

least one night without any stimuli presentation or

presentation of a different stimulus in-between.

Fossa Design

The fossa model was a life-sized model made out of

straw (approx. 100 cm long and 55 cm high;

Fig. 2A). The fossa control was a cushion (approx.

55 cm 45 cm 15 cm; Fig. 2a). The fossa model,

respectively, the control, was hooked onto a track

Table 1: Definition of behavioural categories scored from video

recordings

Category Definition

Alarm calls Any vocalization given in response to the

presented predatorcontrol models or

mouse lemur vocalizations

Flight Sudden movements into the opposite direction

of the presented stimulus

Freeze Abrupt stationary position without movement of

any body parts

Orientation Orientation of body axis while stationary

Locomotion Locomotion in any direction more than one body

length, continuous event if intervals between

locomotion 45

in any direction

(A)

(B)

(a)

(b)

(C) (c)

0.5 m0.5 m

0.5 m 0.5 m

0.5 m 0.5 m

Fig. 2: Predator model and control: fossa (A),

fossa control (a), snake (B), snake control (b),

raptor (C), raptor control (c).




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cable outside the cage and concealed. At the start of

the experiment, the stimulus was pulled along

outside of the experimental part of the enclosure

(Fig. 1a) and again concealed in its final position.

Presentation time of the fossa model accounted in

median for 73 s (25th: 61.9 s, 75th: 83.8) and forthe control in median 61.5 s (25th: 52 s, 75th:

69.9 s).

Snake Design

The snake model was a rubber snake (approx.

130 cm long, 3 cm in diameter; Fig. 2B). As a

control, we used a knotted cloth (approx. 100 cm

long, 5 cm diameter; Fig. 2b). These stimuli were

placed on a shelf surrounding the cage (70 cm above

the ground) on three sides (Fig. 1b) and attached to

a string. By pulling the string (as indicated in

Fig. 1a) the stimulus moved around the cage. When

it reached the operator, it was hidden behind the

operators back. Presentation time of the snake

model accounted in median for 131.6 s (25th:

116.4 s, 75th: 138.9 s) and for the control in median

90 s (25th: 79.5 s, 75th: 97.7 s).

Raptor Design

In the raptor design, we presented the mouse lemurs

a wooden silhouette of a raptor, (74 cm 44 cm;

Fig. 2C) as a control we used a cardboard circle

(52 cm B; Fig. 2c). The stimuli were attached to twostrings that led to a gibbet 4 m above the cages

centre. This allowed either stimulus to swing freely

approx. 50 cm above the cages ceiling in a pendu-

lum fashion. After uncovering the stimulus, it was

presented twice with a 5-s interval in-between.

Afterwards, it was caught, concealed and fixated in

its original position. Presentation time of the raptor

model accounted in median for 11.7 s (25th: 10.8,

75th: 13.2 s) and for the control in median 12.4 s

(25th: 11.2, 75th: 12.8 s).

Playback Experiments

In the playback experiments, we presented the same

study animals two different types of alarm calls:

zecks and whistles. As a control, we used calls of

sympatric bats, which are within the hearing rangeof mouse lemurs (Niaussat & Petter 1980; Fig. 3).

Vocalisations were recorded during experiments in

which mouse lemurs were confronted with one of

their predators, the Coquerels giant mouse lemur

(C. Fichtel, unpubl. data). Playback stimuli consisted

of a bout of vocalisations (56 s). Zeck and bat call

playbacks were each generated from recordings of

eight different individuals, whistle playbacks were

generated from different sections of three individu-

als. Each bout of vocalizations was repeated three

times with 5 s silent intervals in-between. Sound

pressure level was equalized by adjusting the relative

amplitude with SYNTRILLIUM Software Cool Edit

2000 1.1 (Syntrillium, Phoenix, AZ, USA). Playback

stimuli were presented with a Toshiba Satellite Pro

laptop. The laptop was connected to an USB

Audio interface Audiotrak OPTOplay soundcard,

Avisoft Portable ultrasonic amplifier (frequency

range: 1125 kHz) and an Avisoft Ultrasonic

Speaker ScanSpeak (frequency range: 1120 kHz).

