The authors have declared that no competing interests exist.
Conceived and designed the experiments: MS CS MG MWH. Performed the experiments: MS. Analyzed the data: MS. Contributed reagents/materials/analysis tools: MS CS MG MWH. Wrote the paper: MS MG MWH.
As alarm calls indicate the presence of predators, the correct interpretation of alarm calls, including those of other species, is essential for predator avoidance. Conversely, communication calls of other species might indicate the perceived absence of a predator and hence allow a reduction in vigilance. This “eavesdropping” was demonstrated in birds and mammals, including lemur species. Interspecific communication between taxonomic groups has so far been reported in some reptiles and mammals, including three primate species. So far, neither semantic nor interspecific communication has been tested in a solitary and nocturnal lemur species. The aim of this study was to investigate if the nocturnal and solitary Sahamalaza sportive lemur,
The avoidance of predators strongly governs the behaviour of potential prey animals
Interspecific communication between taxonomic groups has so far been reported in a number of mammalian and reptilian species that respond to bird alarm calls
Generally, signal recognition between species might be based on the convergence of acoustically similar signal attributes
To date, neither semantic nor interspecific communication have been tested in a solitary and nocturnal primate species, even though one-third of all primate species are nocturnal and small-bodied, and face a high predation risk mainly due to their small size and their different activity period in comparison to most predators
Due to the diversity of their social systems (solitary, dispersed pairs, harems), their occurrence in sometimes high densities, and their exposed resting position, the sportive lemurs (
Here we investigate the diurnal anti-predator behaviour of the Sahamalaza sportive lemur,
During daylight hours the Sahamalaza sportive lemur rests alone in tree holes or in tree tangles
We furthermore hypothesised that any adequate responses of this solitary sportive lemur species to heterospecific calls are based on learning rather than similarity of calls, and predicted that animals would react to alarm calls and songs of sympatric species according to their meaning rather than their acoustic structure.
This study was conducted under permit from the Madagascan Ministere de l’environnement et des forets (Autorisation de recherche #231/11/MEF/SG/DGF/DCB.SAP/SCB) and was ethically approved by the Welfare & Research Advisory Board of the Bristol, Clifton and West of England Zoological Society.
The Ankarafa Forest is situated in the UNESCO Biosphere Reserve and National Park on the Sahamalaza Peninsula and is part of the Province Autonome de Mahajanga, NW Madagascar. It extends between 13°52′S and 14°27′S and 45°38′E and 47°46′E (WCS/DEC 2002;
There are no large connected areas of intact primary forest left on the Sahamalaza Peninsula, and the remaining fragments all show some degree of anthropogenic disturbance and/or edge effects
Between September and November 2011, a total of 981 playback experiments were conducted on 19 individual sportive lemurs. The tested lemurs rested at the entrance of tree holes during the day and inhabited five different forest fragments.
The first week of the field season was used to walk the five different forest fragments during the day to find mature sportive lemurs in their resting sites, and to identify them individually by their facial masks where possible. We only chose individuals whose resting site/resting position allowed us to clearly see their faces and thus to observe their behaviour in response to the playback experiments. During this first survey, we found nine individuals. As this
The alarm vocalisations of two abundant bird species, the Madagascar magpie-robin and the crested coua, were played to the sportive lemurs. Songs of both species were used as control. All calls were obtained from the online archive of the Macaulay Library (
Spectrograms (
Call type | N | stimulus length (s) | call duration (s) | inter call interval (s) | mean peak frequency (Hz) | source level (dB peSPL) |
Crested coua song | 5 | 4.5 (3.3–4.9) | 0.2 (0.2–0.3) | 0.6 (0.6–0.7) | 1870 (1680–2250) | 70.4 (70.1–74.7) |
