Persistence of alarm-call behaviour in the absence of predators: a comparison between wild and captive-born meerkats ( Suricata suricatta )

TL;DR: The results from captive populations suggest that direct, physical interaction with predators is not necessary for meerkats to perform correct anti-predator behaviour in terms of alarm-call usage and olfactory predator recognition.

Abstract: Performing correct anti-predator behaviour is crucial for prey to survive. But are such abilities lost in species or populations living in predator-free environments? How individuals respond to the loss of predators has been shown to depend on factors such as the degree to which anti-predator behaviour relies on experience, the type of cues evoking the behaviour, the cost of expressing the behaviour and the number of generations under which the relaxed selection has taken place. Here we investigated whether captive-born populations of meerkats (Suricata suricatta) used the same repertoire of alarm calls previously documented in wild populations and whether captive animals, as wild ones, could recognize potential predators through olfactory cues. We found that all alarm calls that have been documented in the wild also occurred in captivity and were given in broadly similar contexts. Furthermore, without prior experience of odours from predators, captive meerkats seemed to dist inguish between faeces of potential predators (carnivores) and non-predators (herbivores). Despite slight structural differences, the alarm calls given in response to the faeces largely resembled those recorded in similar contexts in the wild. These results from captive populations suggest that direct, physical interaction with predators is not necessary for meerkats to perform correct anti-predator behaviour in terms of alarm-call usage and olfactory predator recognition. Such behaviour may have been retained in captivity because relatively little experience seems necessary for correct performance in the wild and/or because of the recency of relaxed selection on these populations.

Summary

Introduction

• Many species, for example, produce alarm calls to warn conspecifics of impending danger (Klump & Shalter 1984) .
• Experienceindependent behaviour, behaviour with low production costs and behaviour evoked by cues with convergent features may be more likely to persist in predator-isolated environments.
• Additionally, the acoustic structure of predator-specific calls simultaneously encodes information about the signaller's perception of response urgency: calls given on spotting a close predator (termed high urgency) are structurally different from those given to the same predator encountered at intermediate (medium urgency) and far (low urgency) distances (Manser 2001) .

Study sites and populations

• Between August 2004 and December 2005, the authors studied six captive populations of meerkats living in zoos in Switzerland , Germany (Cologne, Karlsruhe, Hannover, Osnabrück) and Ireland .
• All outdoor encloses had a clear view of the sky.
• Additional structures such as hollow tree trunks and termite mounds were also present, providing ecologically natural shelters.
• Except for one zoo, where individuals were distinctly marked with hair dye, individual identification was not feasible.
• At this study site, a range of five to 13 (varying between years) wild but well-habituated (close observation within 1 m) groups, varying in size from three to 50 individuals, have been followed since 1995.

Alarm-call usage

• To determine whether captive meerkats used the same repertoire of alarm calls as those described for wild meerkats and whether the calls were used in similar contexts, the authors recorded alarm calls produced by captive meerkats in response to natural sightings on an ad libitum basis.
• The authors also recorded calls given during faecal presentations (see below).
• All alarm calls were recorded (44.1 kHz sampling frequency; 16bit PCM-WAV) at a distance of 2-4 m from the caller using a Sennheiser directional microphone (ME66/K6 with a MZW66 pro windscreen; frequency response 40-20000 Hz ±.

Presentation of Olfactory Cues

• To test whether captive meerkats responded to olfactory cues from predators, and to compare the calls given in such circumstances with those produced in the wild, the authors presented captive groups with faeces from carnivores (potential predators) and herbivores (nonpredators/control).
• Faeces from some species were presented in more than one zoo, but the meerkat group in each zoo received only one sample of carnivore faeces and one sample of herbivore faeces.
• At least 2 h was left between presentations and faeces were removed immediately after testing (when animals showed no further interest).
• The authors only included calls (from captivity and the wild) that were recorded from different individuals.
• The resulting frequency-time spectra were analysed with LMA 2005 (developed by K. Hammerschmidt), a software tool that extracts a set of call parameters from acoustic signals (Schrader & Hammerschmidt 1997) .

Statistical analysis

• Because of differences in the amount of time spent observing each captive population (due to factors such as bad weather, too much disturbance and limited access), the authors were unable to record alarm calls in a standardized way across all zoos.
• The authors therefore present the data on alarm-call usage qualitatively instead of quantitatively.
• For the analysis of acoustic differences between captive and wild populations, the authors first used multi-variate analysis of variance including all of the eight measured call parameters.
• In each of 10 turns, nine of the folds were used to establish the model and the remaining fold was used to estimate the model's validity.
• The authors calculated assignment probabilities expected by chance using a bootstrap approach.