The ultrasound loudspeaker was placed in the south-

western corner of the experimental cage 110 cm

above the ground (Fig. 1a). Mouse lemurs responses

were video- and audio-recorded for 1 min after the

onset of the playback. Playback stimuli were pre-sented once per night and individual in a random-

ized but counter-balanced order.

Data Analysis

Video tapes were analysed with a resolution of 25

frames per second using Apple Final Cut Pro HD 4.5

(Apple Computer GmbH, Feldkirchen, Germany). The

onset of the experiment was defined as the first

reaction towards the presented stimulus. The end of

(a) (b) (c)

Fig. 3: Spectrograms of playback stimuli.

Vocalizations of mouse lemurs: (a) zecks, (b)

whistles, (c) control: call of a sympatric living

bat.




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the model presentation was defined as the time when

the respective model was in a concealed position.

Behavioural responses were scored until mouse

lemurs began to show neutral behaviour (see Table 1

for definition of response categories). In order to

establish a baseline, we additionally recorded a refer-ence period for each individual during which the ani-

mal was not confronted with any stimulus. Playback

experiments were analysed for 60 s after the onset of

the playback stimulus.

Results

Predator Model and Control Experiments

Vocalizations in response to predator models and

control stimuli were given only during the presenta-

tion of the raptor model by one female, who emitted

whistles repeatedly for more than 1 min (Fig. 3b).

Neither predator nor control models elicited flight

responses in mouse lemurs. However, the presenta-

tion of the raptor model elicited freezing behaviour

in all subjects, whereas the presentation of the corre-

sponding control did elicit freezing in only one

subject (Table 2). Instead of responding with overt

flight responses, mouse lemurs oriented themselves,

with the head in the direction of the models, and

monitored them. Orientation time towards the

models was almost 100% during presentation of the

fossa and snake models but did not differ between

predator and control models (Table 2). During thepresentation, mouse lemurs sometimes even moved

in the direction of the models, although time spent

locomoting did not differ between experimental and

control periods (Table 2). The number of scans did

not differ between different predator stimuli (fossa

median: 6.24, 25th: 3.1, 75th: 8.43; snake median:

10.37, 25th: 7.12, 75th: 16.93; raptor median: 0,

25th: 0, 75th: 11.88; reference period median: 9.8,

25th: 5.75, 75th: 16.95; Friedman test v2 = 3.75,

df = 3, p = 0.087).

However, latency to show neutral behaviour (see

Table 1) was longer after the presentation of the

fossa and raptor model compared with the corre-

sponding controls (Fig. 4, Wilcoxon matched-pairs

signed-ranks test: fossa modelfossa control: Z =

)2.521, p = 0.012; raptor modelraptor control Z =)2.521, p = 0.012). The latency to show neutral

behaviour did not differ between the snake and con-

trol model (Fig. 4, Wilcoxon test Z = )0.84, p = 0.4).

A comparison between the reference period in

which no model was presented and the period in

which predator models were presented revealed that

mouse lemurs spent more time locomoting during

the reference period than during predator model

presentations (Fig. 5; Friedman test v2 = 13.94,

df = 3, p = 0.003; Wilcoxon test: reference period-

fossa: Z = )2.24, p = 0.025; reference period-fossa

control: Z = )2.52, p = 0.005; reference period-

snake: Z =)

2.24, p = 0.025; reference period-snake

Table 2: Comparison of behavioural responses between predator models and respective control dummies. Indicated are the median

(1. Quartile3. Quartile) of the percentage of time mouse lemurs showed the respective behaviour

Dummies

Freezing Orientation towards the stimulus Locomotion towards the stimulus

Percentage of time (%) Wilcoxon test Percentage of time (%) Wilcoxon test Percentage of time (%) Wilcoxon test

Fossa 0 96 (8399) Z = )1.4 2 (08) Z = )0.84

Control 0 91 (6998) p = 0.161 1 (04) p = 0.401

Snake 0 87 (7390) Z = )0.14 12 (1019) Z = )0.84

Control 0 85 (7197) p = 0.889 4 (021) p = 0.401

Raptor 18 (87) Z = )2.023 10 (059) Z = )1.4 0 Z = )1.83

Control 0 (0) p = 0.043 49 (2795) p = 0.161 2 (015) p = 0.068

Design

RaptorSnakeFossa

Time(s)

450

400

350

300

250

200

150

100

50

0

Control stimulus

Predator model

Median

25%75%

MinMax

*

*

Fig. 4: Latency in seconds, between the end of stimulus presentation

and until animals showed neutral behaviour. *p < 0.05 paired

Wilcoxon signed rank test.