Crested coua alarm | 5 | 6.5 (5.8–8.1) | 0.5 (0.4–0.6) | 0.7 (0.6–1) | 1915 (1780–2688) | 70.7 (70.7–72.1) |
Madagascar magpie-robin song | 4 | 9.5 (8.3–11) | 1.8 (1.5–2) | 5 (3.6–5.8) | 3885 (3750–4613) | 71.2 (70.8–71.8) |
Madagascar magpie-robin alarm | 4 | 8.7 (4.6–9.9) | 0.4 (0.3–0.8) | 1.8 (0.5–2.9) | 6460 (5810–6650) | 71.2 (71.2–71.5) |
Blue-eyed black lemur contact call | 4 | 0.1 (0.1–0.1) | 0.1 (0.1–0.1) | N/A | 680 (660–832.5) | 69.6 (69–69.8) |
Blue-eyed black lemur aerial alarm | 4 | 1.8 (1.7–1.9) | 1.8 (1.7–1.9) | N/A | 1200 (1200) | 69.9 (69.7–70.3) |
Blue-eyed black lemur terrestrial alarm | 4 | 0.4 (0.4–0.5) | 0.4 (0.4–0.5) | N/A | 250 (230–337.5) | 70.3 (69.9–70.5) |
Blue-eyed black lemur agitation call | 4 | 1.9 (1.8–2.2) | 0.3 (0.3–0.7) | 0.3 (0.1–0.5) | 1030 (880–1110) | 70.2 (69.8–70.6) |
Median (interquartile range; Q1–Q3) stimulus length (start of first call unit to end of last call unit), call duration (duration from call onset to call offset), inter call interval (time gap between call offset and successive call onset), peak frequency of call (measured from power spectrum), and source level (in dB peSPL re 1 m) of crested coua song, crested coua alarm, Madagascar magpie-robin song, Madagascar magpie-robin alarm, blue-eyed black lemur contact call, blue-eyed black lemur aerial alarm, blue-eyed black lemur terrestrial alarm blue-eyed black lemur agitation call recordings used as playback stimuli.
To determine the similarity of the calls used as playback stimuli we used an implementation of dynamic time warping
The calls were played back using an iPod Nano, model A1320 (Apple Inc., Cupertino, CA) and wireless loudspeaker (JBL On Stage Micro II; Harman International Industries, Inc., Stamford, CT; Frequency range 80 Hz-20 kHz). Sound pressure level of call playbacks were measured in a semi-anechoic chamber in Bristol using a 40BF microphone, 26AB preamplifier and 12AA power module (all G.R.A.S. Sound & Vibration, Holte, Denmark) calibrated by D1411E acoustic calibrator (Dawe Instruments, Brentford, UK). Mean sound pressure levels were 69–71 dB peak-equivalent SPL re 1 m (see
As field test of playback quality we played all stimuli in the absence of lemurs and checked for responses from individuals of the species being played back that were in the vicinity. We obtained vocal responses of crested couas, Madagascar magpie-robins and blue-eyed black lemurs after playbacks of their calls, and sometimes individuals approached us, which confirmed our replays were of adequate quality and level. In cases where we attracted individuals of the replayed species during our experiments with sportive lemurs, the experiment was stopped and that trial was discarded. As far as we are aware, we never elicited responses from predators after playbacks of alarm calls, although we are not able to completely exclude that we might have attracted predators without us noticing them. We did not consider a possible attraction of predators as problematic as alarm calls of both birds and lemurs are commonly heard in the forest fragments.
Playback equipment was either hidden behind a bush or in a tree (0.5–2 m above ground) at a horizontal distance of approximately 5 m from the
Rest | Animal sits or lies inactively; eyes closed or open, but without attentive scanning |
Vigilance | Animal stops an ongoing behaviour and orients head and eyes toward a specific direction or component of the environment or scans the environment. Eyes are wide open, but slight movement still takes place |
Autogrooming | Animal grooms itself; licking or gnawing its fur |
Change position | Animal climbs slightly up or down the tree tangle or tree hole (max. 50 cm) |
Lick/bite tree | Animal licks the surface of its sleeping tree and/or uses its teeth to gnaw off parts of the surface – often observed in combination with Autogrooming |
Out of sight | Animal is out of sight in the tree hole or canopy |
Scanning up | Animal is vigilant and looks up into sky or trees |
Scanning down | Animal is vigilant and looks down to the ground |
No change | Animal continues behaviour displayed before the playback of a specific call type |
Diurnal ethogram as observed during playback experiments. Durations (in seconds) of category I behaviours were determined within the five minute intervals before and after each playback. Category II was used to quantify behaviour immediately (within 5 s) after each playback.