Alarm-Call Usage

• The amount of calling differed between captive populations, but alarm calling was observed in all six groups.
• Airplanes, helicopters and zeppelins were typically far away (> 500 m), whereas birds commonly flew past closeby (< 50 m).
• Some of the calls produced in response to planes, helicopters and zeppelins were also similar to the medium-urgency aerial calls normally elicited by raptors in the wild.
• In response to sudden disturbances, such as rapid movements, captive meerkats produced calls very similar to the panic calls produced in such situations in the wild.
• Finally, the majority of alarm calls produced in response to faecal presentations resembled the lowurgency recruitment calls (Fig. 1 ) elicited in response to olfactory cues in the wild.

Olfactory Predator Recognition

• Low-urgency recruitment calls produced by captive meerkats in response to faecal presentations differed in their fine acoustic structure from those given in similar contexts in the wild.
• The analysis of variance revealed statistically significant differences for five of the included call parameters.
• Captive meerkats produced longer calls with a higher fundamental frequency and first harmonic, more energy located at lower frequencies and a higher amplitude ratio than wild individuals.
• Because some of the calls from captive individuals looked spectrographically similar to medium-urgency terrestrial calls given in the wild, the authors included a set of these calls (N calls = 10) in the DFA to see how they classified.
• Classification results from the discriminant function analysis on low-urgency recruitment calls produced in response to carnivore faeces in captivity (cr, N calls = 10) and hair samples of the African wildcat in the wild (wr, N calls = 10).

Discussion

• All alarm calls that have been documented in wild meerkats (Manser 1998 (Manser , 2001) ) were produced by captive meerkats on one or several occasions.
• This suggests that captive meerkats exhibit the same vocal repertoire of alarm calls as wild meerkats.
• Behaviours which are essentially independent of experience may change slowly following the loss of predators (Coss 1999; Blumstein et al. 2000; Blumstein 2002 ).
• The results from their faecal presentations suggest that captive meerkats growing up in a relatively predator-free environment can still recognize and respond adaptively to odours signaling the presence of potential predators, in a similar fashion to wild individuals (Manser 2001) .
• Slight deprivation might explain why captive individuals produced calls with a high fundamental frequency typical of young individuals and those of small body size (Hammerschmidt et al.

Figures

Figure 2. The time that captive meerkats spent (a) inspecting stimuli and (b) calling in 284 response to presentations of carnivore and herbivore faeces. Because of low sample size, 285 statistical analysis was only conducted on inspection time. Sample sizes reflect the number of 286 groups. 287 288

Figure 1. Examples of low-urgency recruitment calls produced by wild and captive meerkats 180 in response to olfactory predator cues. 181 182

Table 2. Description of acoustic parameters included in the analysis of low-urgency 201 recruitment calls emitted in captivity and in the wild (measured by LMA; see Schrader & 202 Hammerschmidt 1997). 203 204

Figure 3. Classification results from the discriminant function analysis on low-urgency 312 recruitment calls produced in response to carnivore faeces in captivity (cr, Ncalls = 10) and hair 313 samples of the African wildcat in the wild (wr, Ncalls = 10). Medium-urgency terrestrial calls 314 produced by wild meerkats in response to mammalian predators were also included (wt, Ncalls 315 = 10). 316 317 318 Discussion 319 All alarm calls that have been documented in wild meerkats (Manser 1998, 2001) were 320 produced by captive meerkats on one or several occasions. This suggests that captive 321 meerkats exhibit the same vocal repertoire of alarm calls as wild meerkats. That the amount of 322 calling differed between populations may simply reflect differences in the time spent 323 observing each population or variation in the presence of disturbances. Captive meerkats not 324 only produced alarm calls, but produced them in contexts resembling those in the wild. 325 Although calls often elicited by raptors in the wild were regularly evoked by stimuli such as 326 airplanes, this may not be surprising given the presumably lesser likelihood of encountering 327 real threats. Besides, wild meerkats occasionally alarm to planes (Manser, M. B., personal 328 observation). Our observations are similar to those on some non-human primates, where 329 captive populations use the same or very similar alarm-call types as wild populations (Fichtel 330 & van Schaik 2006; Coss et al. 2007) but occasionally alarm to harmless stimuli (Brown et al. 331 1992). 332 There are a number of explanations to why alarm calling could have been retained in 333 captive meerkats. First, it is possible that the presence of some predatory stimuli may be 334

Table 1. The most common alarm-call types emitted by wild meerkats (for details, see Manser 2001).