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control: Z = )2.52 p = 0.012; reference period-

raptor: Z = )2.521, p = 0.012; reference period-rap-

tor control: Z = )3.38, p = 0.012, snake-raptor Z =

)2.19, p = 0.028, raptor-raptor control Z = )2.02,

p = 0.043). Number of scans did not differ between

the reference period and predator model presenta-

tion (fossa median: 6.24, 25th: 3.1, 75th: 8.43; snake

median: 10.37, 25th: 7.12, 75th: 16.93; raptor med-

ian: 0, 25th: 0, 75th: 11.88; reference median: 9.8,

25th: 5.75, 75th: 16.95; Friedman test v2 = 3.75,

df = 3, p = 0.087).

Playback Experiments

Mouse lemurs did not vocalize in response to play-

backs of alarm or control calls. Time spent moving

up- or downward did not differ between playback

treatments (time (s) spent moving upwards: zeck

median: 0, 25th: 0, 75th: 0; whistle median: 1.6,

25th: 0, 75th: 2.73; control median: 0, 25th: 0, 75th:

0; Friedman test: v2 = 4.37, df = 2, p = 0.152; time

(s) spent moving downwards: zeck median: 0.84,

25th: 0, 75th: 6.14; whistle median: 0, 25th: 0, 75th:

3.9; control median: 0, 25th: 0, 75th: 0; Friedman

test: v2 = 1.529, df = 2, p = 0.465). However, time

spent orienting towards the sound source differed

between playback stimuli, and mouse lemurs

showed a longer orientation time after the presenta-

tion of mouse lemur vocalizations than after control

calls (Fig. 6, Friedman Test v2 = 10.75, df = 2,

p = 0.005; Wilcoxon test zeckscontrol: Z = )2.38,

p = 0.017, whistlescontrol: Z = )2.52, p = 0.012).

Orientation time towards the loudspeaker did not

differ after the presentation of zecks and whistles

(Fig. 6, Wilcoxon test Z =)

1.68, p = 0.093). Presen-

tation of zecks and whistles elicited higher scan rates

than control calls (zecks median: 18.5, 25th: 10,

75th: 23.25; whistles median: 17, 25th: 12.25, 75th:

22.25; control median: 0, 25th: 0, 75th: 1.75; Fried-

man test v2 = 10.90, df = 2, p = 0.004; Wilcoxon

test: zeckcontrol: Z = )2.371, p = 0.018;

whistlecontrol: Z = )2.52, p = 0.012; Wilcoxon test:

zeckcontrol: Z = )2.371, p = 0.018; whistlecontrol:

Z = )2.52, p = 0.012) but scan rate did not differ

between zeck- and whistle presentation (Wilcoxon

test: Z = )0.28, p = 0.778).

Discussion

The results of this study show that mouse lemurs did

not respond with any overt flight responses after

presentation of the predator models. Instead, they

exhibited two different anti-predator responses: in

response to the fossa and snake models mouse

lemurs showed a rather unspecific monitoring

behaviour, probably to assess the potential risk that

emanates from the predator. In response to aerial

predator models, mouse lemurs showed a specific

anti-predator response, namely freezing behaviour,

which was longer following the raptor model than

after the raptor control presentation. Because the

latency to exhibit neutral behaviour was longer after

the presentation of the fossa and snake models than

control models, we conclude that mouse lemurs

seemed to perceive a difference between the fossa

and raptor models and their corresponding controls.