Call types were presented in a randomised order to individual sportive lemurs in the time window between 8 am and 6 pm. We aimed to play back all four or five versions of the same call type to an individual before repeating a previously presented call. We presented only one song/contact call plus one alarm call to an individual sportive lemur on a single day, and such a playback session lasted approximately 30 to 50 minutes, depending on the time the individual needed to settle to the observer’s presence. Over a period of two months a mean number of 55 (min: 17, max: 78) playback experiments were conducted with individual sportive lemurs. The five different versions of general alarm calls of crested couas were played back between 26 and 28 times, resulting in a total of 137 playbacks to 19 different individuals (
L | Crested coua alarm | Crested coua song | Madagascar magpie-robin alarm | Madagascar magpie-robin song | ∑ | |||||||||||||||
1 | 2 | 3 | 4 | 5 | 1 | 2 | 3 | 4 | 5 | 1 | 2 | 3 | 4 | 5 | 1 | 2 | 3 | 4 | ||
1 | 1 | 0 | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 1 | 1 | 0 | 1 | 9 |
2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 3 | 1 | 2 | 1 | 2 | 2 | 2 | 37 |
3 | 1 | 1 | 1 | 2 | 1 | 2 | 2 | 2 | 1 | 3 | 2 | 3 | 3 | 1 | 2 | 1 | 1 | 1 | 1 | 31 |
4 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 38 |
5 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 3 | 2 | 2 | 1 | 2 | 2 | 2 | 2 | 2 | 38 |
6 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 1 | 2 | 1 | 3 | 2 | 2 | 3 | 3 | 2 | 39 |
7 | 1 | 1 | 1 | 1 | 1 | 2 | 0 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 19 |
8 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 38 |
9 | 1 | 1 | 0 | 0 | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 1 | 1 | 13 |
10 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 38 |
11 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 1 | 2 | 2 | 2 | 2 | 2 | 2 | 3 | 2 | 2 | 2 | 38 |
12 | 1 | 1 | 2 | 1 | 1 | 1 | 1 | 2 | 1 | 1 | 2 | 2 | 1 | 2 | 1 | 1 | 2 | 2 | 2 | 27 |
13 | 1 | 2 | 2 | 2 | 4 | 2 | 2 | 2 | 2 | 1 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 3 | 2 | 39 |
14 | 1 | 1 | 1 | 2 | 1 | 1 | 2 | 1 | 1 | 1 | 2 | 2 | 0 | 2 | 2 | 1 | 1 | 2 | 1 | 25 |
15 | 1 | 0 | 0 | 1 | 1 | 1 | 2 | 0 | 1 | 0 | 2 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 14 |
16 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 18 |
17 | 1 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 3 |
18 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 3 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 39 |
19 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 3 | 2 | 2 | 1 | 38 |
∑ | 28 | 26 | 27 | 28 | 28 | 31 | 28 | 28 | 26 | 27 | 31 | 34 | 27 | 27 | 28 | 29 | 29 | 31 | 28 | 541 |
Numbers of playback-experiments conducted with five different versions of crested coua alarm and song, Madagascar magpie-robin alarm, and four version of Madagascar magpie-robin song with each sportive lemur (L).