Full text

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Year:2007
PersistenceofAlarm-CallBehaviourintheAbsenceofPredators:A
ComparisonBetweenWildandCaptive-BornMeerkats(Suricatasuricatta)
Hollén,LI;Manser,MB
Abstract:Performingcorrectanti-predatorbehaviouriscrucialforpreytosurvive.Butaresuchabilities
lostinspeciesorpopulationslivinginpredator-freeenvironments? Howindividualsrespondtotheloss
ofpredatorshasbeenshowntodependonfactorssuchasthedegreetowhichanti-predatorbehaviour
reliesonexperience,thetypeofcuesevokingthebehaviour,thecostofexpressingthebehaviourand
the number ofgenerations underwhich therelaxed selectionhas taken place.Here weinvestigated
whethercaptive-bornpopulationsofmeerkats(Suricatasuricatta)usedthesamerepertoireofalarmcalls
previouslydocumentedinwildpopulationsandwhethercaptiveanimals,aswildones,couldrecognize
potentialpredatorsthrougholfactorycues.Wefoundthatallalarmcallsthathavebeendocumented
inthewildalsooccurredincaptivityandweregiveninbroadlysimilarcontexts. Furthermore,without
priorexperienceofodoursfrompredators,captivemeerkatsseemedtodistinguishbetweenfaecesof
potentialpredators(carnivores)andnon-predators(herbivores).Despiteslightstructuraldierences,the
alarmcallsgiveninresponsetothefaeceslargelyresembledthoserecordedinsimilarcontextsinthe
wild.Theseresultsfromcaptivepopulationssuggestthatdirect,physicalinteractionwithpredatorsis
notnecessaryformeerkatstoperformcorrectanti-predatorbehaviourintermsofalarm-callusageand
olfactorypredatorrecognition.Suchbehaviourmayhavebeenretainedincaptivitybecauserelatively
littleexperienceseemsnecessaryforcorrectperformanceinthewildand/orbecauseoftherecencyof
relaxedselectiononthesepopulations.
DOI:https://doi.org/10.1111/j.1439-0310.2007.01409.x
PostedattheZurichOpenRepositoryandArchive,UniversityofZurich
ZORAURL:https://doi.org/10.5167/uzh-282
JournalArticle
AcceptedVersion
Originallypublishedat:
Hollén,LI;Manser,MB(2007).PersistenceofAlarm-CallBehaviourintheAbsenceofPredators:
AComparisonBetweenWildandCaptive-BornMeerkats(Suricatasuricatta).Ethology,113(11):1038-
1047.
DOI:https://doi.org/10.1111/j.1439-0310.2007.01409.x

1
Ethology (2007), 113: 1038-1047 1
doi: 10.1111/j.1439-0310.2007.01409x 2
3
4
Persistence of alarm-call behaviour in the absence of predators: a 5
comparison between wild and captive-born meerkats (Suricata suricatta) 6
7
8
Linda I. Hollén & Marta B. Manser 9
10
Zoologisches Institut, Universität Zürich, Zürich, Switzerland 11
12
Abstract 13
Performing correct anti-predator behaviour is crucial for prey to survive. But are such abilities 14
lost in species or populations living in predator-free environments? How individuals respond 15
to the loss of predators has been shown to depend on factors such as the degree to which anti-16
predator behaviour relies on experience, the type of cues evoking the behaviour, the cost of 17
expressing the behaviour and the number of generations under which the relaxed selection has 18
taken place. Here we investigated whether captive-born populations of meerkats (Suricata 19
suricatta) used the same repertoire of alarm calls previously documented in wild populations 20
and whether captive animals, as wild ones, could recognize potential predators through 21
olfactory cues. We found that all alarm calls that have been documented in the wild also 22
occurred in captivity and were given in broadly similar contexts. Furthermore, without prior 23
experience of odours from predators, captive meerkats seemed to distinguish between faeces 24
of potential predators (carnivores) and non-predators (herbivores). Despite slight structural 25
differences, the alarm calls given in response to the faeces largely resembled those recorded in 26
similar contexts in the wild. These results from captive populations suggest that direct, 27
physical interaction with predators is not necessary for meerkats to perform correct anti-28
predator behaviour in terms of alarm-call usage and olfactory predator recognition. Such 29
behaviour may have been retained in captivity because relatively little experience seems 30
necessary for correct performance in the wild and/or because of the recency of relaxed 31
selection on these populations. 32
33
34
Introduction 35
Predation is a major selective force leading to numerous behavioural and morphological 36
adaptations in prey (Lima & Dill 1990). Many species, for example, produce alarm calls to 37