The lack of a difference in latency to exhibit neutral

behaviour between the snake and corresponding

control model might be due to the small sample size

Design

ReferenceRaptorSnakeFossa

%o

fpresentatio

ntime

50

40

30

20

10

0

Control stimulus

Predator model

Reference periode

Median

25%75%

MinMax

***** *

*

*

Fig. 5: Percentage of presentation time animals locomoted during

the reference period and predator model presentation.

Design

Bat callWhistleZeck

Orientationtowardsstimulus(s)

70

60

50

40

30

20

10

0

Control

Mouse lemur call

Median

25%75%

MinMax

**

Fig. 6: Orientation time towards the loudspeaker during stimulus

playback experiments.




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of eight individuals, however. In addition, mouse

lemurs except one individual did not produce alarm

calls after detecting predators, indicating that they

may not rely on early warning of conspecifics.

Finally, playback experiments with alarm calls

recorded during experimental confrontation with areal predator revealed that mouse lemurs did not

associate any specific escape strategies with these

calls. Instead these alarm calls might be directed at

the predator or may serve to recruit conspecifics.

Anti-Predator Strategies

Mouse lemurs did not show any overt flight

responses after the presentation of the predator

models but exhibited monitoring behaviour instead,

in which they oriented themselves towards the

models. This monitoring behaviour might be adapted

to the hunting strategy of their predators. Many ter-

restrial predators are stalking or sit-and-wait

predators which are ambush hunters that rely on an

element of surprise to capture their prey (Schaller

1968, 1972). Once a stalker or sit-and-wait predator

is detected by prey animals they usually have no

further chance to hunt successfully (Schaller 1967).

In this case, it can be beneficial for prey animals to

keep track of the predator in order to prevent an

additional attack.

Anecdotal reports of fossas hunting strategies

suggest that solitary individuals exhibit an ambush

hunting strategy (Wright et al. 1997) but also that 2or 3 males occasionally hunt cooperatively and rely

on pursuing prey (Luhrs & Dammhahn 2010).

Although fossas are mainly terrestrial, they exhibit

extraordinarily climbing skills while mating in trees

or pursuing prey in trees (Hawkins 2003; Luhrs &

Dammhahn 2010). Thus, keeping track of detected

fossas might be advantageous for mouse lemurs

because in case of an attack they are able to move

on terminal branches that are inaccessible to fossas.

Snakes that prey upon mouse lemurs belong to

the families Boidae, Viperidae, Pythonidae and Colu-

bridae, which are considered to be sit-and-wait

predators as well. Once prey animals have detected

such snakes, the danger of being captured is low

(Slip & Shine 1988; Ayers & Shine 1997). Thus, the

observed monitoring behaviour of mouse lemurs

might also be advantageous to prevent snake

attacks.

In contrast to the other treatments, the raptor

model elicited freezing behaviour in mouse lemurs:

they jumped immediately downwards and remained

in their position without any further movement.

Birds of prey use two distinct techniques for hunting

prey: first, active search or flight hunt, and second

sit-and-wait hunt or perch hunt (Jaksic & Carothers

1985). Because most raptors rely heavily on visual

or acoustic cues to detect their prey, moving animals

are perceived more easily than stationary ones (Rice1983). Thus, it should be advantageous for prey

animals to remain immobile and freeze as soon as

an avian predator has been detected (Fitzgibbon

1990; Caro et al. 2004). Nocturnal birds of prey that

hunt mouse lemurs, such as the barn owl (Tyto

alba), have been shown to be able to locate and

capture their prey in total darkness (Payne 1971),

hence relying exclusively on acoustic cues. Thus,

remaining motionless and emitting as little noise as

possible seems to be a viable anti-predator strategy

against those birds of prey. Moreover, other noctur-

nal primates, such as red-tailed sportive lemurs and

spectral tarsier, have also been reported to freeze in

response to birds of prey (Fichtel 2007; Gursky

2007).

In conclusion, mouse lemurs seem to rely on a

combination of anti-predator strategies: crypsis,

because they have a small body size, are nocturnal,

solitary and showed freezing behaviour in response

to the raptor model. However, in response to

detected terrestrial predators which hunt by ambush

mouse lemurs showed monitoring behaviour, proba-

bly to assess the potential risk that emanates from

the predator as well as mobbing behaviour in

response to snakes (Eberle & Kappeler 2008).