L | Aerial alarm | Terrestrial alarm | Agitation call | Contact call | ∑ | ||||||||||||
1 | 2 | 3 | 4 | 1 | 2 | 3 | 4 | 1 | 2 | 3 | 4 | 1 | 2 | 3 | 4 | ||
1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 | 1 | 0 | 1 | 0 | 0 | 0 | 1 | 1 | 7 |
2 | 2 | 1 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 31 |
3 | 2 | 1 | 2 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 18 |
4 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 32 |
5 | 2 | 2 | 2 | 2 | 2 | 1 | 2 | 2 | 2 | 2 | 3 | 1 | 2 | 2 | 2 | 2 | 31 |
6 | 2 | 3 | 2 | 2 | 3 | 3 | 2 | 2 | 2 | 2 | 1 | 2 | 3 | 2 | 2 | 2 | 35 |
7 | 1 | 0 | 1 | 1 | 0 | 0 | 1 | 0 | 1 | 0 | 0 | 0 | 0 | 2 | 1 | 1 | 9 |
8 | 2 | 2 | 2 | 2 | 2 | 2 | 1 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 31 |
9 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 0 | 0 | 0 | 1 | 1 | 1 | 8 |
10 | 2 | 2 | 3 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 33 |
11 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 32 |
12 | 2 | 1 | 2 | 1 | 1 | 2 | 1 | 1 | 1 | 0 | 1 | 1 | 2 | 2 | 2 | 1 | 21 |
13 | 3 | 2 | 1 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 32 |
14 | 2 | 1 | 1 | 1 | 2 | 1 | 1 | 1 | 2 | 1 | 2 | 1 | 1 | 2 | 2 | 1 | 22 |
15 | 0 | 1 | 0 | 2 | 1 | 1 | 0 | 0 | 1 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 12 |
16 | 1 | 1 | 2 | 1 | 1 | 1 | 2 | 1 | 2 | 1 | 2 | 1 | 0 | 1 | 1 | 1 | 19 |
17 | 1 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 2 |
18 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 3 | 2 | 2 | 3 | 2 | 2 | 2 | 34 |
19 | 2 | 2 | 2 | 2 | 2 | 1 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 31 |
∑ | 32 | 25 | 29 | 27 | 28 | 26 | 27 | 25 | 30 | 25 | 28 | 24 | 26 | 30 | 30 | 28 | 440 |
Numbers of playback-experiments conducted with four different versions of blue-eyed black lemur aerial and terrestrial alarm calls, agitation and contact call with each sportive lemur (L).
To test for differences in the duration of individual lemurs’ vigilance (measured as seconds of vigilance) before and after the playback of predator and control calls, we performed a Wilcoxon signed rank test (P≤0.05) on each individuals’ mean vigilance duration in the five-minute periods before and after the playback of each stimulus type.
To test for immediate responses, scanning directions were either rated as appropriate or inappropriate. We classified scanning up or down after alarm calls of crested coua and Madagascar magpie-robin as appropriate, as these alarm calls might refer to different kinds of predators. The response was also rated as appropriate if individuals scanned the sky after blue-eyed black lemur aerial alarm or if they looked down after blue-eyed black lemur terrestrial alarm calls. We rated scanning up or down after blue-eyed black lemur agitation calls as appropriate, as this call type might refer to different sources of disturbance. Furthermore, no change of scanning direction after songs/contact calls of either species was classified as appropriate behaviour. Consequently we classified no reaction after alarm calls and scanning up or down after songs/contact calls as inappropriate behaviour.
χ2 tests with Yates-correction of numbers of appropriate and inappropriate behaviour of each individual were used to test for significant differences in the reactions of lemurs towards the playback stimuli (rate 50%; P≤0.05). χ2 tests were also used to test if the sportive lemurs increased or decreased various behaviour displayed immediately before in comparison to immediately after the playbacks.
We used multidimensional scaling to identify patterns in the distance matrix of acoustic similarity indices generated with DTWAVE (
63% and 68% out of 19 individuals responded with increased duration of vigilance after playbacks of alarm calls of crested coua and Madagascar magpie-robin, whilst only 5% and 15% decreased the duration of vigilance after crested coua and Madagascar magpie-robin alarm calls, respectively. Overall, the duration of vigilance increased after playbacks of crested coua and Madagascar magpie-robin alarms (
Call type | Vigilance before call (s) | Vigilance after call (s) | |
Crested coua alarm | 104.5 (36.5–166.8) | 126 (78–229.3) | P = 0.004 |
Madagascar magpie-robin alarm | 50 (18.8–64.8) | 95.5 (65–133.8) | P = 0.003 |
Blue-eyed black lemur aerial alarm | 40 (8.3–68.5) | 95 (39–153) | P = 0.011 |
Blue-eyed black lemur terrestrial alarm | 32.5 (7.8–61.5) | 40 (18.5–70.3) | P = 0.449 |
Blue-eyed black lemur agitation call | 44.3 (13.1–107.5) | 54.3 (40.8–99.5) | P = 0.586 |
Crested coua song | 80.5 (43.8–146.8) | 65 (21.5–88.5) | P = 0.01 |
Madagascar magpie-robin song | 50 (16.6–100.9) | 39.8 (11.6–72.9) | P = 0.360 |
Blue-eyed black lemur contact call | 54.5 (15.5–63) | 18.5 (0–47.4) | P = 0.179 |
Median (quartile 1– quartile 3) vigilance in seconds within 5 min before and after the playback of alarm calls of crested coua (N = 19), Madagascar magpie-robin (N = 19), blue-eyed black lemur (All: N = 19) and songs of crested coua (N = 19), Madagascar magpie-robin (N = 19) and blue-eyed black lemur contact calls (N = 19). Wilcoxon Signed Ranks Test with α ≤0.05.