2
warn conspecifics of impending danger (Klump & Shalter 1984). Several mammalian studies 38
have shown that young individuals need to learn about alarm calls and that the amount of 39
exposure to these calls can affect the speed of such learning (e.g. Hauser 1988; Mateo 1996; 40
Ramakrishnan & Coss 2000; Hanson & Coss 2001; McCowan et al. 2001; Hollén & Manser 41
2006; Hollén, L. I., Clutton-brock, T. & Manser, M. B., unpubl. data). Few studies have, 42
however, considered whether regular encounters with predators are necessary to maintain 43
appropriate anti-predator behaviours within populations (but see Brown et al. 1992; Fichtel & 44
Hammerschmidt 2003; Fichtel & van Schaik 2006). Moreover, in several species, alarm calls 45
are known to provide far more information than a simple warning. They may, for example, 46
indicate the type of predator and/or the urgency of the threat (reviewed in Macedonia & Evans 47
1993; Manser 2001; Coss et al. 2007). It remains unclear whether a lack of relevant 48
experience leads to elimination of alarm-call behaviour, some alteration in the subtleties of 49
sophisticated systems, or has no discernible effect at all. 50
Species which have become isolated from predators, either on islands or in captivity, 51
provide powerful opportunities to investigate the importance of predator experience on alarm-52
call behaviour. Although such isolation may reduce the selection pressure, anti-predator 53
behaviour is not inevitably lost (e.g. Coss 1991, 1999; Blumstein et al. 2000; Blumstein & 54
Daniel 2002). How animals respond to isolation from predators can, for example, depend on 55
the degree to which anti-predator behaviour relies on experience (Coss 1999; Blumstein 56
2002), the cost of performing such behaviour (Magurran 1999; Berger et al. 2001; Blumstein 57
et al. 2006) and the type of cues evoking the behaviour (Blumstein et al. 2000). Experience-58
independent behaviour, behaviour with low production costs and behaviour evoked by cues 59
with convergent features may be more likely to persist in predator-isolated environments. 60
However, the persistence of behaviour will also depend on the number of generations under 61
which the relaxed selection has taken place (Coss 1999). Because of the complexity of the 62
genetic-epigenetic processes leading to the expression of predator recognition and appropriate 63
anti-predator behaviour, a few generations of relaxed selection will not alter any innate 64
perceptual properties. 65
Meerkats (Suricata suricatta) provide an ideal opportunity to investigate the 66
importance of predator experience on the maintenance of alarm-call behaviour because they 67
are found in numerous zoos and their anti-predator behaviour has been extensively studied in 68
the wild (Manser 2001; Manser et al. 2001; Hollén & Manser 2006, 2007; Hollén, L. I., 69
Clutton-brock, T. & Manser, M. B., unpubl. data). They are cooperatively breeding 70
mongooses which naturally inhabit arid regions of southern Africa (Clutton-Brock et al. 71