Alarm Calls

With the exception of one individual, mouse lemurs

did not alarm call in response to any predator

models or to playbacks of alarm calls. They also did

not associate any escape strategy with these calls but

oriented themselves towards the sound source.

Because in this experimental set up mouse lemurs

have been tested singly, an audience effect may

explain the lack of alarm call responses. If alarm calls

are directed at conspecifics and not at predators,

other birds and mammals do not produce alarm calls

when no conspecific is close by (reviewed in Fichtel

& Manser 2010). However, Zecks and Whistles used

in the playback experiments were recorded during

confrontation experiments with a primate predator,

Coquerels giant mouse lemur, in which single

mouse lemurs were confronted with a Coquerels

giant dwarf lemur (C. Fichtel, unpubl. data). Zecks

were also given when a Coquerels giant dwarf

lemur chased a mouse lemur (C. Fichtel, pers. obs.).




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Moreover, Zecks are also given during aggressive

interactions with conspecifics and during distur-

bances at sleeping sites, in which females rest with

kin or sometimes also alone and males usually alone

(Eberle & Kappeler 2002). Thus, it is likely that

Zecks are directed at predators and aggressors andmay have a deterrence function. Whistles are given

during direct confrontations with Coquerels giant

mouse lemur or snakes (C. Fichtel, unpubl. data;

Eberle & Kappeler 2008) but also during the mating

season and during reunion of sleeping group mates

at the sleeping site (Braune et al. 2005). They may

therefore have a recruiting function similar to

recruitment calls of meerkats (Suricata suricatta) or

banded mongoose ( Mungos mungo; Manser 2001;

Manser et al. 2001; Furrer & Manser 2009).

Zecks have a broad frequency range with their

main energy at lower frequencies between 5 and

10 kHz, and are within the hearing range of most

mammalian and avian predators (Fay & Wilber

1989; Yamazaki et al. 2004) and may thus be

involved in predatorprey communication. Whistles,

in contrast, are higher in frequency (1520 kHz),

and within the hearing range of conspecifics but

only in the periphery or above the hearing range of

potential mammalian and avian predators (Fay &

Wilber 1989; Yamazaki et al. 2004), supporting our

assumption that they might be addressed only at

conspecifics and may have a recruiting function.

However, to confirm the different functions of Zecks

and Whistles further playback experiments arerequired.

Because of the reduced visibility at night, preda-

tors might not be detected at greater distances

(Blumstein & Armitage 1997). Thus, early warning

of predators, which requires a certain amount of

time for conspecifics to flee to safety, might not be

generally beneficial in nocturnal species. Studies of

other nocturnal primates have indicated that they do

in fact not rely on early warning of predators and

show conspicuous mobbing behaviour in response to

snakes or even carnivore models (Gursky 2001;

Schulke 2001; Bearder et al. 2002, 2007, Eberle &

Kappeler 2008; see for a review Fichtel in press).

Thus, alarm calls of nocturnal primates might be

directed at predators, but may also attract conspecif-

ics to join the mobbing. Because nocturnal strep-

sirrhines are considered as the evolutionarily most

basal living primates (Martin 1990), this pattern

might represent the ancestral form of alarm calling

in primates (Fichtel 2007, in press). Interestingly, a

comparative analysis of the evolution of alarm calls

in rodents suggested that alarm calling in diurnal

rodents probably also evolved as a means to commu-

nicate to predators (Shelley & Blumstein 2004).

Comparative studies of other nocturnal mammals

are now required to test the generality of this

conclusion.

Acknowledgements

We would like to thank Mme. Olga Ramilijaona and

M. Daniel Rakotondravony of the University of

Antananarivo, the Comission Tripartite de Direction

des Eaux et Forets, and the C.F.P.F. Morondava for

their authorization and support of this study. A big

Misaotra betsaka to lequipe DPZ for assistance

during the experiments, especially to Jean-Claude

Beroboka and to Melanie Dammhahn for sharing

her mouse lemur knowldege with us. CF was finan-

cially supported by the DFG (Fi 92912). The

experiments complied with the current laws of the

country in which they were performed.

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