After crested coua songs the vigilance of tested individuals decreased (
In direct response to crested coua and Madagascar magpie-robin alarm calls, 94% and 89% of the individuals changed their behaviour from resting or autogrooming to vigilance, respectively. Looking at the number of trials, the percentage of vigilance (amount of vigilance in relation to non-vigilant behaviours immediately before and after the playbacks) increased significantly, whilst resting decreased (
Rest % before | Rest % after | P | Vigilance % before | Vigilance % after | P | Autogrooming % before | Autogrooming % after | P | |
Crested coua alarm | 68 (36.5–100) | 22.5 (0–67) | <0.05 | 27.5 (0–55) | 74.5 (33.5–100) | <0.05 | 4.5 (0–100) | 3 (0–20) | >0.1 |
Crested coua song | 61 (0–100) | 51 (0–100) | >0.1 | 31 (0–100) | 40 (0–100) | >0.1 | 8 (0–20) | 9 (0–50) | >0.1 |
Madagascar magpie-robin alarm | 68 (30–100) | 24 (0–50) | <0.05 | 28.5 (0–70) | 75 (50–100) | <0.05 | 3.5 (0–25) | 1 (0–9) | >0.1 |
Madagascar magpie-robin song | 72 (25–100) | 61 (25–100) | >0.1 | 23 (0–75) | 35 (0–75) | >0.1 | 5 (0–20) | 4 (0–25) | >0.1 |
Blue-eyed black lemur aerial alarm | 67.5 (0–100) | 23(0–100) | <0.05 | 24 (0–100) | 77 (0–100) | <0.05 | 8.5 (0–28.5) | 0 (0) | >0.1 |
Blue-eyed black lemur terrestrial alarm | 72 (0–100) | 62 (0–100) | >0.1 | 24 (0–50) | 36 (0–100) | >0.1 | 4 (0–100) | 3 (0–14) | >0.1 |
Blue-eyed black lemur agitation call | 73.5 (0–100) | 55 (0–78) | >0.1 | 19 (0–50) | 41.5 (12.5–100) | >0.1 | 7.5 (0–75) | 2.5 (0–25) | >0.1 |
Blue-eyed black lemur contact call | 78 (44–100) | 7 (44–100) | >0.1 | 19 (0–44.5) | 20 (0–50) | >0.1 | 2.5 (0–12.5) | 4 (0–22) | >0.1 |
Mean (minimum-maximum) percentages of behaviours observed immediately before and after presentation of alarm calls and songs of crested coua and Madagascar magpie robins, as well as aerial, terrestrial alarm, agitation, and contact calls of blue-eyed black lemurs. χ2 test (rate 50%; P≤0.05).
No individual looked directly in the direction of the speaker in response to the playback stimuli. In total, 77% and 85% of the individuals displayed more appropriate scanning behaviour after the alarm calls of crested coua and Madagascar magpie-robin (looking up in all cases), as did 81% of the individuals after blue-eyed black lemur aerial alarm calls, resulting in significant changes on group level.