3
1999a), where they are preyed on by a variety of raptors, mammals and snakes (Clutton-72
Brock et al. 1999a,b). They exhibit a sophisticated alarm-call system, consisting of calls given 73
only in response to specific predator types (for example, raptors) and calls that are unrelated 74
to a single predator type (for example, moving animals) (Manser 2001). Additionally, the 75
acoustic structure of predator-specific calls simultaneously encodes information about the 76
signaller’s perception of response urgency: calls given on spotting a close predator (termed 77
high urgency) are structurally different from those given to the same predator encountered at 78
intermediate (medium urgency) and far (low urgency) distances (Manser 2001). Calls of 79
different urgency do not fall into discrete categories, but rather grade from a harmonic into a 80
noisy structure as the level of urgency increases (Manser 2001). 81
In this study, we investigate whether meerkats from European zoos produce alarm 82
calls in response to natural visual cues and experimentally presented olfactory cues (faeces). 83
We use these two cue types to assess what type of predatory experience might be important 84
for the maintenance of alarm-call behaviour: captive meerkats are likely to have no 85
experience of predatory olfactory cues, but might have encountered some visual predatory 86
threats (albeit from different species to those usually seen in the wild). We assess whether the 87
repertoire of calls found in the wild is present in captivity, and whether the acoustic structure 88
of alarm calls produced by captive meerkats, and the context in which they are given, matches 89
that for wild individuals. 90
91
92
Methods 93
94
Study sites and populations 95
Between August 2004 and December 2005, we studied six captive populations of meerkats 96
living in zoos in Switzerland (Basel), Germany (Cologne, Karlsruhe, Hannover, Osnabrück) 97
and Ireland (Dublin). All individuals present in these populations were born in captivity and 98
the number of generations of captive living ranged from one to five. Groups had access to 99
both outdoor (range: 30-480 m
2
, mean = 178 m
2
) and indoor (range: 1-40 m
2
, mean = 19 m
2
) 100
enclosures. All outdoor encloses had a clear view of the sky. The substrate in the outdoor 101
enclosures composed a mix of sand and mud, and the meerkats could therefore dig natural 102
burrows and holes themselves. Additional structures such as hollow tree trunks and termite 103
mounds were also present, providing ecologically natural shelters. The outdoor enclosures 104
were directly alongside walking paths for visitors but obscured by glass or stone walls (at 105

4
least 1 m in height). Dogs were not allowed in any of the zoos, but in Cologne zoo a keeper 106
once walked past with a dog. Some of the groups were close to other carnivore enclosures 107
(20-30 m), whereas others were more than 100 m away and out of visual contact. Group size 108
varied between six and 16 individuals, which is within the natural range (Clutton-Brock et al. 109
1999a). Except for one zoo, where individuals were distinctly marked with hair dye, 110
individual identification was not feasible. All individuals from which we collected data were 111
of adult age (> 12 mo, Clutton-Brock et al. 1999b). 112
Alarm-call behaviour in wild meerkats was studied at the Kuruman River Reserve in 113
the South African part of the Kalahari Desert (26º58´S, 21º49´E) (study site details provided in 114
Clutton-Brock et al. 1999a). At this study site, a range of five to 13 (varying between years) 115
wild but well-habituated (close observation within 1 m) groups, varying in size from three to 116
50 individuals, have been followed since 1995. Each animal was marked for individual 117
identification with hair dye or hair cuts applied to their fur unobtrusively during basking at the 118
morning sleeping burrow. The exact age and life-histories of all individuals except a few 119
immigrant males were known because they had been monitored since birth. Although their 120
alarm-call system has been described in detail elsewhere (Manser 1998, 2001), table 1 provides 121
an overview of the common call types and the contexts in which they are given. 122
123
Table 1. The most common alarm-call types emitted by wild meerkats (for details, see
Manser 2001).
* Occasionally also elicited by vultures
Call type Urgency Context
Specific Low aerial Low Raptors* far away (> 500 m)
Medium aerial Medium Raptors* at medium distances (100-500 m)
High aerial High Raptors closeby (< 100 m)
Low terrestrial Low Mammals far away ( > 200 m)
Medium terrestrial Medium Mammals at medium distances (20-200 m)
High terrestrial High Mammals closeby (< 20 m)
Low recruitment Low Deposits such as faeces or hair samples of
predators or foreign meerkats
High recruitment High Snakes/deposits of predators (seldom to
deposits of foreign meerkats)
General Alert Low Non-dangerous birds closeby, raptors far
away, terrestrial animals
Moving animal Low/High Animals moving (raptors, mammals, non-
dangerous birds, foreign meerkats)
Barking High Perched raptors (< 500 m), raptors circling
above, mammals very closeby
Panic High Sudden movements in close proximity
124
125
126

Frequently asked questions

Q1. What are the contributions in "Persistence of alarm-call behaviour in the absence of predators: a comparison between wild and captive-born meerkats (suricata suricatta)" ?

Here the authors investigated whether captive-born populations of meerkats ( Suricata suricatta ) used the same repertoire of alarm calls previously documented in wild populations and whether captive animals, as wild ones, could recognize potential predators through olfactory cues. Furthermore, without prior experience of odours from predators, captive meerkats seemed to dist inguish between faeces of potential predators ( carnivores ) and non-predators ( herbivores ). These results from captive populations suggest that direct, physical interaction with predators is not necessary for meerkats to perform correct anti-predator behaviour in terms of alarm-call usage and olfactory predator recognition.