Call type | Appropriate ∑ | Inappropriate ∑ | |
Crested coua alarm | 79 | 36 | P<0.001 |
Madagascar magpie-robin alarm | 83 | 43 | P<0.05 |
Blue-eyed black lemur aerial alarm | 61 | 30 | P<0.05 |
Blue-eyed black lemur terrestrial alarm | 29 | 50 | P>0.1 |
Blue-eyed black lemur agitation call | 42 | 50 | P>0.1 |
Crested coua song | 66 | 52 | P>0.1 |
Madagascar magpie-robin song | 65 | 23 | P<0.001 |
Blue-eyed black lemur contact call | 73 | 21 | P<0.001 |
Appropriate reactions (scanning up or down after crested coua alarm and Madagascar magpie-robin alarm, scanning the sky after blue-eyed black lemur aerial alarm, down after blue-eyed black lemur terrestrial alarm and either up or down after blue-eyed black lemur agitation call, no change of scanning direction after songs/contact calls of each species) or inappropriate (no reaction after alarm calls; scanning up or down after songs/contact calls) of scanning direction of tested sportive lemurs. χ2 test (rate 50%; α≤0.05); Degrees of freedom (Df) = 12 for crested coua alarm, 13 for crested coua song, 12 for Madagascar magpie-robin alarm, 10 for Madagascar magpie-robin song, 11 for blue-eyed black lemur aerial alarm, agitation call and contact call; 9 for blue-eyed black lemur terrestrial alarm.
Our results suggest that the Sahamalaza sportive lemur is capable of taking advantage of other species’ alarm calls. As predicted, tested sportive lemurs significantly increased vigilance after playbacks of alarm calls of sympatric bird species, the crested coua and the Madagascar magpie-robin. Furthermore, they responded with increased vigilance to aerial alarm calls of the sympatric blue-eyed black lemur, but contrary to our prediction, not to their terrestrial alarm and agitation calls.
In response to playbacks of songs/contact calls of the three species, the sportive lemurs became significantly less vigilant after songs of the crested coua, and vigilance also decreased, though not significantly, after songs/contact calls of the Madagascar magpie-robin as well as the blue-eyed black lemur, possibly because these songs/contact calls are indicating that no predator is around. These results show that this
This kind of interspecific communication between taxonomic group was so far only found in diurnal and group living animals (red squirrels (
In immediate response to alarm calls of the crested coua and the Madagascar magpie-robin the tested animals displayed significantly more appropriate scanning behaviour. Animals usually scanned the sky, indicating that the birdś alarm calls might signal for raptors rather than predators in general. Furthermore, in line with the results on change of duration of vigilance, sportive lemurs displayed significantly more appropriate scanning behaviour after aerial alarm, but not after terrestrial alarm and agitation calls of the blue-eyed black lemur. The tested individuals scanned towards the sky, but never to the ground when they reacted to aerial alarm, suggesting that they expected the potential danger from above and thus classified the alarm call correctly. In conclusion, the tested Sahamalaza sportive lemurs seem to understand the semantic of the aerial alarm call of the blue-eyed black lemur, and change their behaviour accordingly, but it remains unclear if agitation and terrestrial alarm calls are understood and not deemed important or if they are not classified as alarm calls. Agitation calls are usually given in inter- and intragroup encounters and conflicts (M Seiler, pers. obs.), so it might not be sensible for sportive lemurs to react in response to them. In immediate response to the songs of the crested coua and Madagascar magpie-robin, as well as to the contact calls of the blue-eyed black lemur, the tested individuals usually did not react, indicating that they did not associate a possible risk with these stimulus types and thus classified the songs/contact calls correctly.
The recognition of signals between species is either based on the convergence of acoustically similar signal attributes
Although the Sahamalaza sportive lemur clearly reacted to the alarm calls of three different sympatric species, their responses were not as strong as when we directly presented vocalisations of an aerial and a terrestrial predator in a previous study
In conclusion, our results in this study suggest that the Sahamalaza sportive lemur is able to increase the chance of detecting a predator early through eavesdropping on sympatric species’ alarm calls, in addition to its predator specific anti-predator behaviours that include early acoustic detection and keeping track of predators. This additional “eavesdropping” might be an essential ability for a solitary living animal, which cannot count on early predator detection through group members. The ability of learning the meaning of other species’ alarm calls is therefore an important factor of the anti-predator behaviour of the Sahamalaza sportive lemur.
We would like to thank Madagascar National Parks (MNP), especially the director of Sahamalaza - Iles Radama National Park, M. ISAIA Raymond, for their continuing collaboration. Thank you also to the DGEF and CAFF/CORE for granting us research permits for our work in Sahamalaza, and to Prof. RABARIVOLA Clément for his ongoing help. Jean-Michele, Gabby Bell, Lisa Knudsen, along with all Ankarafa field guides, contributed substantially to the data collection. We also thank Olivier Friard for his help in running the acoustic similarity analysis.